Brown Rot Strikes Prunus Fruit: an Ancient Fight Almost Always Lost

Brown rot strikes Prunus fruit: an ancient fight almost always lost Leandro de Oliveira-Lino, Igor Pacheco, Vincent Mercier, Franco Faoro, Daniele Bassi, Isabelle Bornard, Bénédicte Quilot-Turion

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Leandro de Oliveira-Lino, Igor Pacheco, Vincent Mercier, Franco Faoro, Daniele Bassi, et al.. Brown rot strikes Prunus fruit: an ancient fight almost always lost. Journal of Agricultural and Food Chem- istry, American Chemical Society, 2016, 64 (20), pp.4029-4047. 10.1021/acs.jafc.6b00104. hal- 01594477

HAL Id: hal-01594477 https://hal.archives-ouvertes.fr/hal-01594477 Submitted on 26 Sep 2017

HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Version postprint always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Review J. Agric.FoodChem. Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost Just Accepted or consequences arising from the use of information contained in these “Just Accepted” and manuscripts. ethical guidelines that apply to changes the to journal the pertain. manuscript text ACS and/or cannot graphics be which could Accepted” held Web site and affect published responsible as an content, ASAP article. Note for that and technical editing may all introduce errors minor legal disclaimers in the journal. After a manuscript is technically edited and formatted, it will be removed from to the authors. “Just Therefore, the “Just Accepted” Web site may not include all articles offered service optional an is Accepted” “Just (DOI®). Identifier Object Digital the by citable and readers that will be published all to accessible are They record. of version official the considered be not should but reviewed, peer fully been have manuscripts Accepted” “Just abstract. HTML an by accompanied format PDF in full in appear dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts Society provides “Just Accepted” online prior to technical as editing, formatting for publication and author proofing. a The American Chemical free service “Just Accepted” manuscripts have to been peer-reviewed and accepted the for publication. They are research posted community to expedite the Brown rotstrikesPrunusfruit:anancientfightalmostalwayslost , Just AcceptedManuscript Leandro OliveiraLino,IgorPacheco,VincentMercier,Franco Faoro, IsabelleBonard,DanieleBassi,andBenedicteQuilot Comment citer cedocument: Downloaded fromhttp://pubs.acs.orgonMay9,2016

• DOI:10.1021/acs.jafc.6b00104 Subscriber accessprovidedbyINRAInstitutNationaldelaRechercheAgronomique of their duties. produced byemployeesofany Commonwealth realmCrowngovernment inthecourse However, nocopyrightclaim ismadetooriginal U.S.Governmentworks, orworks Published byAmerican ChemicalSociety.Copyright©American ChemicalSociety. Society. 1155Sixteenth StreetN.W.,Washington,DC20036 Journal ofAgricultural andFoodChemistryispublishedby theAmericanChemical • PublicationDate(Web):02May2016 Version postprint Page 1of72 always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 18 18 17 16 15 14 13 12 11 10 9 9 8 7 6 5 4 3 2 1

1 * Corresponding Author: Igor Pacheco. Email: igor.p Email: Igor Pacheco. Author: Corresponding * § France Montfavet, F84140 6 Milano, Italy 2, 20133 Celoria ViaMilano, 5 France MarcellèsValence Saint 26320 4 3 F84000, France 2 Brazil. Brown rot strikesrotBrown iatmno i cez Arre Abetl, Univ Ambientali, e Agrarie Scienze di Dipartimento INRA, Intégrées, Recherches de Unité Expérimentale Brazil, of Education of Ministry Foundation, CAPES INRA, Unité de Pathologie Végétale, UR0407, Domaine UR0407, Végétale, Pathologie de Unité INRA, Mac Líbano5524, El Av. Chile. Universidad INTA, de equally contributing authors authors equally contributing INRA, Leandro Oliveira LinoLeandro Faoro

UR1052 Génétique et Amélioration des Fruits et Légu et Fruits des Amélioration et Génétique UR1052 5 , Daniele Bassi Daniele , Comment citer cedocument: Journal ofAgriculturalandFoodChemistry Prunus ACS Paragon PlusEnvironment 1,2,§ 5

, Isabelle Bornard, Isabelle , Igor Igor Pacheco, fruit:ancientan fight almost always lost 1 3,5§,* 6 , Bénédicte Quilot-Turion, , Vincent ,Mercier [email protected] [email protected] Brasília DF 70040020, 70040020, DF Brasília ul, Santiago, Chile. Chile. ul,Santiago, Domaine Gotheron, F Gotheron, Domaine rià el Sui di Studi degli ersità St. Maurice, BP 94, BP Maurice, St. mes, Avignon, mes, 4 , Franco , Franco 2 . Version postprint always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 24 24 23 22 21 20 19 40 40 39 38 37 36 35 34 33 32 31 30 29 28 27 26 25

edd o utial lmt hs ies: h patho the disease: this limit sustainably to needed orch the in occurrence its influences significantly of aspects basic There period. postharvest the during mainly losses drama the to due market fruit stone the for problem Abstract Keywords a currently related resistance. to BR understand mechanisms information the compile comprehensively in sources resistance the on report of mechanisms fo BR, causing agents of distribution and diversity this of purpose the Thus, protocols. and strategies different evaluate studies thi Summarizing physical). chemical, genetic, (e.g. d of range wide a exploring increased, recently has on residues reduce and treatments chemical decrease importa becomes problem this Solving perish. models resistance BR of and most pesticides to resistance Bon o (R cue by caused (BR) rot Brown : : : Monilinia Comment citer cedocument: Monilinia Monilinia Journal ofAgriculturalandFoodChemistry spp., brown rot, rot, brown spp., ACS Paragon PlusEnvironment spp. infection both of the fungi and of the fruit, the of and fungi the of both infection spp.

Monilinia spp. infection, which indicates that environment environment that indicates which infection, spp. and Prunus Prunus 2 Monilinia Prunus , QTL QTL , germplasm. In this review, we we review, this In germplasm. spp., has been an economic economic an been has spp., model species, with diverse diverse with species, model s information is difficult, as difficult, is information s ard. However, progress is is progress However, ard. research programs in plant programs research cusing on the biochemical biochemical the on cusing tic losses, with the biggest biggest the with losses, tic review is to present the the present to is review isease control strategies strategies control isease is much literature about about literature much is gen is able to develop develop to able is gen t u t te ed to need the to due nt ri. hs research Thus, fruit. albe o better to vailable and Page 2of72 Version postprint Page 3of72 always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 45 45 44 43 42 41 64 64 63 62 61 60 59 58 57 56 55 54 53 52 51 50 49 48 47 46

hn (07Tn, h Uie Sae (.Mo) Ital (2.9MTon), States United the (10.7MTon), China the for countries important most five The apricot. almond, cultivated the including members, important Introduction 1 period of incidence, extending from bloom to posth to bloom from extending incidence, of period p phenological host sensitive most the being latter imma in BR and blight, twig blight, blossom causing fruits stone of disease ( rot brown Rosaceaeous), other advisedin Chinahave been applications humans for toxicity and use pesticide in re decreases Centres, IPM Regional of creation the with input re to order in IPM promoted strongly has government mandatory as (IPM) Management Pest Integrated which 2009/128/EC Directive European the of release in stricter become has use fungicide of residu regulation reduced with fruit fresh of demand the since cruci a is point latter This product. final quality con be to has pests of range broad the addition, In environmenta different their to according fruit, of (0.8MTon) and Greece (1.4MTon) Among the plethora of pathogenic agents attacking attacking agents pathogenic of plethora the Among Different cropping practices are employed for the p the for employed are practices cropping Different genus The Comment citer cedocument: Prunus Journal ofAgriculturalandFoodChemistry 8 . . has hundreds of species with some economically economically some with species of hundreds has ACS Paragon PlusEnvironment Monilinia

1 spp. are able to infect various plant organs, organs, plant various infect to able are spp. . . R i te cnmcly ot important most economically the is BR) 3 6 , Brazil and other countriesother and Brazil , al issue in current fruit cropping, cropping, fruit current in issue al l and nutritional requirements. requirements. nutritional and l production of these fruits are are fruits these of production 2,3 ture and mature fruits, the fruits, mature and ture . In the United States, the the States, United the In . hase. The relatively long long relatively The hase. peach, plum, cherry and and cherry plum, peach, ret h utpiiy of multiplicity the arvest, duce chemical pesticide pesticide chemical duce U onre, fe the after countries, EU rle t rah high a reach to trolled roduction of this variety this variety of roduction 4,5 sulting in progressive progressive in sulting al quantities and the the and quantities al niae te s of use the indicates y (1.9MTon), Spain Spain (1.9MTon), y . Reduced pesticide pesticide Reduced . Prunus rp (and crops 7 . Version postprint always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 70 70 69 68 67 66 65 88 88 87 86 85 84 83 82 81 80 79 78 77 76 75 74 73 72 71

States, of value yearly market fruit the in losses and unavoidable severe, in result resistance, host and agents BR some in resistances fungicide diverse spr disease favouring factors cropping and climatic international collaborative initiatives for new cul new for initiatives collaborative international as included been have These appli control. BR for methods of requirements reduced with varieties new of resistan fruit enhance and characterize to order in publications recent in discussed and topics These agents). biochemicalphysical harvest 12,13 strategies control alternative emerging and with control related aspects as well as BR, of epidemiology fructicola, fungicider many are there as cropping, fruit stone sustainability to lead but seasons, humid in damage necess are applications Fungicide methods. chemical temperature. at room infection nec and peaches of 60% over of losses in result can crops apricot and peach for AUD million production plum and cmail wt IM n ognc giutr (biol agriculture organic and IPM with compatible , o vi tee damages, these avoid To yearly losses are estimated to be 170 million USD million 170 be to estimated are losses yearly see below). An important research field has been d been has field research important An below). see Comment citer cedocument: Monilinia Journal ofAgriculturalandFoodChemistry 10 ad n utai yal lse ae siae a 1 at estimated are losses yearly Australia in and ; ACS Paragon PlusEnvironment oss s , tosn mlin Euro million thousand 1,7 is losses

7 . According to Martini and Mari Mari and Martini to According . Monilinia 14,9 4 . Significant efforts are being invested invested being are efforts Significant . 11 spp. diseases are controlled by by controlled are diseases spp. . Under laboratory conditions, BR BR conditions, laboratory Under . tivar development around the the around development tivar ce to BR for the generation the for BR to ce ssat tan ( strains esistant (e.g. tree management) management) tree (e.g. sometimes unpredictable unpredictable sometimes are thoroughly reviewed thoroughly are challenges in pome and pome in challenges a, h ocrec of occurrence the ead, important objectives of objectives important the poor availability of availability poor the tarines after 5 days of of days 5 after tarines ain f exogenous of cation traditional chemical chemical traditional ary to diminish BR BR diminish to ary ogic agents, post post agents, ogic for peach, cherry cherry peach, for 9 , the worldwide worldwide the , edicated to the the to edicated ; in the United United the in ; Monilinia

Page 4of72 Version postprint Page 5of72 always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 110 110 109 108 107 106 105 104 103 102 101 100 112 112 111 93 93 92 91 90 89 99 99 98 97 96 95 94 soyoa Cas etoyee, re Helioteliale Order Leotiomycetes, Class Ascomycota,

eiwd rils cnrsinl cs ad unpublis and acts, congressional articles, reviewed compi we aim, this For BR. to resistance conferring initiative. an project European Breedomics Fruit as such world, described to be important pathogens of Ericaceae: Ericaceae: of pathogens important be to described fructigena Honey; Winter) fruit stone and pome to pathogenic are that species of families Ericaceae Genus Sclerotiniaceae, Taxonomy 2.1 2 resistance BR of the dissection for genetic knowledge generating enhancing at aimed programs breeding main the fruit. in resistance BR for factors host molecular discuss and development infection of steps of start the for points representing features fruit descript brief of distribution geographic a and morphology After topic. this on working years Sclerotinia n h peet review, present the In Monilinia Of the 35 species of the genus genus the of species 35 the Of belongi fungi polytrophic are BR causing agents The Aehl & uln) Honey Ruhland) & (Aderhold that produce moniloid conidia and pseudosclerotia. pseudosclerotia. and conidia moniloid produce that spp. fungi cause brown rot brown fungispp. cause Comment citer cedocument: oiii laxaMonilinia Journal ofAgriculturalandFoodChemistry 15,16 . The generic name name generic The . ACS Paragon PlusEnvironment Monilinia

we will focus on stone fruit characteristics characteristics fruit stone on focus will we (Aderhold & Ruhland) Honey and and Honey Ruhland) & (Aderhold . They attack members of the Rosaceae and and Rosaceae the of members attack They . 5 Monilinia 17 Monilinia . At least two species have been been have species two least At . Monilinia infection. We will examine the the examine will We infection. To finish, we will describe the the describe will we finish, To oe, he ae h main the are three Honey, fruit BR resistance. BR fruit led information from peer from information led species, we will focus on on focus will we species, includes those members members those includes s: s: d ROSBREED American American ROSBREED d hed data obtained over over obtained data hed ion of the taxonomy, taxonomy, the of ion Monilinia fructicolaMonilinia oiii vaccinium- Monilinia biochemical and and biochemical ng to the Phylum Phylum the to ng in stone fruit, fruit, stone in s, Family Family s, Monilinia Monilinia

(G. Version postprint always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 135 135 134 133 132 131 130 129 128 127 126 125 124 123 122 121 120 119 118 117 116 115 114 113

ogune on i te rnhn tplge o hos of topologies branching the in found hosts congruence Ericaceae attacking Disjunctoriae and at Junctoriae, consistent: is sections two in genus of sequences rRNA in cranberry of cottonball causing corymbosi additional inoculum. inoculum. additional p give may lignification, endocarp the after fruit, fruit mature and immature of infection for inoculum tissue infected on form Conidia response. host a as that canker twig a of formation the with continues t into down and peduncle the into spreads infection typica blossoms of infections The cultivars. almond cr the destroy can it but crops, fruit in load crop blos general In conditions. temperature and wetness germ and tissues, host susceptible to rain and wind prod which floor, The (ascospores). spores and (apothecia) structures orchard the on or (conidia) spore fruiting asexual produce which tree, the on either of cycle overwint are disease spring the The in sources inoculum Primary onwillwe focus In this review, cos of hypothesis the suggest to lead phylogenies, asn mmy er o blueberry of berry mummy causing Comment citer cedocument: Journal ofAgriculturalandFoodChemistry Monilinia ACS Paragon PlusEnvironment

Monilinia Monilinia and 19 . According to phylogenetic analyses based based analyses phylogenetic to According . Sclerotinia 6 pce i rpeetd n iue 1. Figure in represented is species spp. and BR in stone fruits. fruits. inandstone BR spp. species, the separation of the of separation the species, op at flowering in susceptible susceptible in flowering at op structure (sporodochia) and and (sporodochia) structure 18 lly remain attached and the the and attached remain lly

15,20,21 peciation between them them between peciation often develops a gumdrop gumdrop a develops often lace to conidia, providing providing conidia, to lace 22 and and akn Rsca hosts, Rosaceae tacking and serve as secondary secondary as serve and spores are dispersed by dispersed are spores . Infections on immature immature on Infections . ering BR fruit mummies mummies fruit BR ering som blight reduces the the reduces blight som inate under favourable favourable under inate he twig. The infection infection The twig. he , moreover, partial partial moreover, , uce sexual fruiting fruiting sexual uce oiii oxycocci Monilinia s n pathogen and ts 15 . .

Page 6of72 Version postprint Page 7of72 always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 159 159 158 157 156 155 154 153 152 151 150 149 148 147 146 145 144 143 142 141 140 139 138 137 136

. fructicola M. co in disposition and tufts, conidiospores average) fructigena in fruit in monilioses of agents three the between of Differentiation 2.2 respectively. respectively. laxaM. ave On reported. are species the among size s conidia useful them makes simplicity their and 1920 since metho These morphology. tube germ and size conidial fruit peach on laxaM. for found was PDA on rate growth – (20 observed were species three the between rates Dif colonies. radial fragmented observe to possible w margins, lobbed with mycelium of rings concentric 22 at (PDA) agar and dextrose potato with (Figure 2). required is techniques and differentiation the However surface. infected whole mm 0,5 than less tufts conidiospores greenishgrey spots. black 10% and tufts conidiospores . fructiculaM. Studies to identify the the identify to Studies id to possible is it eye, naked with observation By respectively. However, However, respectively. s mle cmae to compared smaller is a clu rnig rm ht t lgt eg, larg beige, light to white from ranging colour has M. fructigenaM. has browncoloured, medium size (1 mm on average) average) on mm (1 size medium browncoloured, has Comment citer cedocument: 8 I clue eim t s osbe o nls chara analyse to possible is it medium culture In . a smtms e ifcl ad h ue f molecula of use the and difficult be sometimes may Journal ofAgriculturalandFoodChemistry Monilinia ACS Paragon PlusEnvironment produces one or two germ tubes per conidium, and and conidium, per tubes germ two or one produces

Monilinia species species M. laxaM. M. fructicolaM. . fructigenaM. species reported that, in culture medium medium culture in that, reported species 7 showed the biggest lesion growth rate rate growth lesion biggest the showed . laxaM. o C, C, , followed by followed , , 13x9 m and 22x12 m, m, 22x12 and m 13x9 , . laxaM. ncentric circles in the fruit. fruit. the in circles ncentric ferences in colony growth growth colony in ferences can be distinguished by by distinguished be can on average that cover the the cover that average on in fruit between between fruit in orchard conditions conditions orchard hile in in hile rage the conidia size of size conidia the rage till till entify the differences differences the entify 5C. h highest The 25ºC). is characterized by by characterized is s ae en used been have ds 22 M. fructigenaM. M. fructigenaM. Dfeecs in Differences . (. m on mm (1.5 e tr as cters . laxaM. 23 and and it is is it . M. M. r r

rpsd h suy f h sal u ui o ribosom of unit sub small the of study the proposed detect and identify to reli methods develop to used been have PCR) Reaction, Chain conidium laxaM. associated with European BR of pome fruits fruits pome of BR European with associated and of distribution range Host 2.3 species of r host and distribution geographical the diversity describing molecular and morphological about studies fruit stone and detect and identification for useful be to reported fruit cherry in infections fruit stone of infections fruit quiescent on addition, a are (AFLP) polymorphism length fragment amplified microsatellites speciesspecific on al et of subunits small 18S the between sequence spacers, transcribed for protocols differentiate 8 . fructigenaM. Several molecular biology techniques (mostly based based (mostly techniques biology molecular Several reported a detection and identification method of of method identification and detection a reported and molecular techniques have been developed for specie for developed been have techniques molecular 8 . Monilinia Monilinia M. fructicolaM. Monilinia Monilinia Comment citer cedocument: 32 . Journal ofAgriculturalandFoodChemistry Some of these approaches have set the basis for sev for basis the set have approaches these of Some s n cnmcly motn Bgn that BRagent important economically an is that caused BR of stone and pome fruits, fruits, stonepome and of BR caused that genes, have been proposed been have genes, isolates from the three major species. Many PCR PCR Many species. major three the from isolates spp. identification, based on the comparison of in of comparison the on based identification, spp. ACS Paragon PlusEnvironment isolates consistently produce only one germ tubep germ one only produce consistently isolates 31

. In Banks et al al et Banks In . Monilinia Monilinia 8,27 8 . Identification methods based on on based methods Identification . pce. utn n Brown and Fulton species. 30

spp. ad o te al dtcin of detection early the for and , 15,36 32 , monoclonal antibodies are are antibodies monoclonal , ion of of ion

. However, its occurrence in occurrence its However, . 22,25,26 ne f h tre main three the of ange Monilinia Monilinia . Ma et al et Ma . lso reported reported lso n te 8 rDNA 28S the and of of l N (DA to (rDNA) DNA al able and sensitive sensitive and able in the Polymerase Polymerase the in 33,34,35 Monilinia s identification identification s spp. in pome pome in spp. fungi based based fungi . has been been has 27 and Hu Hu and 28,29 spp., spp., ternal ternal eral eral In . 24 er er , Page 8of72 Version postprint Page 9of72 always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 207 207 206 205 204 203 202 201 200 199 198 197 196 195 194 193 192 191 190 189 188 187 186 185 184 Asia, North and South America, New Zealand and Aust and Zealand New America, South and North Asia,

United States the of regions different in reported also been has stone of BR and China Europ in documented well been also has fruits stone extrapolated to the other members of of otherthe members extrapolated to from acquired knowledge the of part that expect may fructigena and grapes example cherry Cornelian distribution, wide E to pathogen the of events introduction recent and fructicola Poland Republic France sp current countries: its to due list pest quarantine European it when 2014, early until pathogen quarantine a was . fructigenaM. The low genetic diversity found in Spanish and Fren and Spanish in found diversity genetic low The fructicolaM. laxaM. These three species share high levels of DNA simila DNA of levels high share species three These 6 . 57

, compared with American or New Zealand diversity, diversity, Zealand New or American with compared , , Slovakia Slovakia , displayed more than 99,1% for the the for 99,1% than more displayed 52 , Slovenia Slovenia , a be hsoial ascae wt uoen blo European with associated historically been has 43,44,45 Comment citer cedocument: 61 36,38 M. fructicolaM. (G.Wint) is the most widely distributed species, o species, distributed widely most the is (G.Wint) xiie 9,% eune iett while identity sequences 97,5% exhibited 60 and dragon fruit dragonfruit and Journal ofAgriculturalandFoodChemistry 58 n ohr ta d nt eog o oaee family, Rosaceae to belong not do that others and , China 48 and pome fruit fruit pome and , Serbia and Spain Serbia and , Hungary , ACS Paragon PlusEnvironment 53 Italy ,

6 and Iran and has been reported to infect other hosts such as such hosts other infect to reported been has 54,55 34 62 , Switzerland Switzerland , Austria (subsequently erradicated) erradicated) (subsequently Austria . . 40,41 Monilinia 46 9 . . 35 . However in the last two decades it it decades two last the in However . . . genus. genus. Cyt b Cyt world, including Brazil including world, 49,50 urope urope gene was removed from the the from removed was

Germany read in the following following the in read one species may be be may species one ralia e ch populations of of populations ch 59 37,38 63 rities. . In addition to its its to addition In . . In this way, we we way, this In . 7,47 . laxaM. Brazil , . In Europe, it it Europe, In . indicates few few indicates M. fructicolaM. sm blight ssom ccurring in in ccurring 51 Czech , and 39 and and 39,42 for for M. M. 56 , , , ,

M. fructigena M. Malus is very well illustrated in Rungjindamai et al et Rungjindamai in illustrated well very is Monilinia A fourth species, species, fourth A In summary, it is no longer relevant to affirm that affirm to relevant longer no is it summary, In lessdistributed other Two ot, ugss rltv wd hs rne f thes of range host wide relative a suggests hosts,

was reported to infect to reported was 64 . Molecular differences between European and Japane and European between differences Molecular . has been recently designated as a new species caus species new a as designated recently been has species have the ability to colonize fruit of virt of fruit colonize to ability the have species Comment citer cedocument: were previously demonstrated, on the basis of the I the of basis the on demonstrated, previously were Journal ofAgriculturalandFoodChemistry 65 . M. polystromaM. ACS Paragon PlusEnvironment . polystromaM. Crataegus pinnatifida pinnatifida Crataegus

Monilinia 66 , Poland , Poland Prunus mumePrunus has been reported to occur in pome and and pome in occur to reported been has Monilinia spp. have been reported to date, among among date, to reported been have spp. 10 10 as cle ‘sai Bon Rot’ Brown ‘Asiatic called (also 57 and Hungary pce ae described. are species in Japan Japan in M. fructigenaM. 70 14 . . . In the same way, the fact fact the way, same the In . the three main main three the uitproducing countries countries uitproducing ded with with ded dwide distribution of of distribution dwide the different BRagents different the al ce similarity analyses analyses similarity ce ean isolates of of isolates ean 68 icant biological and and biological icant 67 72 , and be the causal causal the be and , . . soe a host a showed , ually any ually

8,69 8 M. fructigenaM. ; this species is is species this ; e agents. Few Few agents. e Finally, . se isolates isolates se TS region TS ing BR in in BR ing Monilinia Prunus M. ) is is ) . It . M. M. M. 71 , ,

Page 10of72 Version postprint Page 11of72 always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 254 254 253 252 251 250 249 248 247 246 245 244 243 242 241 240 239 238 237 236 235 234 233 232 255 255 lhuh n ot f h css h fnu penetrates fungus the cases the of most in Although ifrn booi mcaim my e novd n pa in involved be may mechanisms biologic Different growth fruit relation in to Penetration sites 3 isolates. apple between proteins some of expression specific Penetration site may also depend on the development the on depend also may site Penetration encountered frequently most is site which on depend fruit wounded and healthy both infect may that that reported cracks small has fruit the if greater is incidence (Fig microcracks skin preexisting through epiderma entering and cuticle the degrading either by fruits A) 3 (Figure bases, trichoma via or (Figure stomata, wounds, through occur to reported o latent of establishment the after intact surface, able be also may species the of most F), 3 (Figure te infection employed or entrances these on focused T points. entry occurring naturally via only tissue opportunistic an as considered been often has spp. fructicola afte impact, rot fruit and occurrence bight blossom by flowers

As stated before, in this review we only discuss as discuss only we review this in before, stated As For example, the penetration of of penetration the example, For i Baiin utvr ad eetos f peach of selections and cultivars Brazilian in , Monilinia Monilinia M. fructigenaM. Comment citer cedocument: Journal ofAgriculturalandFoodChemistry p. sgetd y n bec o creain betwee correlation of absence an by suggested spp., ACS Paragon PlusEnvironment infects fruit via wounds only, in contrasts to contrasts in woundsonly, via fruit infects

74 M. fructicola fructicola M. . The same way in peach, hyphae infect infect hyphae peach, in way same The . 11 11 r quiescent infections. infections. quiescent r herefore, many studies have have studies many herefore, in immature apricot fruit was was fruit apricot immature in r wounds or r artificial inoculation of of inoculation artificial r 77 fungi that may enter in the the in enter may that fungi ure 3 D and E). Fungus Fungus E). and D 3 ure to penetrate fruit through fruit penetrate to 3 B and C), intact cuticle cuticle intact C), and B 3 . Indeed, infection may may infection Indeed, . sts injuring the fruit first. first. fruit the injuring sts al stage of the fruit. For For fruit. the of stage al by fungal germ tubes. tubes. germ fungal by hgnss f ri and fruit of thogenesis l tissue tissue l pects of fruit infection. infection. fruit of pects using ‘open doors’, doors’, ‘open using and apricot apricot and 73 I fruit, In . 76 . It has been been has It . 75 or directly directly or Monilinia . laxaM. M.laxa M. n n

cmae gn epeso poie otie b mic by obtained profiles expression gene compared , probabl BR, to susceptibility high a in resulting , h scn sae as kon s pt adnn” is hardening”, “pit as known also stage, second The p fertilization, ovule after starts stage first The importa arevery fruit of development of stages The 78 on ta arct wr pntae truh cuticl through penetrated were apricots that found 76,80,81 through lenticels. lenticels. through Comment citer cedocument: . . Journal ofAgriculturalandFoodChemistry ACS Paragon PlusEnvironment Monilinia

spp. spp. 12 12 76,83 . This stage is characterized by by characterized is stage This . y due, in part, to the fact that fact the to part, in due, y pment pment se expression is involved in involved is expression se the highest nutrient content content nutrient highest the ion of phenylpropanoid and phenylpropanoid of ion htsnhtcly active, photosynthetically ty to the pathogen the tyto e of unripe peaches only. only. peaches unripe of e like catechin, epicatechin epicatechin catechin, like the susceptibility to BR BR to susceptibility the cation of the endocarp, endocarp, the of cation le. Sharma and Kaul Kaul and Sharma le. etal fall and ends when when ends and fall etal stance, Guidarelli et al al et Guidarelli stance, 2) RNA samples from from samples RNA 2) odtos by conditions nt to understand the the understand to nt ora aayi of analysis roarray t hsooy and physiology it h sae most stage the e and stomata, stomata, and e 78 . . M. 79

Page 12of72 Version postprint Page 13of72 always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 303 303 302 301 300 299 298 297 296 295 294 293 292 291 290 289 288 287 286 285 284 283 282 281 305 305 304 amnteae gns ad hs uprig pote a supporting thus and genes, jasmonaterelated mature and ripen, enabling quiescent infections to to infections quiescent enabling ripen, and mature maturity. stage This red. to yellow to greenish from changes development. fruit along resistance BR compounds in 75 of penetration Direct t of surface the to pathogen the of adhesion allows allow conditions maturity fruit when cuticle intact appressoria thecuticle of penetration direct Infection by 3.2 growth stage embryoat the latent infections of wo other from differing infections, latent of rates Michailides studies. those in used cultivars and methodology in 85,86,87 diver the across rate infection latent the in shift mesocarp str etc.), acids, organic and compounds phenolic of p (e.g. chemistry surface fruit in changes cuticle, th as such place, take surface fruit the in changes increased this with Associated begin. to infections

woe eoeitd vrepeso rsls n a in results overexpression redoxmediated whose , . However, the results vary among studies, probably studies, among vary results the However, . t h tid tg, h hget el xaso i o is expansion cell highest the stage, third the At fe cnda germination, conidial After Notably, various works in different different in works various Notably, Stone fruits become increasingly susceptible to pat to susceptible increasingly become fruits Stone 75 o sals a aet neto ad ae h penet the ease and infection latent a establish to . . 88 bevd ht i hreig f rns rsne th presented prunes of hardening pit that observed Comment citer cedocument: Journal ofAgriculturalandFoodChemistry Monilinia ACS Paragon PlusEnvironment

spp. is enhanced by its production of cutinases cutinases of production its by enhanced is spp. Monilinia 13 13 Prunus species are able to develop develop to able are species 85,87 se stages of fruit development development fruit of stages se colonization colonization rks reporting a minimum rate minimum a reporting rks roduction of sugars, decline sugars, of roduction . species have observed a a observed have species inning and fracturing of the of fracturing and inning he host during infection during host he ucture and integrity of fruit fruit of integrity and ucture susceptibility, structural structural susceptibility, become active and new new and active become

For instance, Lou and and Lou instance, For ends with physiological physiological with ends bserved and colour colour and bserved ta rl o these of role ntial n increased fungal fungal increased n due to differences differences to due 89 hogens as they they as hogens . This structure structure This . ain f the of ration e lowest lowest e 90 . . Version postprint always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 328 328 327 326 325 324 323 322 321 320 319 318 317 316 315 314 313 312 311 310 309 308 307 306 330 330 329 infection can occur in both pubescent and notpubes and pubescent both in occur can infection basis trichomes the through Infection 3.3 4. chapter given are in process of virulence discuss their function and distribution in dry frui dry in distribution and function their discuss peaches like fruits drupe for especially limited is stomata Infection through 3.4 task. con general drawing and studies between b comparisons surface, fruit of generally, more and, length and variat Large peaches. to compared BR to susceptible peaches onfound mature fructicolaM. directly. more surface fruit reach could spores development, infection of time the reduced brushing entrance fungal cra epidermis in result can fracture ge basis trichome spore to important film” “water of formation the densit high the Indirectly: 2) and fungicide as act exudate Directly: 1) ways: two in fruit the protect controversial remains infection the in trichomes of

A dense layer of trichomes covers the surface of th of surface the covers trichomes of layer dense A The literature about stomata and their function on function their and stomata about literature The mo are nectarines whether clear yet not is Finally, is able to penetrate apricots at hair bases.. Simi bases.. hair at apricots penetrate to able is . fructigenaM. Comment citer cedocument: 92,93 Journal ofAgriculturalandFoodChemistry . Smith Smith . ACS Paragon PlusEnvironment 78,95 in stone fruit fruit stone in

94 showed that removing pubescence by means of means by pubescence removing that showed .

14 14 91 . More details about the infection infection the about details More . Other studies Other t like nuts, capsules and pod and capsules nuts, like t y of trichomes could prevent prevent could trichomes of y fo rcoe ln may gland trichome from s

k rslig n ons for points in resulting ck, Ide, rcoe may trichomes Indeed, . 96 cent peach fruit. The role The fruit. peach cent ions of trichomes density trichomes of ions A aoiy f studies of majority A . etween varieties make make varieties etween rmination. In contrast, contrast, In rmination. suggesting that the the that suggesting clusions a very hard hard very a clusions reproductive organs organs reproductive e peach fruit. The The fruit. peach e lar results were results lar e eitn or resistant re 74 affirmed that affirmed Page 14of72 Version postprint Page 15of72 always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 353 353 352 351 350 349 348 347 346 345 344 343 342 341 340 339 338 337 336 335 334 333 332 331 355 355 354 system; however, fruit stomata are only functional functional only are stomata fruit however, system; exchang gas the in aeration provide stomata stages, functi same the have they that suggests cells guard ontogeny fruit throughout constant remains and fruit the of fruit fresh acting on the skin skin the actingon fresh f the within pressure turgor as growth of forces by wounds cracks and skin Infection through 3.5 wounds. in and stomata, with coincide not did centre lesion Ho cells. guard through was infection primary cases se tangential or radial serial of examination Close reg walled thin the through cell guard a penetrates conditions by infected apricots in observed was cavities whi 4) (Figure early stage. this atsusceptibility factors, the of one be could stomata ins fruitlets early In susceptibility. pathogen for l no may and microcracks of number the to compared permanently open closeor remain develop can stomata fruits, the of development the

97 . They can occur in small numbers or are even restr are even or numbers in small occur Theycan . Cuticular crack is defined as the physical failure physical failure asthe defined crack is Cuticular the into apertures stomatal through invasion Fungal could stomata of number the fruits, peach mature In 74 98 . The authors reported that the fungus enters via t via enters fungus the that reported authors The . . The number of stomata per fruit is determined bef determined is fruit per stomata of number The . Comment citer cedocument: Journal ofAgriculturalandFoodChemistry ACS Paragon PlusEnvironment 100 . Cuticular cracks on nectarine fruit occur duringoccur fruit nectarine oncracks Cuticular .

98 . . 15 15 . fructicolaM. ruit cells or hydration of fruit of hydration or cells ruit 99 ctions showed that in most in that showed ctions tead, the high density of of density high the tead, to a certain extent. Due to Due extent. certain a to ons, as on leaves. In early early In leaves. on as ons, itial invasion was through through was invasion itial . The morphology of the the of morphology The . ion at the stomata pore. pore. stomata the at ion es for the photosynthetic photosynthetic the for es wever, in few cases the cases few in wever, into lenticels and either either and lenticels into of the fruit skin, caused caused skin, thefruit of onger be determinant determinant be onger ch may explain the the explain may ch icted to certain parts parts certain icted to under laboratory laboratory under be insignificant insignificant be he stomata and stomata he substomatal substomatal ore petal fall fall petal ore the the Version postprint always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 379 379 378 377 376 375 374 373 372 371 370 369 368 367 366 365 364 363 362 361 360 359 358 357 356 380 380 such as unbalanced water flux into and out of the f the of out and into flux water unbalanced as such cr fruit to contribute factors Several microcracks. tha weakness of zones provoke and occur can deposit bet lag time a case, this In growth. cell epidermal inter the of speed growth the when fruit of surface stage growth fruit final genotypes genotypes p and peach apricot, on investigated was resistance pres of Effect regions. fruit intact infecting than fru the of regions wounded infecting after obtained reports several in demonstrated as agents, re theof and microcracks amount cultivarspecific significant finding by cherries, in BR and cracking al et Borve However them. of inside fact the despite microcracks, by attraction direct patte anarchic an in microcracks the in accumulate conid germinating that noticed and lenticels around microc and cracks of number significant a observed area surfacethefruit of 10% m which densities, crack cuticular high present can lenticels the around the initiated that shown have skin fruit the of Observations cuticul of absence and strain, cuticle cuticle, the

kn onig ervs h fut f t mi barrie main its of fruit the deprives wounding Skin on studies first the of One 108 Ijrdfut neto dvlpd n l fut wi fruit all on developed infection Injuredfruit . Comment citer cedocument: Journal ofAgriculturalandFoodChemistry 101,102,103 ACS Paragon PlusEnvironment

101 104 . . . Microcracks and cracks can develop on the the on develop can cracks and Microcracks . , (Figure 3D, 3E and Figure 5). Larger fruits fruits Larger 5). Figure and 3E 3D, (Figure , . laxaM. 16 16 106 , demonstrated a clear link between between link clear a demonstrated , penetration in microcracks microcracks in penetration 77,107, acking, often in interactions, interactions, in often acking, ence of skin barrier in BR BR in barrier skin of ence sulting incidence of BR. of incidence sulting ween fruit growth and cutin cutin and growth fruit ween nal cells is more rapid than than rapid more is cells nal ruit, maximal elastic limit of limit elastic maximal ruit, where BR infection rates rates infection BR where that the germ tubs grew grew tubs germ the that it were significantly higher higher significantly were it correlations between the the between correlations ar membrane deposition. deposition. membrane ar lum fruit, to find resistant resistant find to fruit, lum rn and without apparent apparent without and rn ay represent more than than more represent ay ia of of ia racks organized radially radially organized racks cracks are frequently frequently are cracks t may evolve into into evolve may t . laxa M. r to biotic stress stress biotic to r h ut similar quite th tended to to tended 105 , , Page 16of72 Version postprint Page 17of72 always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 403 403 402 401 400 399 398 397 396 395 394 393 392 391 390 389 388 387 386 385 384 383 382 381 As for cracks and microcracks, genetic determinism determinism genetic microcracks, and cracks for As genetic diversity by evaluating 81 peach genotypes genotypes peach 81 evaluating by diversity genetic a et Ogundiwin However, injured. was fruit the when fa resistance that and level flesh the at resist expressed few that suggest observations These species. sam a of genotypes between observed was variability uninjur when contrary, the On species. all in speed (e.g. irrigation and thinning) on their density on their and thinning) (e.g. irrigation eff the demonstrated have studies but investigated, by influenced be may structure but control, genetic a lenticels stomata, of Number easier. colonization for sites entry preferential offer microcracks needed be panels may germplasm highly on contrasted consi trials large resistance, of factors To potential propagation. lesion of speed the on act slightly resista total provide not may fruit) (wounded flesh f Resistance rot. brown to resistance any abrogated progeny peach canning infection of variability the explored further group genotype the on depending both, or resistanceBR that suggested variabili observed authors The fruit. unwounded and

n ocuin i i eiet ht tmt, lenticel stomata, that evident is it conclusion, In Comment citer cedocument: Journal ofAgriculturalandFoodChemistry ACS Paragon PlusEnvironment 110

, concluding that wounding the fruit generally generally fruit the wounding that concluding , is associated with the pericarp or the mesocarp mesocarp the or pericarp the with associated is 109 17 17 . Nonetheless, more recently the same same the recently more Nonetheless, 101 . . dering a high replicate number number replicate high a dering reaction after wounding of a of wounding after reaction Monilinia ctors were no more efficient efficient more no were ctors ed fruit were infected, large large infected, were fruit ed nce to infection but may may but infection to nce environment conditions. conditions. environment actors at the level of the the of level the at actors nd pores may be under under be may pores nd by infection on wounded wounded on infection by ect of cultural practices practices cultural of ect e species and between between and species e further explore these these explore further . ty in both cases and and cases both in ty l l s, pores, cracks and and cracks pores, s, ant factors may be be may factors ant 109 and make fungi fungi make and , explored larger larger explored , has not been been not has Version postprint always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 426 426 425 424 423 422 421 420 419 418 417 416 415 414 413 412 411 410 409 408 407 406 405 404 428 428 427 the spores from the inoculum source to the organ ho organ the to source inoculum the from spores the c phase prepenetration The 6). (Figure penetration prepenetration stages: three in divided broadly be relatio parasitic a of establishment subsequent the development Infection 4 or in damaged tissues tissues damaged in or on accumulate that exudates plant from and water of obt is which germination, for moisture free require and germination Adhesioncuticle to the 4.1 and infection germination spore for crucial factor al et Rungjindamai by reviewed c As wall. cell plant the and cuticle the penetrate highly a in enzymes walldegrading cell of variety in cytoskeleton the of components accumulates hypha pro penetration the support to pressure turgor high th At surface. plant appressoria the on tube germ the of growth as of formation the iii) and surfaces, host degrade to structures, infection position optimally to contact in growth oriented and sensing chemical i) include here. detailed bewill not

appressoria n eea, ug uiie ies mcaim t inf to mechanisms diverse utilize fungi general, In or an of entry the implies that term a is Infection Conidia and ascospores, which are the main inoculum main the are which ascospores, and Conidia r otn omd ht a hv mlnsd al and walls melanised have may that formed often are Comment citer cedocument:

111 Journal ofAgriculturalandFoodChemistry Iiil vns r ahso t te uil ad di and cuticle the to adhesion are events Initial . 112 ACS Paragon PlusEnvironment . Germination of conidia takes about an hour in the in hour an about takes conidia of Germination .

14 , the presence of moisture near the fruit is a is fruit the near moisture of presence the , 18 18 ii) the production of enzymes of production the ii) development. development. regulated fashion in order to order in fashion regulated specialized structures such such structures specialized ained from films or droplets droplets or films from ained nship td n ay rils and articles many in ited nen te rnpr of transport the oncerns st that will be infected. It It infected. be will that st response to mechanical mechanical to response pntain n post and penetration , the surface of the host the of surface the ganism into a host and and host a into ganism cess. The penetration penetration The cess. the tip and secretes a a secretes and tip the ect host tissue, which which tissue, host ect 36 . The process could could process The . pntain site, penetration e for BR infections, infections, BR for develop develop rected rected

Page 18of72 Version postprint Page 19of72 always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 451 451 450 449 448 447 446 445 444 443 442 441 440 439 438 437 436 435 434 433 432 431 430 429 453 453 452 4.2 Latent infection Latent infection 4.2 the reactive and to rehydrate timeneed spores that hours, 60 last sometimes could process germination 4 require ascospores while water, free of presence C. gloeosporioidesC. A surface. plant the to tightly penetrate, to both of combination a or force, wh of Irrespective plant. host the by provided cues 4.3 spp.Monilinia to methods molecular treatments, fungicide targeted strategi shipping postharvest as well as practices, posthar and pre determine to needed is infections peaches for reported been has a species fruit different or for investigated orchards in infections latent of incidence the develops and BR growth restarts fruit the of colonization and infection successful growth, fruit vi be may infections quiescent These stops. quickly bu begins, infection subcuticular A fruit. immature unfavourable are stage growth

Appressorium The relationship between the numbers of conidia on conidia of numbers the between relationship The con microclimatic when latent remain may Infections Formation of of Formation have been developed beenhave M. fructicola fructicola M. Comment citer cedocument: Journal ofAgriculturalandFoodChemistry by wax isolated from fruit of its host plant, avochost its plant, of fruit wax from byisolated formation and hypha penetration penetration hypha and formation appressorium ACS Paragon PlusEnvironment

expresses genes and proteins enabling later later enabling proteins and genes expresses ppressorium is induced by specific physical or chemical chemical or physical specific by induced is 14 36,88 85 . . . Therefore early identification of fungal fungal of identification early Therefore . 31 . Latent infection generally happens in in happens generally infection Latent . 19 19 77,86, . . differentiation can be stimulated in in stimulated be can differentiation

88,

89, 91

appressoria 113 . As the fruit matures, fungal fungal matures, fruit the As . ether fungi use enzymes or or enzymes use fungi ether protoplast vest disease management management disease vest . A significant positive link link positive significant A . got o te pathogen the of growth t identify latent infection of of infection latent identify sible or nonvisible. Along Along nonvisible. or sible to 6 hours. However the the However hours. 6 to s I odr o choose to order In es. fter harvest has been been has harvest fter in the case of dried dried of case the in the fruit surface and and surface fruit the need to adhere adhere to need iin ad fruit and ditions 36 . ado, but not but not ado, Version postprint always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 477 477 476 475 474 473 472 471 470 469 468 467 466 465 464 463 462 461 460 459 458 457 456 455 454 478 478 planta host cell wall. To analyse the contribution of cell of contribution the analyse To wall. cell host supported be to likely is Penetration surface. the h the pushes and cytoskeleton, the by also possibly of inhibitors contained waxhost plants other from isolated wax by appressoria fructicola d they contrast, In appressoria diverse. be may mechanisms that from produced pegs penetration (through pen direct by as well as (stomata) openings natural trig to appressoria features germ topographical and particular lips, perceived cell guard stomatal the volatiles on fruit observed and nutrients of presence the as topographysurface fruit to incidence BR to related tis for only not enzymes pectolytic required fungi, in expressed is Finally, genepenetration. the that show to able were Monilinia of promoter al et Dumas process, penetration the

growth, but also to assist forceful penetration. penetration. to forceful assist butalso growth, Appressorium the within turgor by generated be can pressure High spp.), to control green fluorescent protein expres protein fluorescent green control to spp.), etan te omto o seilzd neto s infection specialized of formation the restrains o maue ise ad eae a a arpye pa saprophyte a as behaves and tissues immature to Since . n aue etrn fut Te uhr sgetd th suggested authors The fruit. nectarine mature on Colletotrichum lindemuthianum lindemuthianum Colletotrichum Comment citer cedocument: Journal ofAgriculturalandFoodChemistry appressorium omto by formation olttihm lindemuthianum Colletotrichum ACS Paragon PlusEnvironment

appressorium mediated penetration was observed both by both observed was penetration mediated 114 . fructicolaM. aeu nlsssgetd ht non that suggested analyses Careful . 20 20 115 used the endopolygalacturonase endopolygalacturonase the used appressoria development. development. (a necrotrophic fungus like like fungus necrotrophic (a on fruit surfaces has been been has surfaces fruit on walldegrading enzymes to enzymes walldegrading and hydrophobicity, as well well as hydrophobicity, and by enzymes that soften the the soften that enzymes by u mcrto during maceration sue ypha to penetrate through penetrate to ypha 116,90. 116,90. , as other necrotrophic necrotrophic other as , etration of intact cuticle cuticle intact of etration e dfeetain of differentiation ger , uhr suggested authors ), appressoria sion. These authors authors These sion.

Appressoria appressorium tructures such as as such tructures tubes apparently apparently tubes d o observe not id ro to prior thogen thogen were were at and and in- M. Page 20of72 Version postprint Page 21of72 always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 501 501 500 499 498 497 496 495 494 493 492 491 490 489 488 487 486 485 484 483 482 481 480 479 503 503 502 4.4 4.4 appressorium suggested was pathway calciumcalmodulin as well as mature in as accessible, readily are nutrients when also observed that that observed also laxa melanindefi a that reported has colleagues and Cal melanised gray Magnaporthe to higher and leads solutes efflux appressoria redu the in involved is melanization that concluded penet of inhibition an and melanization no observed fungus exposed authors These penetration. surface al et Howard development. pathogens fungal different to necessary considered melanizatio the and virulence their with associated melanins name usually phenols, fungal various from formed be pigme dark extracellular The tyrosine. of oxidation synthes fungi Various organisms. other and fungi by mo indolic or phenolic of types various of composed

(albino mutant) was no longer able to induce peach induce to able longer no was mutant) (albino Appressoria ned mn fna ptoes sc as such pathogens, fungal many Indeed, macro biological pigments, brownblack are Melanins anprh grisea Magnaporthe 112,117 appressoria wall. According to Dean Dean to According wall. 90 Comment citer cedocument: Te rdcin f eai b mcoraim hs b has microorganisms by melanin of production The . . . melanization increase pathogenicity pathogenicity increase melanization Journal ofAgriculturalandFoodChemistry , , yiuai oryzae Pyricularia . laxaM. to cause infection and disease development development disease and infection cause to ACS Paragon PlusEnvironment

rae wt prqio, n niio o melanin of inhibitor an pyroquilon, with treated 118 o ouin o hg omtc rsue and pressure osmotic high of solutions to proposed the importance of melanization for for melanization of importance the proposed appressoria 21 21 119 and , , this causes the locking of cytosolic cytosolic of locking the causes this , olttihm legenarium Colletotrichum pressure. pressure. appressoria nts produced by fungi may fungi by produced nts fruit. Also, a role of cAMP cAMP of role a Also, fruit. nomers that are produced are that nomers ration of the leaves. They They leaves. the of ration for infection and disease disease and infection for cient mutant strain of of strain mutant cient to o prst o the of porosity of ction n of of n z mlnn rm the from melanin ize etra inaequalis Venturia d as heterogeneous heterogeneous as d twig blight twig in the formation of of formation the in from the rice blast blast rice the from appressoria molecules molecules 120,117 118 , need need , . They . was was . De . een een M. , , Version postprint always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 526 526 525 524 523 522 521 520 519 518 517 516 515 514 513 512 511 510 509 508 507 506 505 504 528 528 527 of of laxa colony the of melanization inhibited vitro blight twig peach induce not could biosynthesis, the importance of acidification for the secretion o secretion the for acidification of importance the by factors pathogenicity of secretion importance the suggesting respectively, 6fold, and of genes polygalacturonase two for encoding transcrip of expression relative the 3.6–3.7, pH at cul nectarine susceptible less the in than cultivar i observed was acid gluconic of accumulation higher sensiti differing with ‘Plácido’ cv. peach and Top’ compared When conditions. liquidculture under and accumu acid organic main the was acid gluconic that acid gluconic and ‘Venus’, Top’, ‘Big cvs. peach of colonization fructicola, pathoge of expression the pH regulates lowering 4.5 a fungi of conditions.adverse under thefield in permanence development of success the improve could fruit host of infection successful the for required concluded they So type. wild the by produced those

M. fructicola fructicola M. to produce melanin is crucial for its pathogenicit its crucialfor is produce melanin to , chlorogenic acid or pyroquilon added to the cultu the to added pyroquilon or acid chlorogenic , ug aeal o oiy h hs H rlmnr d Preliminary pH. host the modify to able are Fungi Free and Rehnstom and also and 76 Comment citer cedocument: . Analysis of the acidification process in colonize in process acidification the of Analysis . are able to infect nectarines, by producing lesions producing by nectarines, infect to able are Journal ofAgriculturalandFoodChemistry M. fructigenaM. ACS Paragon PlusEnvironment 123,

however, showed that melanindeficient mutants mutants melanindeficient that showed however, indicate that they can reduce host pH during during pH host reduce can they that indicate M. fructicola 122 22 22 . They concluded that the ability of of ability the that concluded They . M. fructicolaM. . Nevertheless their presence presence their Nevertheless . 121 vities to vities . The authors also underlined underlined alsoauthors The . tivar. Under liquid conditions, conditions, liquid Under tivar. f pathogenicity factors by factors pathogenicity f . Finally, they found that that found they Finally, . y. y. ts of mfpg2 and mfpg3, mfpg3, and mfpg2 of ts lated at the infection site site infection the at lated n the susceptible peach peach susceptible the n of acidification for the the for acidification of nicity genesnicity that melanization is not not is melanization that to a nectarine cv. ‘Big ‘Big cv. nectarine a to ‘Tirrenia’ by secreting secreting by ‘Tirrenia’ re medium of of medium re M.fructicola t on ata , increased 12fold 12fold increased , nd increase their their increase nd d fruit showed showed fruit d .lx, M. laxa, M. . as large as large as

, a 250% 250% a , M. laxa M. M. M. in- M. Page 22of72 Version postprint Page 23of72 always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 551 551 550 549 548 547 546 545 544 543 542 541 540 539 538 537 536 535 534 533 532 531 530 529 553 553 552 4.6 Biochemical arsenal of Biochemical 4.6 pathogen.by the e the of result a as expressed be may pathogenicity Specifi expression. pathogenicity promotes that cue fructicola r etn ehltaseiiae (C ...0, th 4.2.2.10), (EC methyltranseliminase, pectin or polygala attacks hydrolytically that 3.2.1.15), (EC three all by secreted are found was activity cellulase weak very A fruits. pear rotted for whereas secretio cellulase The restricted. very be to seems the pathog of virulence the directly to contributes cutinase as oxysporum Fusarium activation, former from result may enzymes these of surface intact the penetrate to needed cutinases fungus. phosphatases alkaline and pe esterases catalases, dehydrogenases, like enzymes of groups large reported of mycelium of extracts buffer in enzymes fungus

h plglcuoi ai can s takd y thre by attacked is chain acid polygalacturonic The of species all in found been has Cellulase by produced enzymes important most The effects the ascertained decades past the in Studies , suggesting that ambient pH created by the pathoge the by created pH ambient that suggesting , MfCUT1 36 . . . fructigenaM. Comment citer cedocument: Journal ofAgriculturalandFoodChemistry , which is upregulated in an oxidant environment, environment, oxidant an in upregulated is which ,

125 ACS Paragon PlusEnvironment . In the case of case the In .

t a dtce a rc o atvt i etat of extracts in activity of trace a detected was it Monilinia Monilinia spp., namely i) endopolygalacturonase endopolygalacturonase i) namely spp., spp. spp. 23 23 M . fructicola en cturonic acid, ii) pectin lyase lyase pectin ii) acid, cturonic for for Monilinia n was detected in detected was n oiii spp.Monilinia 91 fruit, fruit, nvironmental pH induced induced pH nvironmental , gene expression of the of expression gene , . . . laxa M. . fructicolaM. c genes contributing to to contributing genes c roxidases, glutamic glutamic roxidases, in the necrotroph necrotroph the in produced by this this by produced 75 e enzymes which which enzymes e , but its secretion secretion its but , , of fungicides on on fungicides of 91 t tak a attacks at n is a regulatory regulatory a is n . High levels of of levels High . 124 . may be the the be may in medium medium in Thus, they they Thus, M. laxa, laxa, M.

Ohr nye ta dgae eta sgr hv be have sugars neutral degrade that enzymes Other . ne neto i etbihd te yhe f h pa the of hyphae the established, is infection Once mn ezms erdn nurl uas aaias a (arabinans sugars neutral degrading enzymes Among was the one mainly expressed. Gradziel and Wang Wang and Gradziel expressed. mainly one the was p. oyaatrnss s h peec o calcium of presence the is polygalacturonases spp. as βgalactosidase, but have not been studied in d in studied been not have but as βgalactosidase, arab from arabinose monomeric release to found was and may migrate to the plant plasmalemma and can be and can plasmalemma plant the migrate to and may Comment citer cedocument: MfPMG1 Journal ofAgriculturalandFoodChemistry MfPG1 ACS Paragon PlusEnvironment expression could be due to the activation of the p the of activation the to due be could expression

126 diminished virulence of the pathogen. Authors Authors pathogen. the of virulence diminished Recently, . 127 36 . This enzyme is localized in the hyphae of hyphae the in localized is enzyme This . . An important factor for the expression of expression the for factor important An . 24 24 Chou t al et ation and iii) pectin esterase esterase pectin iii) and ation . fructicola M. The optimum pH for each for pH optimum The t of multi vesicular bodies bodies vesicular multi of t ms such as the browning browning the as such ms different culture media. media. culture different tes the methoxyl groups groups methoxyl the tes (ROS) produced in this this in produced (ROS) C 3.2.1.55) from from 3.2.1.55) C 5

etails investigated five five investigated 127 en found in in found en thogen spread spread thogen . They were were They . observed that that observed nd galactans) galactans) nd 36 . . secreted secreted inans by by inans n the in lant lant M. M. M. Page 24of72 Version postprint Page 25of72 always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 602 602 601 600 599 598 597 596 595 594 593 592 591 590 589 588 587 586 585 584 583 582 581 580 579 occasionally intracellular and the dead protoplasts dead the and intracellular occasionally parti in though intercellular, generally are hyphae of microscopy, electron of affinity particular b Investigations host. the of part any permeate and perpetuate itself, this bursting leads to the desic the to leads bursting this itself, perpetuate Apar cuticle. and epidermis fruit the through burst maturity fruit in stages p the genotype, host the conditions, environment of mumm in fruit the the fungus of permanence help the by degraded pectin from formed is pectate calcium cell host the affected metabolites weight molecular f as described decompartimentalization mix, contents their damaged, been have organelles mitochondri vacuoles, of membranes if Moreover use. sources has pathogen the Subsequently, cells. from o leakage in resulting measurements conductivity by be could function its tissues, infected In intact. lumen

The spread of BR pathogens is generally intercellul generally is pathogens BR of spread The nooyaatrnss n pci etrss activit esterases pectin and Endopolygalacturonases if even occur could plasmalemma host the in Changes In fruit, the rate of increase in rot diameter depe diameter rot in increase of rate the fruit, In 124 . . Comment citer cedocument: Journal ofAgriculturalandFoodChemistry 90,130,131 . laxaM. 124 ACS Paragon PlusEnvironment M. fructigenaM.

. After a few days, conidial pustules of the fungus the of pustules conidial days, few a After . . . Willaman for the middle lamella region. Transmission Transmission region. lamella middle the for 95 , 130 Tee ertos as te olpe of collapse the cause secretions These . attacking pear fruit also confirmed that that confirmed also fruit pear attacking 25 25 36 132 . . , suggested that a hydrophilic gel of of gel ahydrophilic suggested that , drastically impaired as shown shown as impaired drastically cation of the host tissues and tissues host the of cation cular infections they become become they infections cular t from allowing the fungus to fungus the allowing from t are pushed across the cell cell the across pushed are y Reinganum Reinganum y M. fructicolaM. f sugars and amino acids amino and sugars f athogen species and the the and species athogen of carbon and nitrogen to to nitrogen and carbon of y nds on the combination combination the on nds a, chloroplasts or other other or chloroplasts a, 36 . . ar. It could penetrate penetrate could It ar. ollowing a process process a ollowing the membrane is is membrane the ies generate low low generate ies . This gel may may gel This . 129 showed a a showed

To date there is limited evidence evidence limited is there date To co factors host identify to tried long has Research In conclusion, the infection process unfolds differ unfolds process infection the conclusion, In component barrier component barrier The plant cuticle is supposed to constitute an effi an constitute to supposed is cuticle plant The .

Comment citer cedocument: Journal ofAgriculturalandFoodChemistry ACS Paragon PlusEnvironment

36 listed some of them: flowering date, fruiting fruiting date, flowering them: of some listed 26 26 on factors limiting BR in mesocarp and and mesocarp in BR limiting factors on lant. The different layers of layers different The lant. ion progress, Figure 8. 8. ionprogress, Figure s, it is still not possible to to possible not still is it s, flowering for apricots, cork apricots, for flowering ma plugs in stomata, skin skin stomata, in plugs ma ruit. In the meantime, the the meantime, the In ruit. g specific structures (e.g. (e.g. structures specific g ly few cultivars. fewcultivars. ly er authors underlined the the underlined authors er cuticle, a multi cuticle, the host the ed and others avoided. avoided. others and ed ently depending on the on depending ently fruit fruit works have identified identified have works ion, acidification) and and acidification) ion, cient mechanical and and mechanical cient colonize the plant plant the colonize to fruit epidermis epidermis fruit to ntributing to BR BR to ntributing 36 . . Page 26of72 Version postprint Page 27of72 always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 649 649 648 647 646 645 644 643 642 641 640 639 638 637 636 635 634 633 632 631 630 629 628 627 651 651 650 muiy sgetn ta te uil i nt ut a just not is cuticle the that suggesting immunity, betw interrelationships complex reveal to starting s fruit of barriers successive the to corresponding rol these but to need fungi barrier, the infection, develop To understood. this in role a play each may a cells) epidermis cutin, (waxes, surface fruit the neto srcue. oe tde rpre stimula reported studies Some structures. infection germi trigger towax surface host the use to fungus inh of absence i and components terpenoid longerchain of presence the by effect this explained authors waxes by not but host, this of waxes surface the by by formation al et Podila instance, plant in molecules messenger as role a play lipids ReinaPinto review, this with interfere may treatments chemical the and prote or to repair formed are plates new wax occur, spor for crucial water of film the of formation the 135,136,137 de 33, to 21 from number carbon in ranging alkanes, unbranche saturated, long very of mixture complex a todefence infection. fruit in playthe a role diffe in localized compounds biochemical of variety

oee fcos uh s eprtr, h hat sta health the temperature, as such factors However that layer wax epicuticular the is level first The . Waxes can form crystals that enhance water repell water enhance that crystals form can . Waxes Colletotrichum gloeosporioides Colletotrichum Comment citer cedocument: Journal ofAgriculturalandFoodChemistry 138 exposed various studies demonstrating that cuticul that demonstrating studies various exposed ACS Paragon PlusEnvironment 139 hwd ht h griain and germination the that showed

27 27 in avocado is induced specifically specifically induced is avocado in kin. Recent observations are are observations Recent kin. nd its attributes (trichomes) (trichomes) attributes its nd – nation and differentiation of differentiation and nation ct the fruit. fruit. the ct pathogen interactions. For For interactions. pathogen rent layers or tissues may may tissues or layers rent from other plants plants other from pass mechanical barriers barriers mechanical pass hscl are, ic a since barrier, physical griain I wounds If germination. e pending on the plant taxa taxa plant the on pending een cuticular lipids and and lipids cuticular een tory effects of extracted extracted of effects tory d chain aliphatics and n and aliphatics chain d covers the cuticle and is is and cuticle the covers process, process, n fatty alcohols, the the alcohols, fatty n es are not yet well well yet not are es ibitors that allow the the allow that ibitors ence and prevent prevent and ence tus of the plant plant the of tus appressorium 92 . In their their In . 114 . The The . ar ar

h ctce s h scn brir ht h fni ne fungi the that barrier second the is cuticle The wax cuticular that reported was it contrary, the On spp. infection. infection. spp. Comment citer cedocument: 93 . . 144 f.sp. f.sp. Journal ofAgriculturalandFoodChemistry 124 . Unfortunately, with respect to respect with Unfortunately, . . This evidence suggests that the different constit different the that suggests evidence This . and hordei ACS Paragon PlusEnvironment

ucna rmns .p tritici f.sp. graminis Puccinia germination was more rapid and greater on the on greater and rapid more was germination 28 28 143

Podosphaera leucotricha Podosphaera ogen couples is not valuable. valuable. not is couples ogen nd/or during the ontogeny of of ontogeny the during nd/or ion of of ion tfni neatos n a and interactions itfungi

n synthesized exclusively exclusively synthesized n d 19% cutin and filled by by filled and cutin 19% d Monilinia rns persicaPrunus y among different plant plant different among y 3% cutan, 27% waxes, waxes, 27% cutan, 3% namic acid derivatives derivatives acid namic h etnin f the of extension The cipher waxes role in in role waxes cipher ichomes are covered covered are ichomes Magnaporthe grisea Magnaporthe

h qatt and quantity the 140,141,142 various protective protective various es inhibit conidial conidial inhibit es ed to cross. This This cross. to ed spp., there is a is there spp., on certain certain on . Similarly, Similarly, . fruit has has fruit uents uents , , Page 28of72 Version postprint Page 29of72 always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 700 700 699 698 697 696 695 694 693 692 691 690 689 688 687 686 685 684 683 682 681 680 679 678 677 701 701 eeoe t dt. osdrn te uil a a str a as cuticle the Considering date. to developed Prunus 145 a (epicuticular waxes with interspersed and covered of consisting material a composite of organization n opsto ad hcns. h mjr usac t substance major The thickness. and composition in fractures of the presence as well as colonization, “op be could that pores even and stomata trichomes, site discontinuous display may It layer. continuous mention previously as However, process. penetration penetration. for le high induce wouldthen monomers cutin of Sensing act cutinase basal by produced be may that monomers al by et Kolattukudy infection necrotrophic from tissues al inh contrast, in or activators pathogenicity fungal epicuticula of components some as well As pathogen. intera in role messenger molecular a playing occur, li cuticular the between interrelationship complex chemical quantitative and qualitative on that dependent seeing caution, deserves penetration pathogen

Hwvr a hrceiain f h fut surface fruit the of characterization a However, . 146 demonstrated on tomato that cutin plays an importa an plays cutin that tomato on demonstrated The last barrier in the surface is the epidermis ce epidermis the is surface the in barrier last The cruci a be to thought is cuticle the conclusion, In species, among diverse structurally is cuticle The i odr o eemnt cliapcfc kn fe skin cultivarspecific determinate to order in , Comment citer cedocument: 114 Journal ofAgriculturalandFoodChemistry , some pathogens sense plant surfaces thanks to cut to thanks surfaces plant sense pathogens some , ACS Paragon PlusEnvironment

29 29 orts cinerea Botrytis ibit the infection. Isaacson et Isaacson infection. the ibit in the epidermis. epidermis. thein cutin, polyester that is partly partly is cutin,that polyester pids and the fungus may may fungus the and pids ctions between plant and and plant between ctions vels of cutinase required required cutinase of vels nd intracuticular waxes) waxes) intracuticular nd r waxes, they can act as act can they waxes, r s as secretory tissues, tissues, secretory as s ucture of resistance to to resistance of ucture composition. Indeed, a a Indeed, composition. en doors” for pathogen for doors” en d te uil i nt a not is cuticle the ed, f ies vreis of varieties diverse of hat reinforces the cell cell the reinforces hat ivity of fungal spores. spores. fungal of ivity al factor in the fungal fungal the in factor al atures, has not been been not has atures, ll wall that could vary vary could that wall ll nt role in protecting protecting in role nt its proprieties are are proprieties its but exhibits the the exhibits but . According to to According . icle icle Version postprint always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 724 724 723 722 721 720 719 718 717 716 715 714 713 712 711 710 709 708 707 706 705 704 703 702 726 726 725 also accumulate callose, suberin, tannin and pectin and tannin suberin, callose, alsoaccumulate arou Sites colonization. of process the restringing diffusion the and toxins pathogen of diffusion the d of action the against wall cell the of resistance lignif of process The lignin. the is structure wall fet o cfec cd clrgnc cd o reduc or acid, chlorogenic acid, caffeic of effects studies Subsequent polymers. host of degradation in p the with interference by resistance to contribute arresting a such factors other with combination in phenolics, chlor that suggest to authors the led results These cutina suppressed also derivatives acid benzoic and isoforms cutinase major two of appearance activity th but growth mycelia or germination spore suppress to concentrati wit genotypes, high peach of fruit in and fruit immature have acids caffeic and chlorogenic BR for studied theone most of became compoundsof the in compounds these of levels high displayed BR, cultiva peach ‘Bolinha’ from fruit that observation in role their redoxmediated acids Phenolic and 5.2

. fructicolaM. mn te hnlc opud o te pdri o pe of epidermis the of compounds phenolic the Among al suis f ec peoi cmons tre f started compounds phenolic peach of studies Early 75 Lkws, h peec o cfec cd n culture in acid caffeic of presence the Likewise, . . fructicolaM. Comment citer cedocument: 116 . In cultures of of cultures In . Journal ofAgriculturalandFoodChemistry n uecn infections quiescent in ACS Paragon PlusEnvironment

. fructicolaM. 30 30 75 . In addition, a series of cinnamic of series a addition, In . , these phenolic acids did not not did acids phenolic these , roduction of factors involved involved factors of roduction 63 nd the infection point could could point infection the nd h a high level of resistance resistance of level high a h to resistant be to known r, gaain nye; block enzymes; egradation d lttin o infection on glutathione ed substances substances s iron, could have a role in in role a have could iron, s ication could improve the the improve could ication . Furthermore, they may may they Furthermore, . of nutrients from the fruit, fruit, the from nutrients of fungal inhibition inhibition fungal ogenic acid and related related and acid ogenic ir epidermis. This group group This epidermis. ir resistance se levels in culture culture in levels se

n vivoin ey inhibited cutinase cutinase inhibited ey ons, especially in in especially ons, s prevented the the prevented s confirmed the the confirmed 147 127 . . . ach fruit, fruit, ach rom the the rom 38 . . Page 30of72 Version postprint Page 31of72 always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 749 749 748 747 746 745 744 743 742 741 740 739 738 737 736 735 734 733 732 731 730 729 728 727 751 751 750 hnlc cd sprse mN acmlto ad enz and accumulation mRNA suppressed acids phenolic development appressorium sus conidial fructicola in compounds those Adding development. n ps ezms y omn cmlxs ht lc ac block that complexes forming by enzymes pest and defence plant in role important an play ma and (LTPs) Proteins’ Transfer ‘Lipid of to referred be also may proteins cuticular lipids, cuticular proteins resistance.disease to cancontribute an acidity high as such factors fruit how discussed Lichter limiting in compounds phenolic 4.4). of germination and growth the on effect any without product the with interfere can acid, neochlorogenic section 5.3) giv a of effect specific a than rather antioxidants attenuated cutinase

149 lhuh uil rsac hs any oue o the on focused mainly has research cuticle Although . Atv mcaim i rsos t ptoe attac pathogen to response in mechanisms Active 5.3 al et Villarino tha showed group same the by conducted work Further 150 Ee tog tee eut ae neetn, h ro the interesting, are results these though Even . i nt nii griain n lwr eas n f and petals flower on germination inhibit not did have reviewed pathogen quiescence in postharvest postharvest in quiescence pathogen reviewed have 148 . fructicolaM. 91,148 Hwvr ohr nixdn cmons lo signifi also compounds antioxidant other However, . 116 omto fo griae cnda n sbeun B subsequent and conidia germinated from formation Comment citer cedocument: . . . Journal ofAgriculturalandFoodChemistry 122 ACS Paragon PlusEnvironment eosrtd ht hooei ai ad t isomer, its and acid chlorogenic that demonstrated uiae rdcin idctn a eea efc o effect general a indicating production, cutinase

Monilinia spp. spp. Monilinia

31 31 138 . They specifically inhibit pathogen pathogen inhibit specifically They . remains unsolved. Prusky and and Prusky unsolved. remains en phenolic compound (see (see compound phenolic en o o eai in melanin of ion d phenols in unripe fruits fruits unripe in phenols d the fungus (see section section (see fungus the ny have been shown to to shown been have ny importance. They are are They importance. tive sites or alter alter or sites tive m atvt o a of activity yme le of the different different the of le ruit, but inhibited inhibited but ruit, pensions of of pensions diseases and and diseases nlss of analysis t antioxidant antioxidant t k: defence defence k: lesion R . laxaM. cantly M. f f

Ppdfn1 h cags n h tasrpinl ee o gns c genes of level transcriptional the in changes The chi as such enzymes, hydrolytic produce also Plants al et Nanni particular, in defensins On M. fructicola in peach defence against fungal pathogens. pathogens. fungal against defence peach in Comment citer cedocument: Ppdfn1 Journal ofAgriculturalandFoodChemistry . . ACS Paragon PlusEnvironment displayed an antifungal activity through specific specific through activity antifungal an displayed

32 32 153 . . rns domesticaPrunus 151 . Elkereamy et al et Elkereamy . investigated the possible role possible the investigated

ase inhibitors. Unlike simple Unlike inhibitors. ase infection was tested. They tested. was infection ne among two European European two among ne ated, however, defensive defensive however, ated, e filtrates of the fungal fungal the of filtrates e types, as well as other other as well as types, ids, proteins require a a require proteins ids, s Zmnk t al et Zemanek ks. to e hesised consequently, consequently, hesised oitd ih h BR the with sociated s of phenylpropanoid phenylpropanoid of s nction. They include include They nction. qatte atr a after quantities t . laxaM. lucanase gene gene lucanase L.). It is well well is It L.). Ppdfn1 154 described described sc as such , dn to oding tinases, tinases, gene 152

Page 32of72 Version postprint Page 33of72 always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 800 800 799 798 797 796 795 794 793 792 791 790 789 788 787 786 785 784 783 782 781 780 779 778 777 801 801 n h ssetbe n (v ‘ebu’ tee levels these ‘Veeblue’) (cv. one susceptible the in resistant the in expressed constitutively remained signall the involved enzyme, degrading phospholipid (PLD Dalpha phospholipase and PR10 of transcripts after that observed authors The PR. the in proteins intermediary to coding transcripts h hroemdae eec rsossta result that responses defence hormonemediated the of role intermediary an suggesting plums, European fructicola authors, same ph antifungal some of biosynthesis the in involved a t and biosynthesis) phytoalexin and phenylpropanoid (PAL, lyase phenylalanineammonia to coding genes an biosynthesis, camalexin of induction higher a as thaliana overexpression ectopic the Furthermore, ‘Victory’). susceptible in increase rapid a and ‘Stanley’) and in infection after levels transcript PR5 in change to similar pattern a with was Activity resistance. co was cultivars plum among expression differential the pathogen. s cultivar, resistant the in compound the of levels cultivars both on genes these of ti pattern transcript fruit in concentration peroxide Hydrogen attack.

The same authors demonstrated the antifungal activi antifungal the demonstrated authors same The transformants increased resistance to to resistance increased transformants neto i te ee oig o Y3 transcription MYB3 to coding gene the in infection Comment citer cedocument: 156 Journal ofAgriculturalandFoodChemistry described a very similar expression pattern after after pattern expression similar very a described ACS Paragon PlusEnvironment

33 33 . fructicolaM. Alternaria brassicicolaAlternaria uggesting an inhibitor role for for role inhibitor an uggesting resistant cultivars (‘Violetta’ (‘Violetta’ cultivars resistant variety (cv. ‘Violette’), while while ‘Violette’), (cv. variety nrae atr pathogen after increased PR10, PR10, inlig aha o this of pathway signalling genotypes (‘Veeblue’ and and (‘Veeblue’ genotypes d transcript abundance of of abundance transcript d o three cytochrome P450 cytochrome three o this transcription factor in in factor transcription this , with higher but steady steady but higher with , ing of stress responses) stress of ing f hs rti in protein this of enolics. rltd ih hi BR their with rrelated se creae with correlated ssues n h idcin f PR of induction the in artificial inoculation, inoculation, artificial , cl membrane cell a α, i.e ty of PR5, whose whose PR5, of ty central point in in point central ., no significant significant no ., 155 Finally, the the Finally, atr of factor , as well well as , M. A. A. Version postprint always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 824 824 823 822 821 820 819 818 817 816 815 814 813 812 811 810 809 808 807 806 805 804 803 802 826 826 825 of fruit species. species. of fruit development the for knowledge of generation the in in pathways, defence gen these of variability the of study The proteins. induced gene expression and increased enzyme activi enzyme increased and expression gene induced of presence The o application with BR of incidence the in reduction peroxid tiss in accumulation peroxide hydrogen of reduction lipid carbonylation, protein of levels high host, digitatum, Penicillium response in petals flower peach in ROS of component reg this to related is that cycling redox suggested coul status redox in cellular changes that indicate sulphoximin buthionine the inhibitor, synthesis GSH (GSH) glutathione antioxidant the by and (CA) acid do is expression gene that reported Authors status. gene al et Chiu virulence. pathogen enhance stim either can ROS of production The interactions. dual play ROS that reported research recent however death cell programmed and oxidative stress ROS, 5.4

M. fructicolaM. MfCUT1 Liu et al et Liu stil is BR in mechanisms virulence of knowledge The (that encodes the major cutinase of of cutinase major the encodes (that Comment citer cedocument: 158 induced hydrogen peroxide accumulation in flower p flower in accumulation peroxide hydrogen induced investigated the production of hydrogen peroxide, peroxide, hydrogen of production the investigated . fructicolaM. Journal ofAgriculturalandFoodChemistry nnhs ptoe. uig h itrcin ih t with interaction the During pathogen. nonhost a Prunus ACS Paragon PlusEnvironment

germplasm collections has a crucial importance importance crucial a has collections germplasm prs t h srae f nat lwr petals flower intact of surface the at spores 34 34 157 xmnd h rglto o the of regulation the examined ulation. ulation. d impact virulence of BR and BR of virulence d impact ues. They also observed a a alsoobserved They ues. s wih ae fet in effects have which es, f exogenous antioxidants. antioxidants. exogenous f of more resistant varieties varieties resistant more of ation and a significant significant a and ation lt hs rssac or resistance host ulate e (BSO). These results results These (BSO). e wnregulated by caffeic caffeic by wnregulated ty of NADPH oxidase, a oxidase, NADPH tyof . fructicolaM. n ueuae b a by upregulated and

to to roles in planthost planthost in roles . fructicolaM. l rudimentary; rudimentary; l ) by redox redox by ) a major major a etals, etals, and he Page 34of72 Version postprint Page 35of72 always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 849 849 848 847 846 845 844 843 842 841 840 839 838 837 836 835 834 833 832 831 830 829 828 827 850 850 ht hne nte eo niomn my influence may environment redox the in changes that l antioxidant intracellular influence can compounds responses significant show n pr a with inoculated tissues the same the while peroxide in resulted This tissues. host in peroxidase generate to important complex enzyme membranebound hnlc cd) s el s pcfc epne t th to responses specific as well as acids) phenolic activ barrier), (mechanical factors constitutive of hi They mesocarp). and (epidermis tissues different t different involve may that resistance multifactor respon host the the fungus. permanently inactivates sometimes that suggest fruit, stone Reinganum and Jekins by obtained results react obvious more and greater a produce would area p Several inhibited. are enzymes some of activities c may mycelium of growth BR, of spread the limiting Despi infection. initial of site distant the around in compounds phenolic of accumulation the and fruit trees fruit pome and mar the at phellogen of formation the infection, of 116 patho the by used structures of development the and

. . h dvriy f tde ad eut pbihd indi published results and studies of diversity The cel of death by respond can fruit the cases some In Comment citer cedocument: Journal ofAgriculturalandFoodChemistry 159 , the suberisation of walls of surrounding living c living surrounding of walls of suberisation the , ACS Paragon PlusEnvironment

158 . These results suggested that the antioxidant antioxidant the that suggested results These . 35 35 160 with e compounds (waxes, cutins, cutins, (waxes, compounds e e uh epne amd at aimed responses such te ypes of defence localized in in localized defence of ypes gin of twig lesions in stone stone in lesions twig of gin evels in the pathogen, and and pathogen, the in evels enetrations within a small small a within enetrations ghlighted the involvement involvement the ghlighted onhost pathogen did not did pathogen onhost gen to facilitate infection infection facilitate to gen ceoii fructicolaSclerotinia atc (rtis and (proteins attack e both gene expression expression gene both dcin f hydrogen of oduction el u t 2 cells 20 to up cells ontinue although the the although ontinue ion by the host. The The host. the by ion ROS and cell wall cell and ROS se to penetration penetration to se ls around the point point the around ls cates a complex complex a cates ells in in ells on on Version postprint always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 873 873 872 871 870 869 868 867 866 865 864 863 862 861 860 859 858 857 856 855 854 853 852 851 874 874 ec clia kon o ae n o te ihs lev highest the of one have to known cultivar peach resistance for BR Breeding 6 proposed. been r fruit of model generic no However, ROS). enzymes, eesd y any by released be to declared flesh melting with peach of cultivar bel (see discovered been have resistance of sources peach in BR to resistance host about knowledge the understood. poorly basisare stati the phenotype, BR the However, with traits those fruit. of correlations stone in BR to b resistance may review this of sections previous in discussed M resistance. BR in involved be may characteristics al et Bostock before, mentioned As requirements. bre ma resistance of fruit with associated challenge characteristics the demonstrates ‘Bolinha’ of case fr preharvest of rate high and size, fruit reduced suscepti high quality, fruit poor its despite peach f breeding conventional in resistance BR of donor a Thi content. phenolic high with cuticle thick a and fruit had ‘Bolinha’ that found and cultivars peach ‘Bolinha’ cultivar Brazilian

urnl, omril cultivars commercial Currently, Apart from cultivar ‘Bolinha’, from which many stud many which from ‘Bolinha’, cultivar from Apart Comment citer cedocument: Prunus Journal ofAgriculturalandFoodChemistry ACS Paragon PlusEnvironment reig rga aon te ol. eades of Regardless world. the around program breeding

161,162 . Feliciano et al et Feliciano . are more or less sensitive to BR. The The BR. to sensitive less or more are 36 36 163 bility to enzymatic browning, browning, enzymatic to bility s cultivar has been been has cultivar s with particularly small size size small particularly with 75 resistant to BR has been been has BR to resistant commercial with conflict y investigated resistance in in resistance investigated i drop uit as well as their genetic genetic their as well as

or canning and lowchill lowchill and canning or suggested that cuticular that suggested ow) and no commercial commercial no and ow) l f eitne s the is resistance of el esistance to BR has has BR to esistance n ohr ri traits fruit other any ipiae i host in implicated e and stone fruit, few few fruit, stone and ies have developed developed have ies stical and genetic genetic and stical dn fr R as BR, for eding 134,164,165,155 used as as used . The The . Page 36of72 Version postprint Page 37of72 always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 897 897 896 895 894 893 892 891 890 889 888 887 886 885 884 883 882 881 880 879 878 877 876 875 899 899 898 6.1 Genetic resources, breeding programs and phenot programs breeding Genetic resources, 6.1 and plums apricots, to BR resistance of control genetic deciphering the sweet), and (sour cherries for trait theg in found resistance BR of sources of the lack scarcely precise and is highly subjected to the cri the to subjected highly is and precise scarcely i fieldborne by caused impact disease the on based scal subjective a from level resistance a accession assessment inoculum Fieldborne 6.2 objectives. specific exp its to according protocol, particular a adopted a strategies experimental employed the in consensus stone on impact BR cultivardependent of assessment phenotypi robust of basis the in materials breeding cross), a from offspring or accessions (cultivars, genetic of population a among variations phenotypic co to protocol, phenotyping or measurement reliable tr given a for studies genetic or programs breeding mai However, the programs. breeding of one is backgrounds genetic quality fruit resistance of sources reliable Identifying quality. comm poor of accessions or cultivars in present are

The simplest system to score BR resistance is to as to is resistance BR score to system simplest The is presently a major objective for breeding program breeding for objective major a presently is As mentioned before, some traits associated with ho with associated traits some before, mentioned As

Comment citer cedocument: Journal ofAgriculturalandFoodChemistry ACS Paragon PlusEnvironment

n o tefrt tp o te salsmn of establishment the for steps first the of one 37 37 and then identify interesting interesting identify then and to be introgressed in high high in introgressed be to erimental capacities and /or /or and capacities erimental ermplasm of stone fruit, this stone fruit, of ermplasm remains a challenge. a challenge. remains terion of the evaluator and evaluator the of terion fxd y h observer, the by fixed e i i te eiiin f a of definition the is ait dt. n h cs of case the In data. c noculum. Although it is is it Although noculum. nd each laboratory has has laboratory each nd ally diverse individuals individuals diverse ally fruit, there is a lack of lack a is there fruit, mpare afterwards the the afterwards mpare s in different countries countries different in s yping strategies ypingstrategies ojcie o such of objectives n sign to each analyzed analyzed each to sign ercial and productive productive and ercial st resistance to BR BR to resistance st ece. Hence, peaches.

(Serbia), Cacak of Institute Research Fruit the In 169 72 . . Comment citer cedocument: Avne slcin soe rltvl hg levels high relatively showed selections Advanced . Journal ofAgriculturalandFoodChemistry 167,168 166 ACS Paragon PlusEnvironment . In the same research center, but in the sour cher sour the in but center, research same the In . , a subjective scale from 1 to 9 (1 for no attack, attack, no for (1 9 to 1 from scale subjective a ,

38 38 ‘Conserva 947’ have been been have 947’ ‘Conserva ber of accessions. The use The accessions. of ber bjective scale scoring was was scoring scale bjective higher diversity was found found was diversity higher eig rgas l over all programs eeding of numerous promising promising numerous of o wih i o high to mid which rom preliminary evaluation of evaluation preliminary perimental orchard, this this orchard, perimental es from autochthonous autochthonous from es 11 of identification the d selections at the final the at selections d ion germplasm was was germplasm ion inning of the peach peach the of inning e Institute of Plant Plant of Institute e n a oa o 75 of total a ong t hmd and humid to d l (described as as (described l 9 for 9 of ry Page 38of72 Version postprint Page 39of72 always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 947 947 946 945 944 943 942 941 940 939 938 937 936 935 934 933 932 931 930 929 928 927 926 925 924 948 948 kn are (one/none fut, pr conce spore fruit), (wounded/unwounded barrier skin su fruit the from spores fieldborne of elimination impa BR of result final the affect can that factors a This conditions. laboratory under fruit harvested assessment infection Artificial 6.3 two screening tests for resistance to to resistance for tests screening two sections”). “Q (see populations segregating in trait resistance g of studies for also useful been has protocol this almonds. from resistance BR introgress to order in inters some as well as heritage ‘Bolinha’ with some va with selections experimental advanced cultivars, s landraces, origins: different very from genotypes to resistance for fruit mature screen elsewhere ethanoldisinf and hypochloride sodium diluted with of suspension conidial a after hours 72 diameter rot average the considered progra peachbreeding cling the within Davis, UC at lesion. reco by progress infection following allows also It before incubation of time and humidity temperature,

As mentioned in other sections of this review, Pasc review, this of sections other in mentioned As One of the first groups that started to use artific use to started that groups first the of One arti by scored be also can evaluation resistance BR 110 . In this way, a large phenotyping effort has been been has effort phenotyping large a way, this In . Comment citer cedocument: Journal ofAgriculturalandFoodChemistry ACS Paragon PlusEnvironment M. fructicolaM.

containing 10 containing 39 39 . laxaM. . fructicolaM. in apricots (7 accessions), accessions), (7 apricots in ct in an experiment, such as such experiment, an in ct rding the diameter of the BR the of diameter the rding fc,peec/bec of presence/absence rface, enetic dissection of the BR the of dissection enetic The material selected with with selected material The lw te oto o many of control the llows BR impact measurement. measurement. impact BR 5 ial inoculations of BR was BR of inoculations ial m, m, ected fruits), as specified specified as fruits), ected rious pedigrees including including pedigrees rious pecific hybrids generated generated hybrids pecific inoculation (10 l drop of of drop l (10 inoculation spores/ml, on previously on spores/ml, tandard canning peach peach canning tandard TLs for BR resistance resistance BR for TLs in over 4000 peach peach 4000 over in 127,170,171 al et al et al iil neto of infection ficial ntration, and and ntration, . Researchers Researchers . carried out to to out carried 133 evaluated evaluated Version postprint always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 972 972 971 970 969 968 967 966 965 964 963 962 961 960 959 958 957 956 955 954 953 952 951 950 949 973 973 rot diameter progression were recorded, Figure 9. T 9. Figure recorded, were progression diameter rot laxa dropl l 20 a with inoculated was fruit Each fruit. un of inoculation artificial of consisted tests The cerasifera access (7 plums diploid and accessions) (12 peaches and ‘Leonense’ x ‘Bolinha’) by dropinoculations. B dropinoculations. by ‘Bolinha’) x ‘Leonense’ and ‘Maciel’, x 672’ iden (‘Conserva crosses three were evaluated 1493’ ‘Cascata and 1218’ ‘Conserva 1596’, ‘Cons as such selections Interesting cultivars. and compa when component genetic significant a observed 10 (containing solution and 72 fruits infected of percentage the monitoring reported been have materials breeding r BR and inoculation, artificial with screened been intro as davidiana such materials, interesting very generated to resistance (including resistance pest on focused INRAAvigno In material. tested the in levels flesh no that suggesting test, injured the within spread als uninju the within progression work lesion of variability This processes. linked not r were epidermal resistance that suggested they Accordingly, tests. from rankings resistance BR the between correlation

Material from the breeding program of EmbrapaPelot of program breeding the from Material at a concentration of (10 of concentration a at resistance to peach materials peach materials to resistance and interspecific hybrids between them) at INRA, A INRA, at them) between hybrids interspecific and Comment citer cedocument: Journal ofAgriculturalandFoodChemistry 5 ACS Paragon PlusEnvironment spores/mL) over intact harvested fruits. The autho The fruits. harvested intact over spores/mL)

6 soe/l. ecnae fifce fut and fruits infected of Percentage spores/ml). 40 40 108 162 . . B sreig wr md by made were screenings BR . injured and artificially injured injured artificially and injured e ts n eysmlr rot similar very and test red resistance expressed at the the at expressed resistance et containing conidia of of conidia containing et roadsense heritability was heritability roadsense esistance results on these these on results esistance ‘Conserva 672’ x ‘A.334’ ‘A.334’ x 672’ ‘Conserva the uninjured and injured injured and uninjuredthe he authors observed no no observed authors he n, a breeding program program breeding a n, 6 atr paig a spraying after h 96 erva 1798’, ‘Conserva ‘Conserva 1798’, erva R by BR ions of of ions esistance and flesh flesh and esistance ring some selections selections some ring gression of of gression o highlighted high high highlighted o as (Brazil) has also also has (Brazil) as tified vignon, France. France. vignon, . salicinaP. . laxa M. 165 Authors . Prunus ) has has ) , , M. P. P. rs Page 40of72 Version postprint Page 41of72 always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 997 997 996 995 994 993 992 991 990 989 988 987 986 985 984 983 982 981 980 979 978 977 976 975 974 998 998 melting flesh peaches were selected selected were peaches flesh melting Offspri Italy). Bologna, of University at (formerly program breeding the in objective important an been equalresistance betterorof to be were determined t from seedlings Twelve 80%. around be to estimated spores/ml) in two points near peduncle cavity, incu cavity, peduncle near points two in of spores/ml) drop a with inoculation ethanol), (dilute disinfection fruit in consisting a procedures by evaluated been have resistance BR high showing s Italy), (CRAFRU, Rome of agriculture for council program breeding two from mostly reported been have phenotype scoring BRresistance obtaini seedlings, of numbers high bearing programs of on based strategies, phenotyping new us traits resistantrelated BR of dissection been has population this materials, prebreeding ‘Conte (cv. parent resistant the than resistance of individ with results interesting most the presented S humidity. relative ‘Eleg x ‘Contender’ The 95100% analysed. were combinations and 25ºC at incubation infe of percentage as registered was impact disease of suspension a with sprayed artificially

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spp. in peach cultivars for the fresh market has market fresh the for cultivars peach in spp. 175 . . 172,173 41 41 in plantain 174 . laxaM. . This group is currently developing developing currently is group This . . In these works, mature fruits were fruits mature works, these In . . laxa M. spray of conidial suspension suspension conidial of spray uals presenting higher levels levels higher presenting uals oiil upnin (10 suspension conidial sdu hpclrt and hypochlorite sodium d (10 ng from crosses between between crosses from ng than the ‘Bolinha’ cultivar. cultivar. than ‘Bolinha’ the dr) eie generating Besides nder’). bation for 7 days at 22ºC 22ºC at days 7 for bation everal apricot accessions accessions apricot everal cted fruits after 5 days of days 5 after fruits cted ng promising results for for results promising ng ant Lady’ F1 population population F1 Lady’ ant f nvriy f Milan of University of 5 ee he progenies three hese spores/ml), and the the and spores/ml), eful in the genetic genetic the in eful s. At the Regional Regional the At s. artificial inoculum inoculum artificial rtificial inoculation inoculation rtificial everal parental parental everal s n breeding in is 5

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M. fructicola 42 42 and 30,176,177 2 lesion, a storage rot rate of rate rot storage a lesion, y recommended combining combining recommended y ss. ss. M. laxa est value of resistance to to resistance of value est g the evaluated crosses, crosses, evaluated the g re than 50%). Based on on Based 50%). than re at BR resistance on the the on resistance BR at s soae o (natural rot storage ns, rs for 3 seasons: lesion lesion seasons: 3 for rs ust method to evaluate evaluate to method ust pollinations of cultivars cultivars of pollinations l) hwd 0 of 010% showed ely) on wounded, artificially artificially wounded, on t the Pacific AgriFood AgriFood Pacific the t . e: selections such as as such selections e: New Zealand). In this this In Zealand). New ike ‘493C11VIII8’ or or ‘493C11VIII8’ ike rial. Remarkably, the the Remarkably, rial. ivars and advanced advanced and ivars spore suspensions suspensions spore oorpark’), bred in in bred oorpark’), dity) and cuticle cuticle and dity) seasons), seasons), ’ and 9 and ’ Page 42of72 Version postprint Page 43of72 always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 1047 1047 1046 1045 1044 1043 1042 1041 1040 1039 1038 1037 1036 1035 1034 1033 1032 1031 1030 1029 1028 1027 1026 1025 1024 h pretg o rte fut bten ah genoty each between fruits rotten of percentage the inoculation). after h days 11 and 8 after assessment relative 9597% and 13ºC at incubation spores/ml; di fruit hypochlorite sodium and ethanol accession; inoculation artificial to submitted were genotypes Canada Columbia, British Centre, Research led b copd ne itgae ps cnrl st control orchard. in the chemical input exogenous minimize pest integrated under cropped be already the however, application; fungicide of suppression resis low too have still now to up found selections resistance BR improved with selections fruit high of cultivars in resistance introgress to germplas wider exploring that indicates differences section this in presented works the all in observed t the in differences consistent seasonally species, materials. insweet cherry highlev of nosources are there that demonstrating result the confirmed and accessions these of plants f avoid to enough not was level resistance observed ‘Staccato’(cultivars resistance high a showing cultivars some identified resistant less and mean to close mean, overall than resistance three established they mean, population

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43 43 170 . The ‘BR resistant’ cultivars and and cultivars resistant’ ‘BR The . 179 . During 4 years, a total of 36 36 of total a years, 4 During . quality could result in new new in result could quality ested materials have been been have materials ested m and using these sources sources these using and m (2550 fruits triplicates per per triplicates fruits (2550 el genetic resistance to BR BR to resistance genetic el Based on the difference in in difference the on Based than mean. Although they they Although mean. than s of Brown and Wilcox Wilcox and Brown of s level in two of four years four of two in level categories: more resistant resistant more categories: rssac i soe fruit stone in resistance f tance levels to allow the the allow to levels tance Te xsec o these of existence The . ifcin sry f 10 of spray sinfection; ungicide applications in applications ungicide most resistant could could resistant most pe and the overall overall the and pe mdt; R impact BR umidity; rategies, suited to to suited rategies, that the the that 180 4 ,

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181 and can now be exploited to radically radically to exploited be now can and 44 44 resistance to BR would allow allow would BR to resistance segregating trees. trees. segregating les in breeding programs. In programs. breeding in les gth. However, the variability the However, gth. n of resistance alleles into into alleles resistance of n g is a very time and effort and time very a is g d the interactions between between interactions the d able materials to generate generate to materials able and agronomical practices practices agronomical and ng in peaches, as well as as well as peaches, in ng Indeed, highthroughput highthroughput Indeed, o the variation in the the in variation the o cnutd o identify to conducted n studies, their principal principal their studies, rm genetic studies for for studies genetic rm results are frequently are results ity of fungicide inputs, fungicide of ity equence have been been have equence by timeconsuming timeconsuming by reig o BR for creening uh possible ough grams grams Page 44of72 Version postprint Page 45of72 always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 1096 1096 1095 1094 1093 1092 1091 1090 1089 1088 1087 1086 1085 1084 1083 1082 1081 1080 1079 1078 1077 1076 1075 1074 1073 1097 1097 ri rssac t B my e mliatr system multifactor a be may BR to resistance fruit of trait the control that regions genomic to linked a alleles favourable bearing seedlings of selection purposes these for strategy valuable a is selection resis BR enhanced with seedlings of selection early apnT aayi. h suy eeld he QTL, u three revealed study was The analysis. MappingQTL population, the through segregating SNPs 1037 program breeding Davis UC the in crossing and peach canning from derived accessions parental Davis (‘Dr. progeny PopDF the from seedlings 73 of 110 species. host peach using both published, been have resistance. higher confer fa different these of combination the be then would differe from coming may resistance of crosses factors different between loci detected of comparison the re may controll approach regions genome identify to step compulsory This resistance. of donor susceptib potential a between cross a from stemming progenies had resistance of QTL for seeking studies first the have studies association Therefore, understanding. co to lead mayresistance of sources different with facto these of part little a only hold may cultivar

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M. fructicolaM. 45 45 110 . A linkage map composed by composed map linkage A . rs, dealing at the same time time same the at dealing rs, resistance phenotypic data data phenotypic resistance nfusion rather than to better better to than rather nfusion interest. Considering that that Considering interest. ctors in elite genotypes to to genotypes elite in ctors nt donors. The final step step final The donors. nt ing resistance. Hopefully, resistance. ing t marker loci genetically genetically loci marker t focused on biparental biparental on focused a i alw te early the allows it as , o be eggd and engaged been not and that each different different each that and tance. Markerassisted Markerassisted tance. atnzGrí e al et MartinezGarcía f e tos o the for tools new of w o te i LG1 in them of two ’ x ‘F8, 1–42’), with with 1–42’), ‘F8, x ’ eclod back peachalmond ed to BRresistance BRresistance to ed present the first first the present help identifying identifying help le parent and a a and parent le e fr Interval for sed Version postprint always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 1120 1120 1119 1118 1117 1116 1115 1114 1113 1112 1111 1110 1109 1108 1107 1106 1105 1104 1103 1102 1101 1100 1099 1098 1121 1121 programs using similar genetic background. background. genetic using similar programs enhan to tools promising are region this of markers immunity effectortriggered and immunity, genes, triggered candidate potential two included region The year three with correlated significantly was LG1 in of LG4 inthe one and prahs te cnrbt t te ieaue regar literature the to contribute they approaches, the and backgro employed agent genetic pathogenic the different populations, the in differences to due inde and skin for fles mechanisms genetically controlled the confirming genome, peach of LG3 in located resistanc flesh Additionally respectively). genome, the in (located markers SSR EPPISF032 and M1a both between found were ph associations genotypephenotype covariate a as date maturity including model QTL h resistant); less as appeared individuals maturing wi negatively correlated seedlings of date maturity t resistance flesh and skin with associated markers ai The wound. artificial an of absence and presence infectio a artificial with SSR seasons two (63 for phenotyped markers 89 of set a with genotyped cross, ‘C the from individuals F1 meltingfleshed 80 using

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genome. The genomic region of one of the QTL the of one of region genomic The genome. 46 46 e was correlated with SNPs SNPs with correlated was e th their BR resistance (late resistance BR their th h resistance s of phenotypic evaluation. evaluation. phenotypic of s ns of of ns ontender’ x ‘Elegant Lady’ Lady’ ‘Elegant x ontender’ o BR o owever, using a Multiple Multiple a using owever, ig h ietfcto of identification the ding ce efficiency of breeding of efficiency ce (ETI) proteins. SNP SNP proteins. (ETI) m was to find genetic genetic find to was m different phenotyping phenotyping different LG2 and 4 of4 and LG2 und of the studied studied the of und . fructigenaM. kn eitne and resistance skin ntp, significant enotype, pendence between between pendence 174 oig o PAMP for coding studies, probably probably studies, d 6 N) and SNP) 26 nd . . In this material, material, this In 132 . . performed performed Prunus , in the the in ,

Page 46of72 Version postprint Page 47of72 always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 1144 1144 1143 1142 1141 1140 1139 1138 1137 1136 1135 1134 1133 1132 1131 1130 1129 1128 1127 1126 1125 1124 1123 1122 1145 1145 f hntpn ae oeoty n te eeomn o development the and noteworthy are phenotyping of nota However, sense. this in made been has progress resistant cultivars of development the and sources enhanced BRresistance. sel assisted for markers genetic useful potentially and host resistance processes; nevertheless, the sc the nevertheless, processes; resistance host and elemen important some validated and identified have l the In plums. and cherries peaches, in especially some in doors” “open of presence pathogen high of relatively success the for causes main the of one infec and impact disease for condition strict a not involved between elements the about literature contemporary to sustai more contribute could control strategies, together that, BRresistance enhanced with hybrids the across sources t needed are approaches Such way. robust a in level ab strategies phenotyping designing for crucial are that Conclusion 7 moving forward. of waysfind helpstudies to may

h rsac cmuiy a ivse i te identifi the in invested has community research The Prunus In this review we have collected the information av information collected the havewe thisreview In biolo the mechanisms, pathogenesis BR Understanding Monilinia fruit can offer to offer can fruit Comment citer cedocument: spp. and spp. Journal ofAgriculturalandFoodChemistry Prunus ACS Paragon PlusEnvironment

emls ad rvd tos o bedn new breeding for tools provide and germplasm Prunus Monilinia fruit. We conclude that host specificity is is specificity host that conclude We fruit. spp. and the interaction between them, them, between interaction the and spp. 47 47 nable stone fruit cropping. fruit stone nable ection of new cultivars with with cultivars new of ection tion development and that that and development tion ientific community has not has community ientific le to measure resistance resistance measure to le ast decade, many works works many decade, ast ts of the fungal infection infection fungal the of ts to BR. Up to now, little little now, to Up BR. to Prunus ble advances in terms terms in advances ble with other alternative alternative other with qatttv genetic quantitative f ailable in historic and inhistoric ailable o identify resistance resistance identify o in the interaction interaction the in cation of resistance resistance of cation colonisation is the the is colonisation fruit’ epidermis, epidermis, fruit’ gical barriers barriers gical Version postprint always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 1167 1167 1166 1165 1164 1163 1162 1161 1160 1159 1158 1157 1156 1155 1154 1153 1152 1151 1150 1149 1148 1147 1146 1169 1169 1168 elements, but has to be considered in the generatio inthe considered be has to but elements, cle a hampers that constraint persistent a been has environment that influence significant the Finally, among diversity phenotypic the explains r BR precise a generate to elements these assembled article. article. Engli of revision exhaustive the for Blanco, Estela We fellowship. doctoral the supported who Education Insert th and foundation Academy CAPES the thanks L.O.L 79140020). and 74130043 No. Fellowship Doctoral by C was workfunded IP FP7265582). Frame Program; Acknowledgments 8 sources. inoculum natural strategies agronomical adopting by and initiatives, imposed (or asrecommended fungicides, synthetic of by caused damages combat to task difficult the have s validated and developed control pathogen sustainable and breeds resistant and pre the at control BR for methods alternative breeding, for approaches phenotyping new of design

This work was funded by ‘FruitBreedomics’ European European ‘FruitBreedomics’ by funded was work This Information Funding These elements constitute valuable information and and information valuable constitute elements These Comment citer cedocument: Journal ofAgriculturalandFoodChemistry ACS Paragon PlusEnvironment 14

, 9 . In the meantime, stone and pome fruit growers growers fruit pome and stone meantime, the In . 48 48 Prunus has in the infection process process infection the in has species and their varieties. varieties. their and species and practices to eliminate eliminate to practices and n of new of varieties. n othret tgs BR stages. postharvest BR with lower quantities quantities lower with BR ) by IPM regulations and and regulations IPM by ) r dniiain f such of identification ar h rsnain f this of presentation sh s el st ts new test to as well as e Brazilian Ministry of of Ministry Brazilian e would also thank to to thank also would ONICYT, Chile (Post Chile ONICYT, ssac mdl that model esistance trategies are being being are trategies are useful in the the in useful are Project (Seventh (Seventh Project ion Grant No. No. Grant ion Page 48of72 Version postprint Page 49of72 always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 1206 1206 1205 1204 1203 1202 1201 1200 1199 1198 1197 1196 1195 1194 1193 1192 1191 1190 1189 1188 1187 1186 1185 1184 1183 1182 1181 1180 1179 1178 1177 1176 1175 1174 1173 1172 1171 1170 1209 1209 1208 1207 . ol, . Glri G; uln, . . A review A L., M. Gullino, G.; Gilardi, P.; 515523. (5), Colla, ve the in management disease soilborne of situation parli 3. European the of 2009/128/ec Directive http://www.eppo.int/PPPRODUCTS/information/2009_012 EPPO ac to action community for framework a establishing organ agriculture and 2. food of Database FAOSTAT http://faostat3.fao.org/browse/Q/QC/E. 1. References 9 J Bot 1997, 84 (5), 686. 686. (5), 84 J 1997, Bot Schum K.; Jakobsen, L.; Kohn, A.; HolstJensen, of evolution 15. 17. Epid X.M., Xu, P.; Jeffries, N.; Rungjindamai, by caused fruit stone on Guillermin, 14. F.; Merlin, D.; Plenet, C.; Bussi, pruning. and training tree with inpeach incidence 13. Lescourret, D.; Plenet, C.; Bussi, V.; Mercier, Cro in peach. incidence rot brown on pruning manual P Quarantine as Regulated 12. Pests A2 of List EPPO http://www.eppo.org/QUARANTINE/listA2.htm. 11. https://www.rosbreed. Rot. Brown Peach RosBREED 2016). 14, 10. M., Mari, C.; Martini, Inc Elsevier Strategies, Control Decay: Postharvest 9. X., C. Luo, G.; Schnabel, D.; K. Cox, J.; M. Hu, 6 (9). 2011, ONE PLoS in China. peach of Mich 8. Y.; Luo, P.; J. Xu, Y.; L. Guo, Y.; J. 206212. (2), 57 2010, Microbiology Eukaryotic Fan, of populations 7. structure Population L., Guo, X.; Chen, X.; Zhu, 12851291. 95 (10), 2011, Plant Disease China. 6. e0132012. 10 (6), 2015, PLoS ONE Bo B J.F.; the in Ho, Virulence P.L.; Diminishes Yu, Overexpression F.Y.; MfPG1 Yu, C.M.; Chou, Endopolygalactur Five of Expression M.H., Lee, W.; 5. and 2006 Usage and 2015). Sales Industry Pesticide http://www.epa.gov/opp00001/pestsales/07pestsales/m EPA Preventio of Office Agency Protection Environmental 4.

Monilinia oiii fructicola Monilinia Comment citer cedocument: (Sclerotiniaceae) based on coding and noncoding rD noncoding and coding on based (Sclerotiniaceae) Journal ofAgriculturalandFoodChemistry Monilinia laxaMonilinia ACS Paragon PlusEnvironment Monilinia fructicolaMonilinia

fni acmct, eoils fo Cia Journa China. from helotiales) ascomycota, (fungi, . European Journal of Plant Pathology 2014, 140 (1) 140 2014, Pathology Plant of Journal European . 49 49 , Monilinia laxa Monilinia Fruits 2015, 70 (5), 303309. 303309. 70 (5), 2015, Fruits .: 2014; pp 233265. 233265. pp 2014; .: getable sector. Phytoparasitica 2012, 40 40 2012, Phytoparasitica sector. getable p Protection: 2008; Vol. 27, pp 678688. pp 678688. 27, Vol. 2008; Protection: p hieve the sustainable use of pesticides. pesticides. of use sustainable the hieve emiology and management of brown rot rot brown of management and emiology rown Rot Pathogen Pathogen Rot rown F., Effects of limiting irrigation and of of and irrigation limiting of Effects F., onase Genes and Demonstration that that Demonstration and Genes onase n, Pesticides, and Toxic Substances. Substances. Toxic and Pesticides, n, and critical analysis of the European European the of analysis critical and stock, R. M.; Chung, K.R.; Huang, J. Huang, K.R.; Chung, M.; R. stock, arket_estimates2007 (accessed Nov. Nov. (accessed arket_estimates2007

A.; Mercier, V., Limiting brown rot rot brown Limiting V., Mercier, A.; of brown rot fungi on stone fruits in in fruits stone on fungi rot brown of Monilinia acher, T., Molecular phylogeny and and phylogeny Molecular T., acher, 8_EUe.pdf 8_EUe.pdf ailides, T. J., Genetic diversity of of diversity Genetic J., T. ailides, ( ization of the united nations. nations. united the of ization org/node/424 (accessed Apr. Apr. (accessed org/node/424 ament and of the council: council: the of and ament Monilinia ests in the EPPO Region. Region. EPPO the in ests species causing brown rot rot brown causing species 2007 Market Estimates. Estimates. Market 2007 Rot, Brown Rot). In In Rot). Brown Rot, NA sequences. Am Am sequences. NA Monilinia fructicolaMonilinia l of of l , 1 , . . Version postprint always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 1247 1247 1246 1245 1244 1243 1242 1241 1240 1239 1238 1237 1236 1235 1234 1233 1232 1231 1230 1229 1228 1227 1226 1225 1224 1223 1222 1221 1220 1219 1218 1217 1216 1215 1214 1213 1212 1211 1210 1250 1250 1249 1248 9 MMns P S; et V M; oad R P, Inf P., R. Voland, M.; V. Best, S.; P. McManus, Monilinia 19. Infectio Fruit A Stretch, and J.;45 2010, Hortscience Analysis. Components Principal J. Blight Polashock, K.; Berry M. Mummy Ehlenfeldt, for Blueberry 18. (12), 76 1998, DeBotanique Canadienne BotanyRevue Del A., H. Kesteren, van M.; C. G. Leeuwen, van ( crops fruit of 17. 1 Frtr H; dsae, . Ery rw rt inf rot brown Early J., Adaskaveg, H.; Forster, by detected 31. Ide J., A. Meldrum, C.; 121912 (11), 88 2004, Disease Plant PCR. M. multiplex Tardif, J.; M. Côté, fructicola 30. F J., Jakse, B.; Javornik, F.; Celar, T.; Gril, fructicola 29. J B.; Javornik, 16161624. A.; Munda, F.; Celar, T.; Gril, between variation 28. PCR Nested J., T. Michailides, 312322. (6), 151 2003, Phytopathology of Journal Y.; Luo, Z.; Ma, fructicola 27. 548555. (3), 59 2010, Pathology Plant crops. fruit Lee van L.; M. Bruil, R.; I. differentiate Brouwershaven, van to assay PCR (TaqMan) time 26. Sp J., T. Michailides, Z.; Ma, A.; W. E. Boehm, fructicola groupI rDNA SSU 25. of Use A., Brown, C.; Fulton, fructicola 24. Monili H., 4. Deplaude, G., la Phytoma verger. le dès pêches Martinot, sur monilioses de V., Mercier, p méthode une : répartition leur évaluer et espèces 23. within variation Genomic P., 373378. (4), 106 2000, Pathology Frey, R.; Ioos, fructicola 22. An T., Schumacher, M.; Vaage, A.; HolstJensen, of B Journal Nordic genera. related and sclerotinia T., 21. Schumacher, M.; L. Kohn, A.; HolstJensen, 885899. (6), 89 1997, Mycologia Sclerotiniaceae. 20. 11271130. (12), 89 1999, 16. Honey, E. E., The Monilioid Species of Scleroti of Species Monilioid The E., E. Honey, 16.

xcci n eauto o clias o resistanc for cultivars of evaluation and oxycocci , , von . FluoreszenzAFLPfingerprinting dothide Botryosphaeria and orchards fruit stone in Phytopat flowers. and stone fruits california from Le Microbiology Fems Mfructigena. and Mlaxa from PCR. by identification species to application and , . laxaM. Monilinia Monilinia Comment citer cedocument: ad oii plsrm o iouae ad naturall and inoculated on polystroma Monilia and , oiii laxa Monilinia specific DNA primers. Phytopathology 2000, 90 (2), 90 2000, Phytopathology primers. DNA specific Journal ofAgriculturalandFoodChemistry spp.) on the basis of quantitative characteristics quantitative of basis the on spp.) ACS Paragon PlusEnvironment

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otany 1998, 18 (6), 705719. 705719. (6), 18 1998, otany luorescent AFLP fingerprinting of of fingerprinting AFLP luorescent our différencier les trois espèces d'agents d'agents espèces trois les différencier our 25. 25. Défense des Végétaux 2009, (626627), (626627), 2009, Végétaux des Défense (8), 12051210. 12051210. (8), akse, J., AFLP analysis of intraspecific intraspecific of analysis AFLP J., akse, nia. Mycologia 1928, 20 (3), 127157. 127157. (3), 20 1928, nia. Mycologia . W.; Kramer, M., Ranking Cultivated Cultivated Ranking M., Kramer, W.; . oiii laxa Monilinia uwen, G. C. M.; Kox, L. F. F., A real A F., F. L. Kox, M.; C. G. uwen, n Incidence Using Resampling and and Resampling Using Incidence n 20422050. 20422050. ntification of of ntification cepcfc eeto of detection eciesspecific ineation of the three brown rot fungi fungi rot brown three the of ineation hology 2001, 91 (5), 428439. 428439. 91(5), 2001, hology approximation to the phylogeny of of phylogeny the to approximation assays for detection of of detection for assays ections in sweet cherry fruit are are fruit cherry sweet in ections oses du pêcher, déterminer les les déterminer pêcher, du oses Nuclear rDNA phylogeny of the the of phylogeny rDNA Nuclear ection of cranberry flowers by by flowers cranberry of ection e to cottonball. Phytopathology Phytopathology cottonball. to e a from pistachios in California. California. in pistachios from a tters 1997, 157 (2), 307312. 307312. (2), 157 1997, tters intron to distinguish distinguish to intron from other brown rot fungi of of fungi rot brown other from European Journal of Plant Plant of Journal European 2010, 117 (4), 168172. 168172. (4), 117 2010, , oiii fructigena Monilinia . fructigena M. . Canadian Journal of of Journal Canadian . y infected fruit using using fruit infected y 171178. 171178. 92 (12), (12), 92 Monilinia Monilinia Monilinia Monilinia Monilinia Monilinia Monilinia Monilinia and and , , M. M. M. M. Page 50of72 Version postprint Page 51of72 always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 1289 1289 1288 1287 1286 1285 1284 1283 1282 1281 1280 1279 1278 1277 1276 1275 1274 1273 1272 1271 1270 1269 1268 1267 1266 1265 1264 1263 1262 1261 1260 1259 1258 1257 1256 1255 1254 1253 1252 1251 1292 1292 1291 1290 . Mnrn J F; ihu J; e rb, . . Us O.; X. Eribe, De J.; Lichou, F.; J. Mandrin, A.; 26292637. 103 (6), 2007, Microbiology Applied 34. Petroczy, M.; Palkovics, L., First report of br of report First L., Palkovics, M.; Petroczy, 90 ( 2006, Disease Plant Hungary. in peach imported 34. differ Two P., Melgarejo, J.; of Cubero, identification and I.; rot Gell, brown of diagnosis 33. 199 Pathogens of Plant Identification and Diagnosis of identification and detection the for P., VanHalteren, A.; MaulerMachnik, J.; Frahm, M.; 5 Cx K; iln, . Re, . Fee, . Fau J.; (P. Freier, Apricot on Blight J.; Shoot Raes, ( S.; Cherry Villani, Sweet K.; on Cox, Rot Fruit Brown of Reports 45. Eur 783. of Confirmation D., K. Cox, M.; S. Villani, laxa 44. variation 7077. (1), 21 Genetic 1999, L., A. Jones, L.; C. Snyder, and 43. Ang L.; Mio, L.; Camargo, S149. A.; Fazza, D.; Souza, laxa Monilinia 42. 192194. 67 (2), 2013, Sciences Applied and Exact, Aca Latvian the K., of Lesik, Proceedings Belarus. in orchards 41. a Morphological J., Bech, A.; de aislados Moret, Z.; Muñoz, Monilinia 40. W Pathology Plant of Journal Zeviani, Canadian Brazil. State, A.; F. Silva, F.; S. P. Lichtemberg, for methods physiological and macromorphological 39. Pathol Plant of Journal European Spain. in orchards Segarra, N.; Lamarca, B.; Eguen, M.; Villarino, of Occurrence 38. 305310. 32(2), 2005, Control (M.; rot Liñán, A.; brown Cal, De R.; Torres, I.; Larena, Rot Brown 37. The L., H. Willetts, W.; J. R. Byrde, p 171. 1977; Oxford, control. 36. 763. Mel I.; Viñas, J.; Usall, I.; Gell, A.; Cal, De by 35. 32. Banks, J.; Rizvi, R.; Lane, C.; Hughes, K.; Coo K.; Hughes, C.; Lane, R.; Rizvi, J.; Banks, 32.

Monilinia fructicola Monilinia on Tart Cherry, Cherry, Tart on oiii laxa Monilinia sp. isolates and pathogenicity on apple. Caracteri apple. on pathogenicity and isolates sp. Monilinia Monilinia asn bon o o pahs n rzl Phytopatho Brazil. in peaches on rot brown causing oiii laxa Monilinia Comment citer cedocument: Monilinia sltd rm hris n ihgn Cnda Journ Canadian Michigan. in cherries from isolated p. o pahs y il apiain o Epicoccu of applications field by peaches of spp.) Prunus spp. y pruebas de patogenicidad sobre manzana 2008 manzana sobre patogenicidad de pruebas y spp. in peach orchards in Ebro Valley, Spain. Plant Dis Plant Spain. Valley, Ebro in orchards peach in Journal ofAgriculturalandFoodChemistry species causing fruit brown rot, blossom and twig twig and blossom rot, brown fruit causing species armeniaca cerasus, in Western New York. Plant Disease 2010, 2010, Disease Plant York. New Western in cerasus, ACS Paragon PlusEnvironment n Mfutgn atr nrdcin f Mfructicol of introduction after Mfructigena and

Monilinia ), Kwanzan Cherry (P. serrulata), and Sweet Cherry Cherry Sweet and serrulata), (P. Cherry Kwanzan ), 51 51 spp causing brown rot of stone and Pome fruit. fruit. Pome and stone of rot brown causing spp Monilinia Prunus 2014, 36 (1), 3847. 3847. (1), 36 2014, caused rot brown of report First P., garejo, 7, 11, 391393. 391393. 11, 7, ogy 2013, 137 (4), 835845. 835845. (4), 137 2013, ogy own rot caused by by caused rot own Monilinia all, J., Biological control of postharvest postharvest of control Biological J., all, 3), 375375. 375375. 3), bert, H.; Cooley, D.; Clements, J., First First J., Clements, D.; Cooley, H.; bert, Development of monoclonal antibodies antibodies monoclonal of Development demy of Sciences, Section B: Natural, Natural, B: Section Sciences, of demy opean Brown Rot Caused by by Caused Rot Brown opean Melgarejo, P.; Domenichini, P.; Bellini, Bellini, P.; Domenichini, P.; Melgarejo, k, R.; Dehne, H.; Adam, G.; Diekmann, Diekmann, G.; Adam, H.; Dehne, R.; k, J.; Usall, J.; Melgarejo, P.; De Cal, A., Cal, De P.; Melgarejo, J.; Usall, J.;

. M.; De Mio, L. L. M., Comparison of of Comparison M., L. L. Mio, De M.; . between strains of of strains between spp. in stone fruit trees. Journal of of Journal trees. fruit stone in spp. avium ent PCR approaches for universal universal for approaches PCR ent Fungi of Fruit: Their biology and and biology Their Fruit: of Fungi eli, S.; Amorim, L., First report of of report First L., Amorim, S.; eli, zación morfológica y molecular de de molecular y morfológica zación nd molecular characterization of of characterization molecular nd species identification in Parana Parana in identification species ) and Plum (P. (P. Plum and ) oy 08 9 () S148 (6), 98 2008, logy Monilinia fructicola Monilinia al of Plant Pathology Pathology Plant of al m nigrum. Biological Biological nigrum. m ease 2009, 93 (7), (7), 93 2009, ease Monilinia fructicola Monilinia , 42 (1), 119128. 119128. 42(1), , domestica blight in apple apple in blight 94 (6), 783 (6), 94 a in peach peach in a Monilinia Monilinia ) and and ) on on (P. (P.

Version postprint always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 1330 1330 1329 1328 1327 1326 1325 1324 1323 1322 1321 1320 1319 1318 1317 1316 1315 1314 1313 1312 1311 1310 1309 1308 1307 1306 1305 1304 1303 1302 1301 1300 1299 1298 1297 1296 1295 1294 1293 1332 1332 1331 Affecting Peach Orchards in Slovenia. Plant Disease Plant in Slovenia. Orchards Peach Affecting by Caused Apple 48. Lichou J., M. J. F., Bréniaux D., Mercier V., G V., Mercier D., Bréniaux F., J. M. J., Lichou 48. N L.; A. Valencia, 160. (1), 98 2014, Disease Plant A.; inChile. fruit G. Díaz, A.; B. Latorre, of report First P., J. Zoffoli, 47. Detection 29392943. (3), 3 A., Ghasemnezhad, S.; Nasrollanejad, Australian Iran. Northern in rot brown fruit stone 46. 15841585. (12), 95 2011, Disease 60. Beckerman, J. L.; Creswell, T., First Report of Report First T., Creswell, L.; J. Beckerman, Disea Plant mas). (Cornus Cherry Cornelian Dogwood, 60. Melgar (4), 132 2012, Pathology F.; Plant of Journal European Martinez, I.; Larena, M.; Villarino, in diversity 59. Fi K., Bacigálová, M.; Hudecová, N.; Ondejková, 2010, Science Protection Plant Republic. Slovak the 58. A., 855865. (4), 135 2013, Bielenin, M.; Polan Michalecka, in A.; fruits stone Poniatowska, and pome of rot brown causing 57. coun neighbouring from 247254. 61(2), 2012, Pathology pathogen the of Bro introduction M.; HilberBodmer, E.; of J. analysis Frey, M.; marker Jänsch, SSR A., Patocchi, G.; 56. Repor First M., Mari, A.; Spadoni, C.; Martini, fructicola 55. A.; Garibaldi, L.; M. Gullino, C.; Pellegrino, by caused stone fruit Rot Brown of 54. Report First M., Marn, A.; Munda, 53. E Zapletalova, I.; 907907 91 (7), 2007, Disease Plant Republic. Czech Siruckova, J.; by caused Duchoslavova, rot brown of report 52. Schnab P.; Bryson, C.; Luo, M.; Hu, A.; Grabke, 51. Fi A., Patocchi, M.; Bunter, M.; HilberBodmer, fructicola Monilinia 50. 15541554. (12), 90 2006, Plant Disease B H.; Scharer, M.; HilberBodmer, E.; Bosshard, pathogen rot brown quarantine 49. Ph fructicola. Monilia : moniliose nouvelle Une E., avium

Cue by Caused ) on Apple in Italy. Plant Disease 2013, 97 (5), 689 (5), 97 2013, Disease Plant in Italy. Apple on Monilinia fructicola Monilinia Comment citer cedocument: Monilinia fructicola Monilinia on Apricot in a Swiss Orchard. Plant Disease 2010, Disease Plant Orchard. Swiss in a Apricot on oiii laxa Monilinia Monilinia fructicola Monilinia Journal ofAgriculturalandFoodChemistry ACS Paragon PlusEnvironment Monilinia fructicola Monilinia from the Ebro Valley in Spain using ISSR and RAPD RAPD and ISSR using Spain in Valley Ebro the from

oiii fructicola Monilinia oiii fructicola Monilinia n e Yr, hd Iln, n Msahsts Plan Massachusetts. and Island, Rhode York, New in in Germany. Plant Disease 2011, 95 (6), 772772. 772772. 95 (6), 2011, Disease Plant Germany. in in Italy. Plant Disease 2009, 93 (6), 668. 668. (6), 93 2009, Disease Plant inItaly. oiii fructicola Monilinia 52 52 causing brown rot on stored Japanese plum plum Japanese stored on rot brown causing Journal of Basic and Applied Sciences 2009, 2009, Sciences Applied and Basic of Journal ytoma 2002, 547, 2225. 2225. 547, 2002, ytoma on various stone and pome fruits in the the in fruits pome and stone various on on imported stone fruits in Switzerland. Switzerland. in fruits stone imported on 511524. 511524. 181184. (4), 46 2010, 94 (9), 11661166. 11661166. 94 (9), 2010, Spadaro, D., First report of brown rot of of rot brown of report First D., Spadaro, . . d. European Journal of Plant Pathology Pathology Plant of Journal European d. ejo, P.; de Cal, A., Analysis of genetic genetic of Analysis A., Cal, de P.; ejo, iauque P, Debrus D., Blanc P, Belluau Belluau P, Blanc D., Debrus P, iauque Brown Rot (Rot Brown se 2014, 98 (9), 12751276. 12751276. 98 (9), 2014, se aranjo, P.; Ferrada, E. E.; Torres, R.; R.; Torres, E.; E. Ferrada, P.; aranjo, o Bon o Cue by Caused Rot Brown of t unter, M.; Duffy, B., First report of the the of report First B., Duffy, M.; unter, Characteristic of of Characteristic ggini, G. A. L.; Weger, J.; Schnabel, Schnabel, J.; Weger, L.; A. G. ggini, s Rpr o Bon o Cue by Caused Rot Brown of Report rst tries and the United States. Plant Plant States. United the and tries el, G., First Report of Brown Rot of of Rot Brown of Report First G., el, .; Navratil, M.; Safarova, D., First First D., Safarova, M.; Navratil, .; rst report on on report rst 689. 689. and identification causal agent of of agent causal identification and asd by Caused from Swiss apricots suggests suggests apricots Swiss from Monilinia fructicola Monilinia 94 (5), 643643. 643643. 94 (5), oiii fructicola Monilinia Monilinia oiii fructicola Monilinia spp. fungi fungi spp. Monilinia Monilinia markers. markers. ) on the the on ) in in t t

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Monilinia in Canada. Plant Disease 2003, 87 (10), 12681268. (10), 87 2003, Disease Plant in Canada. showing host specificity. Food Technology and and Technology Food specificity. host showing M. fructigena M. Monilinia fructicola Monilinia species causing brown rot of stone and pome fruit fruit pome and stone of rot brown causing species Prunus in China. Plant Disease 2013, 97 (9), 1249. 1249. (9), 97 2013, Disease Plant in China. 53 53

mume stance. Pest Management Science 2011, 2011, Science Management Pest stance. ccessed April 1st). 1st). April ccessed o rw rt ( rot brown to oii polystroma Monilia 343347. 343347. ocereus polyrhizus). African Journal of of Journal African polyrhizus). ocereus . Mycological Research 2002, 106, 444 106, 2002, Research Mycological . 2009. 2009. of brown rot on rot brown of in Japan. Journal of General Plant Plant General of Journal Japan. in , J. F.; Pierobom, C. R.; Da Silva, J. J. Silva, Da R.; C. Pierobom, F.; J. , ., Distinction of the Asiatic brown rot rot brown Asiatic the of Distinction ., H., First report of brown rot in wine wine in rot brown of report First H., veg, J. E., Suppression of of Suppression E., J. veg, rnal of the American Pomological Pomological American the of rnal ., Proteome analysis of the plant plant the of analysis Proteome ., , K. D., Characterization of the the of Characterization D., K. , E., Genetic variation among and and among variation Genetic E., . Journal of Phytopathology 1992, 1992, Phytopathology of Journal . urne n fut ult o pre of quality fruit and currence ciah, . Sn, T., Sano, Y.; Ichihashi, t n lm asd by Caused Plum on ot nt of Resistance of Wounds on on Wounds of Resistance of nt aa ( paya acids. Physiological and and Physiological acids. oiii fructicola Monilinia heoee lagenaria Chaenomeles oiii fructicola Monilinia . European Journal of of Journal European . on apple in Hungary. Hungary. in apple on Crataegus pinnatifida Crataegus Monilinia Monilinia (Wint.) (Wint.) Monilia Monilia Monilia Monilia

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Monilinia fructicolaMonilinia species in apple fruit. Indian Phytopathology 1990 Phytopathology Indian fruit. in apple species on peach fruit. Postharvest Biology and Technology and Biology Postharvest fruit. peach on oiii fructicola Monilinia Monilinia fructicola Monilinia Monilinia fructicolaMonilinia Monilinia laxa Monilinia Comment citer cedocument: . Plant disease (USA) 1988. 1988. (USA) disease . Plant oiii laxa Monilinia Journal ofAgriculturalandFoodChemistry on Apricots. Journal of Phytopathology 1992, 136, 136, 1992, Phytopathology of Journal Apricots. on ACS Paragon PlusEnvironment . European Journal of Plant Pathology 2014, 140 (3) 140 2014, Pathology Plant of Journal European .

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during bean infection. Applied and Environmental M Environmental and Applied infection. bean during oiii fructicola Monilinia Comment citer cedocument: Magnaporthe grisea Magnaporthe Magnaporthe grisea Magnaporthe Journal ofAgriculturalandFoodChemistry oiii laxa Monilinia Monilinia fructicola Monilinia Prunus ACS Paragon PlusEnvironment

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W.; Akinrefon, O. A., Changes in in Changes A., O. Akinrefon, W.; by which contact with plant cuticle cuticle plant with contact which by ssible Relevance of Extracellular Extracellular of Relevance ssible ournal of the American Society for for Society American the of ournal Sclerotinia fructicola Sclerotinia t epicuticular waxes. In The plant plant The In waxes. epicuticular t ases in Phytopathogenic Fungi. Fungi. Phytopathogenic in ases hemical components. In Acta Acta In components. hemical ce ce . Botanical Gazette 1920, 70 70 1920, Gazette Botanical . oiii laxa Monilinia . Euphytica 1994, 77 (12), (12), 77 1994, Euphytica . f. sp. pisi. Proceedings of of Proceedings pisi. sp. f. Monilinia fructicola Monilinia (Wint.) Rehm, Rehm, (Wint.) Monilinia Infection by by Infection . . 49 (5), (5), 49 . Plant Plant . fruc Version postprint always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 1577 1577 1576 1575 1574 1573 1572 1571 1570 1569 1568 1567 1566 1565 1564 1563 1562 1561 1560 1559 1558 1557 1556 1555 1554 1553 1552 1551 1550 1549 1548 1547 1546 1545 1544 1543 1542 1541 1540 1539 1580 1580 1579 1578 and appressorium formation by the conidia of of conidia the by waxes formation Cuticular E., P. fo appressorium Kolattukudy, Y.; Hegde, and appressorium 140. and germination trigger P. Kolattukudy, gloeosporioides M.; L. wax Rogers, K.; G. Podila, surface lip Surface 139. A., Yephremov, J.; J. 540549. 47 (6), 2009, ReinaPinto, Biochemistry and Physiology 138. 1995; Scotland, Press: Oily Ed. E., J. R. Hamilton, through specific interactions with the membrane lip membrane with the interactions specific through (C peach Moser, M.; The Bellucci, E., M.; Zanetti, Baraldi, V.; Nanni, M.; 151. modulating Mechanisms A., 281289. Lichter, J European D.; control. their and interactions Prusky, pathogen 150. pyroquil of Effects P., Melgarejo, A.; Cal, De laxa 149. D B. Hammock, J.; T.fructicola Monilinia expression Michailides, and Y.; characterization, G. cloning, Wang, Molecular 148. Li T., R. Sherwood, K.; T. Kirk, P.; C. 2 18 (1), 1980, Vance, Phytopathol. Rev. Annu. Resistance. 147. 2 Journal Plant The loss. water transpirational not microbia to resistance affects consistently cuticle J Rose, A.; M. Buda J.; Jenks, A. E.; Matas, R. K.; D. Stark, Kosma, D.; T.; J. Isaacson, Batteas, 146. Coluccia M.; Torres, M.; 20 Serrano, Science J.; Plant in Metraux, Frontiers pathogens. to defense 145. from 619628. evidence (6), 23 2000, Environment layers: distinct c Leaf mechanically M., Riederer, S.; Schaffer, R.; Jetter, and 144. 251263. (1), 177 2008, Phytologist G. Vogg, G.; Bringmann, M.; Stangl, V.; processes prepenetration affect Zabka, properties surface 143. 3340. (13), 68 2006, Pathology Plant st wheat the in differentiation structure infection Moer U.; Daniels, component active C.; morphogenetically Gorzelanny, a K.; is Reisige, octacosanal 142. 419426. 103, 1999, Research Mycological Arche A.; Beckett, viru M.; and T. germination the Butt, on N.; extracts leaf E. and Inyang, waxes 141. 7584. (2), 51 1997, Pathology Plant Molecular 3. inh, . Pat ae. n ae: Chemistry, Waxes: In waxes. Plant G., Bianchi, 137.

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persica ) defensin PpDFN1 displays antifungal activity activity antifungal displays PpDFN1 defensin ) 58 58 em rust fungus. Physiological and Molecular Molecular and Physiological fungus. rust em l infection and biomechanical properties, but but properties, biomechanical and infection l 009, 60 (2), 363377. 363377. 60 (2), 009, pp 176–222. 176–222. pp ids. Plant Pathology 2013, 62 (2), 393403. 393403. (2), 62 2013, Pathology Plant ids. . K. C., Cutin deficiency in the tomato fruit fruit tomato the in deficiency Cutin C., K. . in the barley powdery mildew fungus. New New fungus. mildew powdery barley the in 14, 5, 274. 5, 274. 14, uticular waxes are arranged in chemically chemically in arranged are waxes uticular 59288. 59288. anprh grisea Magnaporthe Prunus ournal of Plant Pathology 2008, 121 (3), (3), 121 2008, Pathology Plant of ournal lence of of lence on on the infection process of of process infection the on on of a redoxresponsive cutinase from from cutinase redoxresponsive a of , F.; L’Haridon, F., The cuticle and plant plant and cuticle The F., L’Haridon, F.; , r, S., The effect of crucifer epicuticular epicuticular crucifer of effect The S., r, .; Bertolini, P.; Guella, G.; Dalla Serra, Serra, Dalla G.; Guella, P.; Bertolini, .; Disease of Mechanism a as gnification involved in host plant recognition and and recognition plant host in involved 39 (4), 267269. 267269. (4), 39 schbacher, B. M., The C28 aldehyde aldehyde C28 The M., B. schbacher, , G. J.; He, Y.; Yu, B.; Pravitasari, A.; Pravitasari, B.; Yu, Y.; He, J.; G. , relieve selfinhibition of germination germination of selfinhibition relieve ; Riederer, M.; Hildebrandt, U., Host Host U., Hildebrandt, M.; Riederer, ; E., Chemical signals from avocado avocado from signals Chemical E., Molecular Biology and Functions, Functions, and Biology Molecular

ids and plant defenses. Plant Plant defenses. plant and ids laurocerasus fungal attack in postharvest postharvest in attack fungal .; Lee, Y. M.; Bostock, R. M., M., R. Bostock, M.; Y. Lee, .; Metarhizium anisopliae Metarhizium rmation in in rmation 5 (3), 261276. 261276. (3), 5 . Physiological and and Physiological . L. Plant Cell and and Cell Plant L. Colletotrichum Colletotrichum Monilinia Monilinia conidia. conidia. Page 58of72 Version postprint Page 59of72 always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 1619 1619 1618 1617 1616 1615 1614 1613 1612 1611 1610 1609 1608 1607 1606 1605 1604 1603 1602 1601 1600 1599 1598 1597 1596 1595 1594 1593 1592 1591 1590 1589 1588 1587 1586 1585 1584 1583 1582 1581 1620 1620 Cell Rep 2009, 28 (1), 95102. 95102. 28 (1), 2009, Rep Cell Er p A.; (PR10) 10 Taheri, related S.; pathogenesis Jayasankar, plum A.; a of Elkereamy, analysis 154. 435451. 5 (5), 2004, Pathology G. G. Farrell, J.; F. Sturgess, J.; A. oxidative to L. respond genes PR10 Mur, endogenous certain 153. o Journal elicitors. other and wounding, filtrates, response in peach in levels mRNA beta1,3glucanase (Wint.) Honey em frutos. Revista Ceres 2008, 55 (2) 55 2008, Ceres Revista frutos. em Honey (Wint.) pessegueir de Piero genótipos B.; C. d. diferentes M. Raseira, de A.; Júnior, Avaliação Wagner C., 165. UK, 2008. B. C. R M. D. Raseira, Layne, B.; Uses, W. and Sherman, Production L.; Botany, B. Peach: Topp, The 164. M., J. Ogawa, J.; A. Feliciano, A.; 77, Vol. Feliciano, 1987; Phytopathology, ‘Bolinha’. cultivar 163. Zanandrea, B.; C. M. Raseira, J.; Santos, 219225. (2), dos 71 2012, Bragantia plants. 162. p 465, M. Vol. 1998; Acta Horticulturae, In phenolics. R. Bostock, A.; M. Thorpe, M.; T. Gradziel, ( 161. 131140. (2), 16 1965, of occurrence The C., Reinganum, by P.; Jenkins, caused 160. interacti parasit host on Studies T., Zwigart, 97130. 68, 1970, Z. Phytopath. 159. 828. path fungal nonhost and host to response in petals R of Y expression Sui, M.; and Wisniewski, peroxide D.; hydrogen Macarisin, J.; of Liu, Production 158. pathogen rot inbrown the L P. Yu, M.; C. Chou, J.; B. reg You, statusmediated M.; Redox C. H., M. Chiu, Lee, R.; K. Chung, 157. 599 93 (4), 2013, Science Plant of Journal Canadian incompatible and di and compatible Cloning S., in Jayasankar, PdMYB3, A.; Elkereamy, repeatMYB, 156. react J 552557. (SPE1), 33 2011, rot Oliveira, brown C.; for K. Fabiane, divergence A.; genetic Júnior, tree Wagner Peaches 155. 152. Zemanek, A.; Ko, T.; Thimmapuram, J.; Hammersc J.; Thimmapuram, T.; Ko, A.; Zemanek, 152.

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.; Droby, S.; Norelli, J.; Hershkovitz, V., V., Hershkovitz, J.; Norelli, S.; Droby, .; ons in in ons .; Yu, F. Y.; Pan, S. M.; Bostock, R. M.; M.; R. Bostock, M.; S. Pan, Y.; F. Yu, .; Monilinia fructicola Monilinia bom, C. R.; da Silva, J. B.; Franzon, R. R. Franzon, B.; J. Silva, da R.; C. bom, rotein during brown rot infection. Plant Plant infection. rot brown during rotein signals in in signals ion. Revista Brasileira de Fruticultura Fruticultura de Brasileira Revista ion. OSgenerating genes in peach flower flower peach in genes OSgenerating rampalli, D.; Paliyath, G., Expression Expression G., Paliyath, D.; rampalli, fferential expression of a plum single single plum a of expression fferential I., Citadin, J.; Zanela, d.; A. M. S. . I., Resistance to brown rot in peach peach in rot brown to Resistance I., .; Bassi, D., Eds. CABI: Wallingford, Wallingford, CABI: Eds. D., Bassi, .; ; Wilcox, S., Breeding for brown rot rot brown for Breeding S., Wilcox, ; to treatment with pathogen culture culture pathogen with treatment to , Lowchill Cultivar Development. In In Development. Cultivar Lowchill , a quiescent infection of stone fruits fruits stone of infection quiescent a interactions during fungal infection. infection. fungal during interactions hlag, F.; Korban, S., Changes in in Changes S., Korban, F.; hlag, Monilinia Arabidopsis diseases of fruit trees. trees. fruit of diseases resistance in peach peach in resistance Monilinia fructicola Monilinia . Molecular Plant Plant Molecular . he role of fruit fruit of role he esearch esearch

Version postprint always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 1658 1658 1657 1656 1655 1654 1653 1652 1651 1650 1649 1648 1647 1646 1645 1644 1643 1642 1641 1640 1639 1638 1637 1636 1635 1634 1633 1632 1631 1630 1629 1628 1627 1626 1625 1624 1623 1622 1621 1661 1661 1660 1659 . QL apn fr rw rt ( rot brown for mapping QTL A., [ resistance (Honey)] Ruhl. et Aderh. 8188. pp 592, Vol. 2002; Horticulturae, Acta region. GenetikaBelgrade 2012, 44 (2), 285297. 285297. (2), 44 2012, GenetikaBelgrade region. Paunovi M.; Lukic, R.; Cerovic, cherr sour S.; autochthonous of Selection Radicevic, M., Mitrovic, 168. Karakl I.; Glisic, 299306. (2), 42 2010, R.; Cerovic, S.; ( Radicevic, hybrids 167. 201207. yugoslav in situ in peach) Vineyard = vulgaris ssp. . Dtoi M T; rmod J; atnr, . Zu F.; Cattonaro, J.; Grimwood, T.; M. Jung, Dettori, S.; Scalabrin, G.; A. Abbott, I.; Verde, T.; 181. che of Evaluation F., W. Wilcox, K.; S. Brown, by infection 180. fructicola c sweet Screening L., fo P. program breeding Sholberg, Summerland F.; Centre Research Kappel, Food 179. 541 33(4), 2004, Pathology Plant Australasian spp. Fra A.; J. Fraser, F.; G. McLaren, fo fruit M.; apricot screening of Methods Walter, H., J. Perry, 178. o Results A., Sartori, A.; Nicotra, L.; p 862, Vol. 2010; Conte, Horticulturae, Acta In FRU. CRA 177. p I, 701 Vol. 2006; Acta Horticulturae, In apricot. for programme Breeding P Fantechi, L.; A., Moser, L.; Conte, Magnotta, A.; Nicotra, S.; 176. artificial by B Leuven, (ISHS), Science Horticultural for Society susceptibility rot brown for M.; Lama, D.; Bassi, C.; Perini, I.; Pacheco, methods 175. ( Ciacciull I.; Eduardo, D.; Bassi, I.; Pacheco, 174. 6065. 10 (5), 2003, Hortus fru for peaches Breeding M., Rizzo, D.; Bassi, 173. br Assaying L., Cantoni, M.; Rizzo, D.; progen and cultivars peach Bassi, in susceptibility Honey) 172. Breedin and Genetics Traditional T., 2254. pp 2012; Gradziel, Press: CRC Fruits, Stone of 171. of sources as species Almond M., T. Gradziel, 170. breedi Peach H., Bonifacio, B.; C. M. 9397. Raseira, pp 713, Vol. 2006; Horticulturae, 169. 166. Paunovic, S. A.; Paunovic, A. S., Investigatio S., A. Paunovic, A.; S. Paunovic, 166.

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persica p 307311. 307311. p r resistance to brown rot caused by caused rot brown to resistance r ia. In Acta Horticulturae, 1996; Vol. 374, pp pp 374, Vol. 1996; Horticulturae, Acta In ia. elgium: 2015; pp 367374. 367374. pp 2015; elgium: 715721. 465, 1998, Horticulturae y. Acta y (Prunus cerasus l.) Genotypes in feketic feketic in Genotypes l.) cerasus (Prunus y p 99102. 99102. p 547. 547. inoculation in the orchard, International International orchard, the in inoculation S.; Shu, S.; Marroni, F.; Zhebentyayeva, Zhebentyayeva, F.; Marroni, S.; Shu, S.; Foschi, S. In Towards faster phenotyping phenotyping faster Towards In S. Foschi, f an apricot breeding programme at the the at programme breeding apricot an f i, A.; Pirona, R.; Rossini, L.; Vecchietti, Vecchietti, L.; Rossini, R.; Pirona, A.; i, .; Barbagiovanni, I.; Corazza, L.; Vitale, Vitale, L.; Corazza, I.; Barbagiovanni, .; n of peach germplasm (. germplasm peach of n (L.) Batsch EmiliaRomagna]. Italus Italus EmiliaRomagna]. Batsch (L.) g. In Genetics, Genomics and Breeding Breeding and Genomics Genetics, In g. own rot ( rot own it quality and brownrot [( brownrot and quality it ) resistance in an intraspecific peach peach intraspecific an in resistance ) ng program in Southern Brazil. In Acta Acta In Brazil. Southern in program ng ajicStajic, Z., Promising sour cherry cherry sour Promising Z., ajicStajic, mpton, C. M.; BoydWilson, K. S. H.; H.; S. K. BoydWilson, M.; C. mpton, , . Jveoi, . Mlnoi, S.; Milenkovic, D.; Jevremovic, S.; c, new genes for peach improvement. In In improvement. peach for genes new cl, . Rsii L; ekn, J.; Jenkins, L.; Rossini, A.; ccolo, er clias rm h Pcfc Agri Pacific the from cultivars herry rry genotypes for resistance to fruit fruit to resistance for genotypes rry r resistance to brown rot ( rot brown to resistance r 747752. 747752. (Aderh. et Ruhl.) resistance on on resistance Ruhl.) et (Aderh. Monilinia laxa Monilinia cacak. GenetikaBelgrade GenetikaBelgrade cacak. 4, 10 (5), 12231242. 12231242. (5), 4, 10 Aderh. et Ruhl. Ruhl. et Aderh. Prunus Monilinia laxa Monilinia

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Page 60of72 Version postprint Page 61of72 always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 1671 1671 1670 1669 1668 1667 1666 1665 1664 1663 1662 genome evolution. Nat Genet 2013, 45 (5), 487494. 487494. 45 (5), 2013, Genet Nat evolution. genome (peach D Rokhsar, M.; Morgante, J.; Schmutz, F.; Salamini, A.; Orellana, P.; Arus, M P.; Tonutti, Miculan, S.; R.; Tartarini, Pirona, D.; R Bielenberg, Falchi, B.; S.; Lazzari, D. Horner, S.; Gonzalez, D.; Copetti, Goodstein, S.; Ficklin, L.; Dondini, G.; Cipriani,

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61 61 Wells, C.; Main, D.; Vizzotto, G.; Silva, H.; H.; Silva, G.; Vizzotto, D.; Main, C.; Wells, D. M.; Xuan, P.; Fabbro, C. D.; Aramini, V.; Aramini, D.; C. Fabbro, P.; Xuan, M.; D. i, B.; Prochnik, S.; Mitros, T.; Policriti, A.; A.; Policriti, T.; Mitros, S.; Prochnik, B.; i, .; Barakat, A.; Testolin, R.; Stella, A.; A.; Stella, R.; Testolin, A.; Barakat, .; .; Lucas, S.; Mica, E.; Maldonado, J.; J.; Maldonado, E.; Mica, S.; Lucas, .; . S., The highquality draft genome of of genome draft highquality The S., . domestica tion and and tion Version postprint always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 1699 1699 1698 1697 1696 1695 1694 1693 1692 1691 1690 1689 1688 1687 1686 1685 1684 1683 1682 1681 1680 1679 1678 1677 1676 1675 1674 1673 1672 1701 1701 1700 Figure 2.Figure 20 Agrios, N. George (Copyright UK Limited, Oxford, 1. Figure Captions Figure 10 Figure 6.Figure around crack formation of beginning theimage shows 5. Figure showing daysbloom) full after (46nectarinefruit 4. Figure 10and 10 L of drop imag all In (o). aperture epidermis an in hyphae of arro The hyphae. by surface of colonization the and germi chaotic a illustrates image This germination. distribution the note to possible is It hpi. 15 at obs 0.5%, blue, Toluidine with coloured maturity at in an – F direction. (m) crack micro in mycelium of g spore E hpi. 15 cultivar ‘Magique’ cv. of cracks (asterisks) spores of germination and i concentration microscopy p electron and D (asterisks) (arrow). aperture germination stomata spore of Beginning C surface Tolu the with coloured maturity, at on ‘Magique’ nectarine infection showing images microscopy (a stomata open an through entering hyphae a see to direction (s) su hpi. 24 stoma photomicrograph fluorescence B (arrows). the fruit to the moves and on (t) develops trichomes fungi The (hpi). infection apr fungi in of development the showing examination 3. Figure

Peach fruit infected by three different different by three infected fruit Peach The process of of process The Figure 4: Light microscopy image of surface impres surface of image microscopy Light 4: Figure Scanning electron microscopy of nectarine cultivar nectarine of microscopy electron Scanning

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1 of conidia concentration. conidia concentration. of spp infection spp infection 62 62 Monilinia of spores (asterisks) and their their and (asterisks) spores of the high density of stomata. stomata. of density high the ermination and development development and ermination es fruit were infected with a with infected were fruit es fection of nectarine surface surface nectarine of fection nation of spores (asterisks) (asterisks) spores of nation erved with light microscopy microscopy light with erved idine blue, 0.5%, 15 (hpi). (hpi). 15 0.5%, blue, idine In this image it is possible possible is it image this In 15) 15) icot surface 8 hours post 8hours surface icot w shows the penetration penetration the shows w a lenticel at maturity. at maturity. a lenticel fungi around the fruit fruit the around fungi mage shows a strong strong a shows mage rrows). C and E light light E and C rrows). rface, twists around around twists rface, species. species. n tihms basis trichomes and enetration through through enetration of a commercial commercial a of ‘Magique’. The The ‘Magique’. sion of a young a of sion croscopy sevier sevier Page 62of72 Version postprint Page 63of72 always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 1732 1732 1731 1730 1729 1728 1727 1726 1725 1724 1723 1722 1721 1720 1719 1718 1717 1716 1715 1714 1713 1712 1711 1710 1709 1708 1707 1706 1705 1704 1703 1702 1733 1733 et aes ad ucpil Eeat ay (ih p h stacked with epidermis the (right on colonization fungal Lady’ Elegant susceptible and panels) left ‘Conte cross the from (F1 BO92038071 resistant Both electron transmission and staining) blue toluidine are varieties, peach two from fruits on inoculation laxa 7. Figure constitutively are present in fruit tissues are abl are tissues fruit in present are constitutively gene the Pathogene enzymes. degrading cellwall or in cutinases reduction a in an cyt results creating that the environment by in colonization or hyphal stop constituents substances wall cell yellow), (CUT, ( synthes waxes epicuticular amongst or colonization, pathogen present constitutively be can substances Fungalind grey). funga promotes that process another is biosynthesis (DT, tissue dismantled generating endopoluygalacturo and exo pectinmethylesterases, polysacchar cellwall hydrolyze enzymes degradating by degradation its after subsequent cuticle the penetrate ii) lenticcracks, micro (OPD; doors open through enter andspp. fungi 8 Figure are (arrows) fibrils cellulose anddigested almost (d) infection fruit susceptible in interface plant elect material This origin. phenolic by of probably arrows) encapsulated almost are walls, cell digest phenol plant f resistant in that show images TEM of cells. adjacent deposition the by possibly blocked, resi the in only however, pectins; of staining pink this At regions substomatal (G). cells guard over germinating sometimes

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63 63 where cell wall matrix has been been has matrix wall cell where e to activate phenylpropanoid phenylpropanoid activate to e completely disaggregated disaggregated completely microscopy (TEM, c,d) level. c,d) (TEM, microscopy illustrated both at light (a,b, (a,b, light at both illustrated is not present in the fungal the in present not is ruit hyphae, though able to to able though hyphae, ruit yphae (H) and conidia (C), conidia and (H) yphae tn fut a, neto is infection (a), fruit stant els or trichomes basis), or or basis), trichomes or els l colonization. Polyphenol Polyphenol colonization. l EPW, light blue), cuticle cuticle blue), light EPW, sisrelated enzymes that enzymes sisrelated nl) rsn discrete present anels) ides through cellulases, through ides rondense material (c, (c, material rondense nases, among others, others, among nases, expression of fungal fungal of expression and cutinases fungal c (seik) n the in (asterisks) ics nder x Elegant Lady’, Lady’, Elegant x nder , 8 atr artificial after 48h n, neto sae the stage, infection ized in response to to response in ized oplasm. Polyphenol Polyphenol oplasm. cd rai acid organic uced chemically adverse adverse chemically ty to to ty n Monilinia Monilinia Monilinia y the the y an i) i) an

o eeomn o bon o 5dy ps atfca in artificial post 5days rot brown of Development C for 40 seconds, put in acrylic plastic boxes and boxes plastic acrylic in put seconds, 40 for C Comment citer cedocument: 5 spores.ml Journal ofAgriculturalandFoodChemistry ACS Paragon PlusEnvironment

1 of concentration deposited without wounding. wounding. without deposited concentration of 64 64 ess. ess. t (16 hours per day). High High day). per hours (16 t were disinfected in water water in disinfected were , cell wall strengthening strengthening wall cell , ature (18°C) and 24°C 24°C and (18°C) ature infected with one with infected fection in in fection Page 64of72 Version postprint Page 65of72 always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 1748 1748 1747 1746 1750 1750 1749 11 Figures / Graphics Graphics / Figures 11 Figure 1.Figure

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Figure 2.

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Page 66of72 Version postprint Page 67of72 always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 1757 1757 1756 1755 1754

3.Figure

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67 67 Version postprint always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 1764 1764 1763 1762 1761 1760 1759 1759 1758

Figure 4.Figure

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Page 68of72 Version postprint Page 69of72 always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 1770 1770 1769 1768 1767 1766 1766 1765 1772 1772 1771 Figure 6.Figure

Figure 5.Figure

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Comment citer cedocument: Journal ofAgriculturalandFoodChemistry ACS Paragon PlusEnvironment

70 70 Page 70of72 Version postprint Page 71of72 always lost. Journal ofAgricultural andFood Chemistry, 64(20), 4029-4047. DOI:10.1021/acs.jafc.6b00104 Oliveira Lino,L.,Pacheco, I.(Auteurde correspondance), Mercier, V.,Faoro,F., Bassi,D., Bornard, I.,Quilot-Turion, B.(2016). Brown rotstrikes Prunusfruit: anancientfight almost 1776 1776 1778 1778 1777 1780 1780 1779 Figure 8.Figure Figure 9.Figure

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