REVIEWS ARTICLES

Alternaria Genus and the Diseases Caused to Agricultural and Horticultural

Antonia FLOREA1 1

1 Faculty of Agriculture,*, Carmen University PUIA of Agricultural Sciences and Veterinary Medicine of Cluj-Napoca, Calea Mănăștur 3-5, 400372 Cluj-Napoca, Romania *corresponding author: [email protected]

Bulletin UASVM series Agriculture 77(2) / 2020 Print ISSN 1843-5246; Electronic ISSN 1843-5386 DOI:10.15835/buasvmcn-agr: 2020.0034

Abstract Alternaria This work is a bibliographic approach to the historical and most recent on genus. The genus consists largely of etspecies al of saprophytic, endophytic and parasitic fungi. The United States Fungal host index ranks the genus Alternaria on the 10th place based on the number of host plants, with over 4,000 species. Govind . (2016) tells us that most species of this genus are missing the sexual form, with the exception of a few species, which have, in addition to the anamorphic form, the telemorphic form. With the discovery of several species and due to the superficiality of past research, the inclusion of this genus in the taxonomy has become problematic. At the beginning, the Alternariataxonomic classification was performed according to the morphology of the species. This bibliographic approach wants to clarify some of the aspects concerning the old and actual taxonomyet ambiguities al. of Alternaria genus. The method used is consulting the etscientific al. literature. The present reclassification ofet al.the species was performed by analysing the DNA ofAlternaria each species omanensis in 2013 by WoudenbergAlternaria and genus fit the is species in 25 sections. In 2016 Lawrence added 2 other sections and in 2019 Ghafri forms a new section based on the new species . In conclusion now divided in 28 sections, each section contains species that are genetically related. Even though most of the ambiguities have been clarified at present, there are still ambiguities regarding the species within and Keywords:between sections. Alternaria

, ambiguities, taxonomy

INTRODUCTION The genus Alternaria (Singh et al the number of host plants, with over 4000 species et al is largely composedet al of ., 2016). Most species of this genus are species of saprophytic, endophytic and parasitic devoid of theet sexual al form (except for a few species, fungi (Lawrence ., 2016; Singh ., 2016). which have in addition the telemorphic form) According toPezizomycotina the taxonomic classification, it (Lawrence ., 2016). With the discovery of Dothideomycetesbelongs to the kingdom of Fungi, the and the several species and due to the superficiality of past branch, the (Stuart sub-branch,et al the class research, the inclusion of this genus in taxonomy et al , theet al subclass has become problematic. At the beginning, the family ., 2009; Lawrence taxonomic classification was performed according the genus., 2016, Alternaria Ghafri ., 2019). The database of the to the morphology of the species and currently, United States of America Fungal host index ranks the reclassification of the species was performed on the 10th position based on by analysing the DNA of each species (Lawrence 54 FLOREA & PUIA et al et al et al et al et al ., 2016; Tralamazza ., 2018; Woudenberg shape, form, size, colour etc. (Nabahat ., 2020) ., 2013). The damages produced on the crops and six main groups were formed (Lawrence ., are significant, with tomatoes registering losses 2016). between 50-86%.et al In addition to cropet losses, al the The third stage was between 1930 and 1960. produce pneumonia, asthma, or sinus ofDuring the genusthis period, Stemphylium an attempt was made to separate theirritation genus (Cruz Alternaria ., 2016; Lawrence ., 2016; the two genera to determine the classification Shyama and Somnath, 2015). Some species of conclusion that the genus. Macrosporium The year 1933 should was a release mycotoxins in the decisive one,nomen because ambiguum the researchers” (Singh etcame al to the organs of the attacked plants. Mycotoxins are et al toxic substances that result due to the pathogen’s be called “ ., 2016; metabolism. The main mycotoxins produced Lawrence ., 2016, 2013). This decision was are: alternariol, alternariol monomethylet al ether, based on the fact that problems occurred because dealtertoxins Perre et I, al II, III and tenuazonic acid (Pinto of the numerous taxons that were superficially and Patriarca, 2017; Tralamazza ., 2018; Van investigated, and more than 400 fake species were ., 2015). These mycotoxins were described (Nishikawa and Nakishima,et al 2020). This found both in raw products (apples, citrus, wheat, etconclusion al was not immediately accepted. Thus, tomatoes, sunflower seeds) and in processed in 1945, Neergaard (Singh ., 2016; Lawrence products, which come from infected plants. ., 2016) tried to redistribute them, based on Mycotoxins have a negative effect on human health. the morphological characteristics of the conidia They can contribute to chromosomal mutationset al etformation. al This classification does not follow the and affect the integrity of DNA in colon cells (Ostry, rules of nomenclature and it is not used (Lawrence 2008;The Pinto history and Patriarch, of the taxonomic 2017; Tralamazza classification ., ., 2016; 2013). 2018).and the current classification of the The fourth stage was between 1960-2000. Alternaria genus informationThis stage was about dedicated the Alternaria to the researcher Enoy Guy Simmons, who put together all the known Alternariagenus (Lawrence and other The history of taxonomic classification has et al., 2016; Pryor B.M. and L. Gilbertson,phaeodictyosporic 2000). gone through five main stages since 1816, the hypfomycetesDuring this period, the genus last revision being made betweenAlternaria 2003 and tenuis2015. similar species were called “ The first stageet alwas between 1816 and 1850 and ”, trying to name species with berry includes the descriptionet al of the Alternariashape conidiaMacrosporium appearance andand darkStemphylium brown spores until (Lawrence ., 2016; Pryor and Gilbertson, imperfect fungi. This category includesUlocladium the genera forms2000; of Ghafri four genera:., 2019). Ulocladium During Macrosporium this period, a , Alternariaconnection and was Brachycladium observed between the anamorphic 1970. Meanwhile, the genus waset Stemphylium , , alforgotten and the differentiation between the . In 1833 the genus Macrosporiumother three genera was confusing (Lawrence was added. Because of the ambiguity ., 2016; Pryor and Gilbertson,Macrosporium 2000). Thecheiranthi genus of the first four genera, they wereBrachycladium always confused. and belonging to the was Alternaria forgotten mainly through the FewUlocladium of the species investigated had been validated.et al generadeclaration emerged of the from species the Alternaria Meanwhile, the genera Alternaria Chalastospora, genus. Embellisia, Later, Nimbya other had been forgotten (Lawrence ., and Teretispora (Singh et al genus, such aset 2016, 2013). al ster, The second stage was between 1850 and 1930. ., 2016; Lawrence This period was marked by theMacrosporium discovery of genus new ., 2016; 2013). Alternaria and (Singhspecies. et Aboutal 400 species et had al been classified, The fifth stage was between 2003-2015, when most of them were placed in the reclassification of the genus ., 2016; LawrenceAlternaria and., 2016).Macrosporium After this onother the relatedgenus Stemphylium species, through and Ulocladium DNA analysis was period, the first taxonomic hierarchy was known elaborated. The first approach of this was performed by the name of . these genera and the Alternaria . Studies Most species were distributed according to the have revealed a very close relationship between Bulletinmorphological UASVM Agriculture characteristics 77 (2) / 2020 of the conidia like: genus. Due to Alternaria Genus and the Diseases Caused to Agricultural and Horticultural Plants 55

the multitude of morphological characters, DNA mainly on the surface of the affected tissue, along alliedsequencing genera was under a goodAlternaria approach name to(Gannibal solve some and with the conidia. Conidia are usually transported phylogenetic problems by reducinget al the number of by wind, water, animals, machinery, insects, etc. Spores, which reach other plants or other organs, Lawrence, 2018; Lawrence ., 2016, Nishikawa cause secondary infections. Asexual reproduction and Nakishima, 2020). Even though these methods is predominant, but there are species that also have advanced a lot in the research of this genus, have a sexual form. Sexual reproduction occurs the discrepancy, the relationship between species after 1-2 cycles of asexual reproduction. However, and the relationship between taxonomy and the sexual form was performed only in laboratory parasitism has not been sufficient to help the etconditions al because it is hard to reproduce the practical recognition of species (Nishikawa and weather conditions for a long period of time (Meng Nakishima, 2020). Currently, 28 sections have been ., 2015). The main causes for the lack of sexual formed within the genus based on et phylogenetic al multiplication are the changes of the heterothallic relationshipset al (Gannibal, 2018;et al Gannibal and system in the homothallicet al system oret the al beginning Lawrence,Causes 2018;of Alternaria 2016; Lawrenceambiguities: morpho., 2016;­ or non-completionCurrent branching of the of the sexual Alternaria multiplication genus Tralamazzalogy of the genus., 2018; Alternaria Singh , .,biological 2016). cycleThe (Lawrence Alternaria .,genus 2016; Mengis divided ., 2015).into 28 cycle and the lack of sexual reproduction One of the main reasons for Alternaria sections.The Eachmain section diseases includes caused the by species Alternaria based on morphologicalspp. to agricultural and DNA and analysis horticultural (Table 1). crops genus ambiguitiesAlternaria is the similarity between the Early blight of potato Alternaria morphological characteristics of the species.et al The solani, Alternaria protenta, Alternaria linariae, mycelium et of al the genus is composed Alternaria grandis caused by of conidiophores and conidia (Singh ., 2016; Lawrence ., 2016). The conidiophores can be simple or branched, pale brown, grey, dark brown Main symptoms appear on the main organs or olive and can be either solitary or grouped in of the plant: leaves, stem and tuber. The attack on bundles. The surface of the conidia can be smooth the foliar system is highlighted by the appearance etor alrough, with or withoutet al septa. The etmycelium al is of brown-blackish, circular spots, small at the found on theet al plant on the necroticet al lesion (Singh beginning of the infection but which can increase ., 2016; Stuart ., 2009,et al Hu ., 2015; over time (Fig. 1). LawrenceAnother reason., 2016; behind Melo these., 2009; ambiguities Pinto and is Patriarca, 2017; Tralamazza ., 2018). the biological cycle and sexual reproduction. The species of the genus can be parasitic, saprophytic and endophytic.et al The main categories that cause significant damage are parasites and saprophytes (Lawrence ., 2016). In order for pathogens to produce infections, the climate must be alternately humid and dry. The optimum temperature of development is between 25-31°C and the relative humidity between 70-80%. In case of favourable climatic conditions,et theal infection occurset al within 5-18 hours while the first symptoms appear in 4-6 days (Mamgain ., 2013; Singh ., 2016). Figure 1 The penetration occurs through the stomata or healthy tissue and it is favoured by the presence of . Early blight of potato (http://omafra.gov. on.ca/IPM/english/potatoes/diseases-and-disorders/ existing lesions. Once the infection is present, the alternaria.html) pathogen releases in plant toxins that can sensitize healthy tissues. The pathogenic mycelium is found Bulletin UASVM Agriculture 77 (2) / 2020 56 FLOREA & PUIA

Table 1. Alternaria

The sections and species of genus based on pylogenetic and morphological analysis. Section of Alternaria genus Species Author

Alternaria alternantherae, Alternaria celosiicola et al Alternantherae Alternaria gonphenae et al Alternaria perpunctulata Lawrence ., 2016 Woudenberg ., 2013 Alternaria arborescens Alternaria angustiovoidea Alternaria gaisen Alternaria alternata Alternaria burnsii Alternaria cerealis Alternaria citriarbusti Alternaria alstroemeriae Alternaria betae-kenyensis Alternaria gossypina Alternaria iridiaustralis Alternaria citrimacularis Paul et al Alternaria Alternaria colombiana et al Alternaria destruens ., 2015 Alternaria dumosa Woudenberg ., 2013,2014, 2015 Alternaria herbiphorbicola Alternaria daucifolli Alternaria limoniasperae Alternaria longipes Alternaria perangusta Alternaria postmessia Alternaria tangelonis Alternaria tomato Alternaria toxicogenica Alternaria turkisafria Alternaria brassicicola Alternaria conoidea et al Brassicicola Alternaria mimicula et al Alternaria septorioides Lawrence ., 2016 Alternaria solidaccana Woudenberg ., 2013 Alternaria abundans Alternaria armoraciae Alternaria breviramosa Chalatospora et al Alternaria malorum Alternaria cetera Woudenberg ., 2013 Alternaria obclavata Alternaria indefessa et al Cheiranthus Alternaria cheiranthi et al Lawrence ., 2016 Alternaria papavericola Crivellia Woudenberg et al., 2013 Alternaria penicillata Alternaria elegans Woudenberg ., 2013 et al Dianthicola Alternaria simsimi et al Alternaria dianthicola Lawrence ., 2016 Alternaria embellisa Woudenberg ., 2013 et al Embellisa Alternaria tellustris et al Alternaria chlamydosporigena. Lawrence ., 2016 Woudenberg ., 2013

Bulletin UASVM Agriculture 77 (2) / 2020 Alternaria Genus and the Diseases Caused to Agricultural and Horticultural Plants 57

Alternaria botryospora Alternaria planifunda Alternaria tumida et al Embellisioides Alternaria proteae et al Alternaria lolii Lawrence ., 2016 Alternaria hyacinthi Woudenberg ., 2013

Alternaria limicola Euphorbiicola et al Alternaria euphorbicola.

Alternaria cucumi Woudenberg ., 2014 Alternaria trigochinicola Alternaria anigozanthi et al Eureka Alternaria geniostomatis et al Alternaria leptinellae Lawrence ., 2016 Alternaria eureka Woudenberg ., 2013 Alternaria ellipsoidea Alternaria vaccariae, Alternaria vaccariicola Alternaria nobilis et al Gypsophilae Alternaria saponariae, et al Alternaria axiaeriisporifera Lawrence ., 2016, 2013 Alternaria juxtiseptata Woudenberg ., 2013 Alternaria gypsophylae Alternaria grsminicola Alternaria arbusti Alternaria caespitose Alternaria californica Alternaria conjuncta Alternaria daucicaulis Alternaria ethzedia Alternaria fumenti Alternaria graminicola Alternaria hordeiaustralica Alternaria hordeicola Alternaria humuli et al Infectoriae Alternaria incomplexa et al Alternaria alternarina Lawrence ., 2016 Alternaria triticina Woudenberg ., 2013 Alternaria metachromatica Alternaria infectoria Alternaria intercpta Alternaria merytae Alternaria novae-zelandiae Alternaria oregonensis Alternaria slovaca Alternaria triticimaculans Alternaria ventricosa Alternaria viburni Alternaria nepalensis Japonicae Alternaria japonica Alternaria telliensis Alternaria caricis Alternaria juncicola et al Alternaria heteroschemos Nimbya et al Alternaria scirpivora Lawrence ., 2012, 2016 Alternaria scirpinfestans Woudenberg ., 2013 Alternaria scirpicola Gannibal, 2018 Omanenses Alternaria omanenses Ghafri et al

., 2019

Bulletin UASVM Agriculture 77 (2) / 2020 58 FLOREA & PUIA

Alternaria araliae Alternaria avenicola Alternaria hedjaroudei et al Alternaria calycipyricola Panax et al Alternaria dendropanacis HashemlouLawrence et al., 2016 Alternaria photistica Woudenberg ., 2013 Alternaria eryngii ., 2020 Alternaria panacis Alternaria chlamydospora Alternaria didymospora Alternaria limaciformis et al Phragmosporeae Alternaria molesta et al Alternaria mouchaccae Lawrence ., 2016 Alternaria phragmospora Woudenberg ., 2013 Alternaria capsici Alternaria agerati Alternaria acalyphicola Alternaria anagallidis Alternaria aragakii Alternaria argyroxiphii Alternaria bataticola Alternaria blumeae Alternaria calendulae Alternaria carthami Alternaria cassia Alternaria cichorii Alternaria cirsinoxia Alternaria crassa Alternaria cretica Alternaria cyphomandrae Alternaria cucumerina Alternaria dauci Barreto et al Alternaria danida Alternaria dichondrae et .,al 2008 Porri Alternaria grandis Gannibal,et al 2015 Alternaria hawaiiensis Lawrence et., al2016 Alternaria solani Soylu ., 2005 Alternaria linariae Woudenberg ., 2013,2014 Alternaria limicola Gannibal, 2018 Alternaria linicola Alternaria macrospora Alternaria multirostrata Alternaria passiflorae Alternaria poonensis Alternaria porri Alternaria protenta Alternaria pseudorostrata Alternaria pseudorostrata Alternaria rahapontici Alternaria scorzonerae Alternaria sesame Alternaria solani-nigri Alternaria steviae Alternaria subcylindrica Alternaria zinnia Alternaria arrhenatheri Pseudoalternaria Alternaria rose et al Gannibal and Lawrence, 2016 Lawrence ., 2016 Bulletin UASVM Agriculture 77 (2) / 2020 Alternaria Genus and the Diseases Caused to Agricultural and Horticultural Plants 59

Alternaria aspera Alternaria septospora Alternaria lanuginose et al Pseudoulocladium Alternaria sylvestris et al Alternaria concatenata Lawrence ., 2016 Alternaria chartarum Woudenberg ., 2013 Alternaria selini Alternaria petroselini et al Radicina Alternaria smyrnii et al Alternaria carotiiniculatae Lawrence ., 2016 Alternaria radicina Woudenberg ., 2013 Alternaria petuchovskii Soda Alternaria shukurtzii et al Alternaria kulundii. Lawrence ., 2016 Alternaria sonchi Sonchi et al Alternaria cinerariae Woudenberget al ., 2013 Teretispora Alternaria leucanthemi et al Lawrence ., 2016 Alternaria cucurbitae Woudenberg ., 2013 Alternaria alii-tuberosi Alternaria castaneae Alternaria gpagarwalii Alternaria microspore Alternaria oblongo-obovoidea Alternaria populicola Alternaria preussii Alternaria pseudobotrytis et al Alternaria sorghi Ulocladioides et al Alternaria zantedeschiae GannibalLawrence et al ., 2016 Alternaria brassicae-pekinensis Woudenberg ., 2013 Alternaria cantlous ., 2018 Alternaria consortialis Alternaria heterospora Alternaria obovoidea Alternaria subcucurbitae Alternaria multiforimis Alternaria terricola Alternaria atra Alternaria capsici-annui Alternaria botrytis et al Ulocladium Alternaria alternariae et al Alternaria manihoticola GannibalLawrence et al ., 2016 Altenaria oudemansii Woudenberg ., 2013 ., 2018 Alternaria bornmuelleri Alternaria cinerea Undifilum et al Alternaria fulva Alternaria oxytropis Woudenberg ., 2013

Concentric circles can be seen on the surface et al leading to the necrosis of the tissue (Bobes, 1983). of the strains (Waals ., 2001; Bobes, 1983). The attack on the potato tubers can be observed On the upper part of the spots appears a black by the presence of dark-brown circular spots, hard brown down composed of the conidiophores and in texture and slightly deep into tissue. On their conidia of the pathogen. As the pathogen develops, surface there is a black rot formed by the conidia the spots on the leaf surface increase and unite on the conidiophores ofBulletin the UASVM . Agriculture At first,77 (2) / 2020 the 60 FLOREA & PUIA

attack canet al be seen on the lower floor of the plant are at that moment small in size but with their thenAlternaria it gradually developsblack spot and takesof canola over the caused plant development can reach up to a diameter of 10 mm Alternaria(Waals brassicae., 2001; Popescu, Saccardo 1993). (Yacoub, 2003). The shape of the spots is elliptical, they have a yellow-brown colour, and the spots on the fruit have an aqueous appearance (Fig. 2). As The pathogen prefers high temperatures, high the spots grow, they come together and can cover humidity, but also the presence of precipitation the entire leaves, causing burns on the stems. On that favours their development. Main symptoms stems and shoots, the affected plants show deep appear on all green organs. Circular or ellipsoidal spotsBlack and carrot the browning rot of theAlternaria tissue (Yacoub,radicina spots with a diameter between 2-10 mm appear 2003; Bobes, 1983). (Singhfirst on etthe al leaves. The spots etare al yellowish-black, caused by and concentric formations appear inside them Meier, Drechsler & E.D. Eddy ., 2016; Kumar ., 2014; Bobeș, The disease can occur in all stages of plant 1983). On the stem, lesions appear from the top development. At the base of leaves, there can be to the base, the spots are elongated in the form of seen an atrophy of the corner that darkens, and the stripes, in the direction of the axis. On the silique, plants wither and fall. The leaves begin to yellow immersedthere are ain multitude the tissue of(Singh small et spots al in size that and ultimately suffer drying processes (Scott and have the shape of black dots or stripes slightly Wenham, 1972). In the roots section appear black ., 2016; Bobes, spots that are deep in the tissue. The edges of 1983). As the pathogen develops, the spots join the spots can be angular or smooth and are well together and form irregular spots. The pathogen defined. On the surface of the spots appears the grows on the surface of the spots, forminget al a mycelium of the pathogen formed by the conidia blackish-brown down composedet al of the conidia and conidiophores of the fungus,et al with a velvety and conidiophores of the fungus (Singh ., appearance. It often affects the inside of the root, 2016; Bobeș, 1983; Kumar . 2015). rarelyAlternariosis the top of the of root carrot (Farrar leaves ., 2004; Scott Alternariaand Wenham, dauci 1972). caused by Groves & SkolkoCercospora carotae The symptoms of this pathogen can be easily confused with the attack of . The leaves that are in a very advanced stage of the attack have spots with necrotic appearanceet al of black-brownBrown spot colour, leaves, surrounded stems and by acalatidium chlorothic onhalo sunflower(Scott and Wenham, 1972;A. Boedohelianthi ., 2010). and Alternaria zinnia A. alternata Keissler caused by Tsubaki Nisihara, Ellis,

Favourable climatic factors for the develop­ ment and spread of the pathogen are high tempe­ ratures above 24°C and high humidity. The optimal Figure 2. Alternariosis in cucurbits ( humidity conditions where the pathogen causes the ) infection are created after long-term precipitation https://pestre. in the interval of 12-24 hours. The days before the ro/blog/bolile-castravetilor/ Alternaria leaf spot of cucurbits precipitations, in which the temperatures are high Ellis & Everhart Alternaria cucumerina etand al the humidity iset lowal for long periods, stop the caused by development of the disease (Van der Westhuizeni ., 1980; Baicu ., 1996). The symptoms are The pathogen attacks all the green organs manifested on all the green organs of the plant. of the plant: leaves, stem and fruits. The spots Circular or angular brown-grey spots appear on that appeared at the beginning of the infection Bulletin UASVM Agriculture 77 (2) / 2020 the foliar apparatus, the edge of the spots being Alternaria Genus and the Diseases Caused to Agricultural and Horticultural Plants 61

CONCLUSION delimited by a yellow halo. The stains can reach a Alternaria diameter of 50mm. On the calatidium and bracts, Currently, the last attempt to taxonomically etthe al spots have a circularet al appearance. The formed reclassify the genus was made between achenesLeaf areblight small on in wheatsize and dry (UdayashankarAlternaria 2003 and 2015, where due to modern technologies; triticina., 2012; Prasada Baicu & Prabhu., 1996). the species was identified by molecular analysis. caused by However, the differences between the species of differentthe different sections sections of the are genus still unknown. Alternaria On have the The disease was reported in tropical and territory of Russia, interactions Solanacae of species from subtropical countries, especiallyet al in the countries et al et al of South and Southeast Asia, by Prasada and been found on plants from the family Prabhua in 1962 (Vergnes ., 2006). It prefers (KokaevaAcknowledgments. ., 2017; Lawrence This research ., 2016).did not re­ areas with warm climates and high temperatures. The first symptoms appear in wheat after 7-8 weeks, evolving with the growth of the plant. The ceive any specific grant from funding agencies in attack can be manifested on all the above-ground the public,REFERENCES commercial, or not-for-profit sectors. organs: leaves, stems, ear, jokes, pale and seed. On the leaf surface, ovoid spots appear, irregular at the beginning, of small dimensions, scattered on 1. Armitage AD, Cockerton HM, Sreenivasaprasad S, AlternariaWoodhall J,alternata Lane CR, Harrison RJ, Clarkson JP (2020). the entire leaf surface. Aset the al disease progresses Genomics evolutionary history and diagnostics of the the Black spots increasespot on carnations in diameter and intertwineAlter­ species group including apple and naria(Siddiqui, dianthi 2007; Stevens Vergnes & Hall., 2006). and Alternaria asian pear pathotypes. Frontiers in Microbiology, 10: 3124. dianthicola Neergard caused by 2. Baicu T, Tatiana Eugenia ȘT (1996). Fitopatologie Agricolă. Alternaria Ed. Ceres, București. cichorii Cichorium The organs attacked by the pathogen are: 3. Barreto RW, Santin AM, Vieira BS (2008). in Brazil on spp. seeds and cultivated leaves, stems and shoots, but attacks on flowers and weedy hosts. Journal of Phytopathology, 156: 425- are rare. On the leaves and nodes brown-grey 430. spots appear, well delimited by a portion of 4. Bobes I (1983). Atlas de fitopatologie și protecția healthy tissue, forming a yellow-greenet halo. al When agroecosistemelor. Ed.Ceres, București. the humidity is high, the spots are covered by the 5. Boedo C, Berruyer R, Lecomte M, Bersihand S, Briard M, mycelium of the black fungus (Mehta ., 2007; resistanceLe Clerc V, Simoneauato the Alternaria P, Pouparda P (2010). Evaluation Popescu, 1993). The attacked leaves fall from the (ofAlternaria different dauci methods for the characterization of carrot leaf blight pathogen stems and on the shoots the mycelium appears in ) revealed two qualitatively different the form of a ring surrounding the stem. The stems resistances. Plant Pathology, 59: 368–375. break very easily above the affected area. On the 6. Comes T, Lazar A, Bobeș I, Hatman M, Drăcea A (1982). Fitopatologie, Ed. Didactică și Pedagogică. București. flowers, brown areas are observed on the white Alternaria botrytis ofpetals the A. and dianthicola discoloration spots on the carnations 7. Cruz CRM, Laforet EP, Oyarzo PV, Silva LC (2016). with red flowers, this symptom being characteristic Identificación de (preuss) Woudenberg Saffron alternariosis Alternaria y Crous. Revista Argentina de Microbiología, 48: 182-183. carthami (Popescu, 1993). 8. Farrar JJ, Pryor BM, Davis RM (2004). Alternaria Diseases caused by Alternaria of Carrot. Plant Disease, 88(8): 776-784. S. Chowdhury Porri 9. Gannibal PB (2015). Distribution of species The attack of the pathogen is observed on among sections. 1. Section . Mycotaxon, 130: 207- Alternaria the foliar apparatus of the plant by the presence 213. Alternaria of small spots, circular or with irregular edge, 10. Gannibal PB (2016). Distribution of species among sections. 2. Section . Mycotaxon, 130: brown colour, and on their edges, light green Alternaria halos are present. As the attack progresses, the 941-949. spots intertwine and enlarge. On the surface of the 11. NimbyaGannibal PB (2018). Distribution of species spots appears a blackish mycelium consisting of among sections. 4. Species formerly assigned to genus et al . Mycotaxon, 133: 37-43. conidiophores and conidia of the pathogen (Ivaşcu ., 2009). Bulletin UASVM Agriculture 77 (2) / 2020 62 FLOREA & PUIA

Alternaria Infectoriae 12. andGannibal Pseudoalternaria PB, Lawrence DP (2016). Distribution of 28. Meng JW, Wen Z, Han HM, Wu EJ, Duan GH, Xie YK, Jin Y, species among sections. 3. Sections AlternariaLi N, Shang alternate L, Zhan J (2015). Population genetic analysis . Mycotaxon, 131: 781-790. reveals cryptic sex in the phytopathogenic fungus Alternaria . Scientific Reports, 5:18250. 13. Gannibal PB, Lawrence DP (2018). Distribution of Alternaria telliensis species among sections. 5. Species producing 29. fromNabahat Solanaceae B, Bruno H, Simoneau NB, Kihal M, Simoneau P conidia with many longitudinal septa. Mycotaxon, 133: (2020). sp. nov., a new species isolated 285-291. in Algeria. Phytotaxa, 440 (2): 089-100. Alternaria Alternaria 14. assignedGannibal to PB, genus Lawrence Ulocladium DP (2018). Distribution of 30. Nishikawa J, Nakishima C (2020). Japanese species of species among sections. 6. Species formerly and their species boundaries based on host Alternaria . 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