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Aphrophoridae Role in Xylella Fastidiosa Subsp. Pauca ST53 Invasion in Southern Italy

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Aphrophoridae Role in Xylella Fastidiosa Subsp. Pauca ST53 Invasion in Southern Italy pathogens Review Aphrophoridae Role in Xylella fastidiosa subsp. pauca ST53 Invasion in Southern Italy Ugo Picciotti 1,2, Nada Lahbib 1,3,4, Valdete Sefa 1, Francesco Porcelli 1,5,* and Francesca Garganese 1 1 Dipartimento di Scienze del Suolo, della Pianta e degli Alimenti, University of Bari Aldo Moro, 70126 Bari, Italy; [email protected] (U.P.); [email protected] (N.L.); [email protected] (V.S.); [email protected] (F.G.) 2 Department of Marine Science and Applied Biology, Laboratory of Plant Pathology, University of Alicante, 03080 Alicante, Spain 3 Faculty of Sciences of Tunis, University of Tunis El-Manar, Tunis 1068, Tunisia 4 INRAT—National Institute of Agronomic Research of Tunisia, Laboratory of Plant Protection, Rue Hédi Karray, Ariana 2049, Tunisia 5 CIHEAM—Centre International de Hautes Etudes Agronomiques Méditerranéennes, Mediterranean Agronomic Institute of Bari, 70010 Valenzano, BA, Italy * Correspondence: [email protected] Abstract: The Philaenus spumarius L. (Hemiptera Aphrophoridae) is a xylem-sap feeder vector that acquires Xylella fastidiosa subsp. pauca ST53 during feeding on infected plants. The bacterium is the plant pathogen responsible for olive quick decline syndrome that has decimated olive trees in Southern Italy. Damage originates mainly from the insect vector attitude that multiplies the pathogen potentialities propagating Xf in time and space. The principal action to manage insect- borne pathogens and to contain the disease spread consists in vector and transmission control. The Citation: Picciotti, U.; Lahbib, N.; analysis of an innovative and sustainable integrated pest management quantitative strategy that Sefa, V.; Porcelli, F.; Garganese, F. targets the vector and the infection by combining chemical and physical control means demonstrates Aphrophoridae Role in Xylella that it is possible to stop the Xylella invasion. This review updates the available topics addressing fastidiosa subsp. pauca ST53 Invasion vectors’ identification, bionomics, infection management, and induced disease by Xylella invasion to in Southern Italy. Pathogens 2021, 10, discuss major available tools to mitigate the damage consequent to the disease. 1035. https://doi.org/10.3390/ pathogens10081035 Keywords: bacterial diseases of non-wood plants; environmental IPM; alien; invasive; quarantine Academic Editors: Stefania Loreti and Marco Scortichini 1. The Insect-Borne Plant Pathogen Received: 21 June 2021 Xylella fastidiosa Wells et al., 1987 (Xf) [1] is a xylem-restricted “fastidious” bacterium Accepted: 12 August 2021 Published: 16 August 2021 that lives in plant xylem and foregut vector lumina [2–4] of some xylem-feeders auchenor- rhynchan [5]. Publisher’s Note: MDPI stays neutral Some phytopathological characteristics related to Xf (e.g., diversified range of plant with regard to jurisdictional claims in hosts) are due to the ability of the bacterium to acquire DNA from the environment through published maps and institutional affil- horizontal transfer [6]. Xf is able to infect more than 300 different host species including iations. crops, ornamental and spontaneous plants [7,8]. In addition, Xylella strains can recombine among themselves [9,10], enriching the gene pool. The genetic diversity of Xf strains allows them to infect several plants species but rarely diseasing them lethally. The bacterium may play a role in plant health, causing nonspecific water shortage symptoms or damage by plugging the xylem vessels [4,11–14]. Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. Moreover, Xf uses part of its vector’s cuticle as a nitrogen source employing enzymatic This article is an open access article chitinase to dissolve exoskeleton [15]; the vector also ingests xylem sap [16] for nitrogen distributed under the terms and and carbon sources. conditions of the Creative Commons Xylella fastidiosa is an exotic pathogen introduced in Europe by the trade of asymp- Attribution (CC BY) license (https:// tomatic coffee plants from Costa Rica [17]. Schaad et al. [18] proposed three Xf subspecies: creativecommons.org/licenses/by/ Xylella fastidiosa subsp. fastidiosa, previously named Xylella fastidiosa subsp. piercei (type 4.0/). strain ATCC 35879T, causing grape Pierce’s disease); Xylella fastidiosa subsp. multiplex Pathogens 2021, 10, 1035. https://doi.org/10.3390/pathogens10081035 https://www.mdpi.com/journal/pathogens Pathogens 2021, 10, x FOR PEER REVIEW 2 of 25 Pathogens 2021, 10, 1035 2 of 25 piercei (type strain ATCC 35879T, causing grape Pierce’s disease); Xylella fastidiosa subsp. multiplex(type strain (type ATCC strain 35871T, ATCC causing 35871T, plum causing leaf scald plum disease/phony leaf scald peachdisease/phony disease); Xylellapeach disease);fastidiosa subsp.Xylella paucafastidiosa(type subsp. strain pauca ICPM (type 15198, strain causing ICPM citrus 15198, variegated causing citrus chlorosis variegated or CVC chlorosisdisease). Furthermore,or CVC disease). literature Furthermore, reports Xylellaliterature fastidiosa reportssubsp. Xylellasandyi fastidiosa(type subsp. strain ATCCsandyi (type700598, strain causing ATCC oleander 700598, leaf causing scorch) oleander [19,20] and leafXylella scorch) fastidiosa [20,21]subsp. and morusXylella(found fastidiosa on subsp.Morus albamorusL.) [(found21]. The onXylella Morussubspecies, alba L.) [22]. namely Thesandyi Xylellaand subspecies,morus, were namely recently sandyi included and morusin Xylella, were fastidiosa recentlysubsp. includedfastidiosa in Xylella[22]. fastidiosa subsp. fastidiosa [23]. Moreover, Su et al. [[24]23] described a new Xylella species on Pyrus pyrifolia (Burm.f.) Nakai, 1926, in Taiwan named Xylella taiwanensistaiwanensis SuSu etet al.,al., 2016.2016. The olive strainstrain foundfound in in 2013 2013 in in the the Gallipoli Gallipoli area area (Apulia, (Apulia, South South Italy) Italy) that that cause cause the theOlive Olive Quick Quick Decline Decline Syndrome Syndrome (OQDS (OQDS or or CoDiRO, CoDiRO, in in Italian) Italian) is isXylella Xylella fastidiosa subsp.subsp. pauca ST53 (Xfp53) [25,26], [24,25], a compact phylotype constituted of some Costa Rican strains (Figure 11).). Xfp53Xfp53 appearsappears differentdifferent fromfrom thethe otherother pauca strains isolated in Central and South America on Citrus sinensis (L.) Osbeck, 1765 and OQDS strain can infectinfect Nerium oleander L., 1753, Coffea arabica L., 1753 and Mangifera indica L., 1753 [[27,28],26,27], as well as Olea europaea L., 1753. Other X. fastidiosa subsp. paucapauca strainsstrains infecting olive trees have also detected in Argentina [[29]28] and Brazil. The latter strain differs from the Xfp53 strain basing on MLST analysis [30]. [29]. Figure 1. (A) Immunofluorescence-positiveImmunofluorescence-positive Xylella cells; ( B) colonies of X. fastidiosa pauca ST53 isolated from a spittlebug- infected periwinkle onon epi- and transilluminated BCYEBCYE medium; ((C)) X. fastidiosa pauca ST53 from BCYE colony seen under a phase-contrast compound microscope. Xylella fastidiosafastidiosais is in in the the quarantine quarantine organism organism list [30 list,31 ][31,32] and it isand known it is as known a biological as a biologicalweapon for weapon the damage for the it damage can infer it tocan a infe country’sr to a country’s crop production crop production system [ 32system–37]. [33– The 38].bacterium The bacterium was detected was in detected Europe inin 2013 Europe [38] andin 2013 could [39] have and suspiciously could have entered suspiciously Kosovo entered(wrongly Kosovo mentioned (wrongly as Slovenia mentioned in Janse as Slovenia 2006) [39 in,40 Janse]. 2006) [40,41]. Xylella moves from plant to plant and invades the territory [[42,43]41,42] mainly by insectinsect vectors. SomeSome AphrophoridaeAphrophoridae can can also also acquire acquir thee the pathogen pathogen from from infected infected plants plants to trans- to transmitmit it to otherit to plantsother [plants43,44]. [44,45]. Aphrophoridae-borne Aphrophoridae-borne plant pathogen plant pathogen transmission transmission could be couldinterspecific be interspecific or intraspecific. or intraspecific.Xylella fastidiosa Xylellamay fastidiosa spread may solely spread by vectors, solely andby vectors, Xf invasion and Xfis vector-mediated,invasion is vector-mediated, eventually. Vector–host–pathogeneventually. Vector–host–pathogen interactions interactions determine whether determine or whethernot an incursion or not an or isolatedincursion pathogen or isolated outbreak pathogen will leadoutbreak to settlement, will lead persistence, to settlement, and persistence,resulting epidemic and resulting development epidemic [45 development]. [46]. As shall be in most cases of vector-bornevector-borne pathogens, the vector management is the primary pathogen management tool [[47–52].46–51]. XylellaXylella hashas secondary ways to pass from infected to to free host plant apart from the vectors, e.g., grafting grafting [53,54] [52,53] or or interplant self- self- grafting (inosculation), but secondary spread spreadinging means are negligible, and infected plant propagation is a way to invade a cultivated territory. Pathogens 2021, 10, 1035 3 of 25 2. Non-Vector/Vector Pest Damage The interest in vector-borne pathogen and vector control management rises because the interaction among the actors—vector, pathogen, and crop—causes relevant damage. We consider here first the proportionality of the damage inflicted by the insect pest alone, then discuss the damage due to the vector–pathogen
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