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Transmission of Xylella Fastidiosa by Naturally Infected Philaenus Spumarius (Hemiptera, Aphrophoridae) to Different Host Plants

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Transmission of Xylella Fastidiosa by Naturally Infected Philaenus Spumarius (Hemiptera, Aphrophoridae) to Different Host Plants UC Berkeley UC Berkeley Previously Published Works Title Transmission of Xylella fastidiosa by naturally infected Philaenus spumarius (Hemiptera, Aphrophoridae) to different host plants Permalink https://escholarship.org/uc/item/2rw7s5rm Journal Journal of applied entomology = Zeitschrift fur angewandte Entomologie, 141(1-2) ISSN 0931-2048 Authors Cornara, D C. Dongiovanni D. Bosco et al. Publication Date 2017-02-01 DOI 10.1111/jen.12365 Peer reviewed eScholarship.org Powered by the California Digital Library University of California J. Appl. Entomol. ORIGINAL CONTRIBUTION Transmission of Xylella fastidiosa by naturally infected Philaenus spumarius (Hemiptera, Aphrophoridae) to different host plants D. Cornara1, V. Cavalieri2, C. Dongiovanni3, G. Altamura2, F. Palmisano3, D. Bosco4, F. Porcelli1, R. P. P. Almeida5 & M. Saponari2 1 DiSSPA-UNIBA Aldo Moro, Sez. Entomologia e Zoologia, Bari, Italy 2 CNR Istituto per la Protezione Sostenibile delle Piante, Sede di Bari, Bari, Italy 3 Centro di Ricerca, Sperimentazione e Formazione in Agricoltura ‘Basile-Caramia’, Locorotondo, Bari, Italy 4 DISAFA – Entomologia, Universita degli Studi di Torino, Grugliasco, Torino, Italy 5 ESPM, University of California Berkeley, Berkeley, CA, USA Keywords Abstract spittlebugs, vector transmission, Xylella fastidiosa The recent establishment of Xylella fastidiosa subspecies pauca in the south- ern Italian region of Apulia threatens agricultural crops and the environ- Correspondence ment. Olive is an important and widespread ancient crop in Italy and, so Maria Saponari (corresponding author), CNR far, the most impacted host. The meadow spittlebug Philaenus spumarius Istituto per la Protezione Sostenibile delle (Hemiptera, Aphrophoridae) has been identified as a vector of X. fastidiosa Piante, Sede di Bari, Via Amendola, 165/A in southern Italy; this species is one of the most common potential vectors 70126 Bari, Italy. E-mail: [email protected] in Europe. To generate disease management strategies, data on X. fastid- iosa transmission by P. spumarius are necessary. Therefore, we carried out Received: July 17, 2016; accepted: August 21, transmission experiments by using field-collected spittlebugs in 2014 and 2016. 2015 (5 and 11 collection dates, respectively), and transferring groups of insects immediately on to recipient plants. Various host plant species were doi: 10.1111/jen.12365 tested: olive, oleander, sweet orange, grapevine and the stone fruit root- stock GF677 (Prunus persica 9 Prunus amygdalus). Xylella fastidiosa was First and second authors equally contributed to the work. detected in all the host plants after insect plant access except for grape- vine; infections to sweet orange and stone fruit were not systemic. In 2015, estimates of insect X. fastidiosa infectivity were obtained; the num- ber of PCR-positive P. spumarius on each plant was positively correlated with the plant infection status. The proportion of P. spumarius infected with X. fastidiosa ranged from 25% to 71% during the entire survey per- iod. The number of X. fastidiosa cells detected in P. spumarius heads ranged from 3.5 9 10 to 4.0 9 102 (CFU equivalents), which is lower than that reported for leafhopper vectors in the Americas. These data show that field-collected P. spumarius have high rates of X. fastidiosa infection and are competent vectors. biological invasion that required endemic competent Introduction vectors for establishment (Almeida and Nunney Pathogen introduction is often regarded as the main 2015). In 2013, olive trees (Olea europaea) on the west driver of emerging infectious diseases, although an coast of the Salento Peninsula (Apulia, Italy) showing arthropod-borne pathogen accidentally introduced in leaf scorch and dieback, that is an unknown disease a new region requires a vector for establishment (Fer- named ‘olive quick decline syndrome’ (OQDS), were eres 2015). The introduction of Xylella fastidiosa into found to be infected with X. fastidiosa subspecies pauca Europe (Martelli et al. 2016) is an example of a (Saponari et al. 2013). Xylella fastidiosa has been 80 J. Appl. Entomol. 141 (2017) 80–87 © 2016 The Authors. Journal of Applied Entomology Published by Blackwell Verlag GmbH. This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made. D. Cornara et al. X. fastidiosa transmission by P. spumarius detected in olive in the USA (Krugner et al. 2014; cv. Coratina, cv. Ogliarola (two autochthonous olive X. fastidiosa subsp. multiplex), Argentina (Haelterman cultivars widely grown in the Apulia region) and olive et al. 2015; X. fastidiosa subsp. pauca) and more seedlings obtained from seeds of the cv. Cima di Mola; recently in Brazil (Coletta-Filho et al. 2016; X. fastid- (ii) oleander (Nerium oleander); (iii) sweet orange iosa subsp. pauca). There are limited data on X. fastid- (Citrus sinensis) cv. Madame vinous; (iv) grapevine iosa infecting olives, but evidence indicates that (Vitis vinifera) cv. Cabernet Sauvignon; (v) stone fruit pathogen genotype defines pathogenicity. While rootstock GF677 (hybrid Prunus persica 9 Prunus dul- X. fastidiosa is associated with but does not cause dis- cis), commonly used for stone fruits breeding; and (vi) ease in olives in the USA (Krugner et al. 2014), periwinkle (Catharanthus roseus). For the two olive Koch’s postulates have been fulfilled in Italy (Sapo- cultivars and grapevines, experimental plants con- nari et al. 2016); pathogenicity data are not available sisted of self-rooted cuttings; for the stone fruit root- from Brazil or Argentina. stock GF677, they consisted of micropropagated Only one genotype, based on multilocus sequence plantlets, whereas seedlings were used for sweet typing, has been recovered from olive trees and other orange cv. Madame Vinous and olive. All the plants hosts in Italy (Loconsole et al. 2016). The genotype is were grown in a greenhouse located on the premises an identical match to X. fastidiosa subsp. pauca strain of the Campus of the University of Bari (in the pest- ST53, reported from Costa Rica in 2014 (Nunney et al. free area). Plants of 15–20 cm with young vegetating 2014; Giampetruzzi et al. 2015). In Italy, ST53 has been apexes were then transferred in a screenhouse in the detected in cherry (Prunus avium L. 1755), myrtle-leaf infected area where the transmission tests were milkwort (Polygala myrtifolia L.), coastal rosemary (Wes- carried out. tringia fruticosa Willd.), acacia (Acacia saligna Labill.) and Spanish broom (Spartium junceum L.). To date, the host Transmission tests range of this genotype includes 22 plant species (Locon- sole et al. 2016). It has been demonstrated that the We collected adult P. spumarius every 2 weeks from meadow spittlebug Philaenus spumarius was a vector of May to October, from infected olive orchards in Gal- X. fastidiosa in Italy using periwinkle as an indicator lipoli (Apulia, Italy), by sweeping net and mouth aspi- plant Saponari et al. (2014); it has also been demon- rator. Insects were collected either from canopy or strated that P. spumarius transmits X. fastidiosa from suckers of olive trees with severe symptoms of desic- infected to uninfected olive trees (Cornara et al. 2016a). cation and dieback. Two distinct olive groves severely Unfortunately, this vector species is ubiquitous and affected by OQDS (with 100% of symptomatic trees), highly polyphagous; the nymphs can feed on huge vari- one in 2014 and another one in 2015, were selected eties of herbaceous plants, while the adults disperse to for insect collection; in both olive groves, the presence an even higher number of plant species, including of X. fastidiosa in olive trees (ca. 200) was confirmed many trees and shrubs (Weaver and King, 1954; by real-time quantitative polymerase chain reaction Delong and Severin 1950). In the contaminated area, (qPCR) (data not shown). Spittlebugs were temporar- olive is the predominant host in the cultivated areas, ily stored in groups of five individuals in aerated plas- although other perennial hosts have been identified, tic vials and brought to an insect-free transfer room. mainly in non-cultivated areas, such as gardens and We caged five randomly selected spittlebugs on each natural landscape. However, since both X. fastidiosa and recipient plant. Cages were made with fine mesh net P. spumarius have a wide host range (EFSA 2015), and sealed at the superior rim of the pot with two rubber plant community composition is important in the epi- bands. Transmission tests took place in an insect-proof demiology of X. fastidiosa -associated diseases, we con- screenhouse. A 4-day and 7-day inoculation access ducted studies in order to (i) evaluate the transmission period (IAP) and 7-day IAP were used in 2014 and of X. fastidiosa by P. spumarius to different host plants 2015, respectively. For each treatment (i.e. host species and cultivars; and (ii) assess P. spumarius natural plant), five replicates were performed; five plants of infectivity in olive orchards infected by X. fastidiosa. the same species/cultivar for each date with five insects per plant, except for periwinkle, for which two replicates per date were used. At the end of the IAP, Material and Methods insects were removed from the plants and stored in Plants 75% ethanol. P. spumarius was identified according to Ossiannilsson (1981). Plants were treated with a sys- Plants used for the transmission experiments included temic insecticide (Imidacloprid, Confidor 200 SL), different species and cultivars: (i) olive (Olea europaea) stored in an insect-free screenhouse and tested by J. Appl. Entomol. 141 (2017) 80–87 © 2016 The Authors. Journal of Applied Entomology Published by Blackwell Verlag GmbH. 81 X. fastidiosa transmission by P. spumarius D. Cornara et al. qPCR. In 2015, the presence and the population size Table 1 Detection of Xylella fastidiosa in leaf samples of the recipient of X. fastidiosa in P. spumarius were determined by plants. Samples were collected at the insect feeding site and on the qPCR in insects surviving the IAP.
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