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Transmission of Xylella Fastidiosa to Grapevine by the Meadow Spittlebug

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Ecology and Epidemiology Transmission of Xylella fastidiosa to Grapevine by the Meadow Spittlebug D. Cornara, A. Sicard, A. R. Zeilinger, F. Porcelli, A. H. Purcell, and R. P. P. Almeida First and fourth authors: DiSSPA, sez. Zoologia ed Entomologia, Universita` degli Studi di Bari Aldo Moro, via Amendola 165/A, 70126 Bari; and second, third, fifth, and sixth authors: ESPM, University of California-Berkeley, 130 Mulford Hall 3114, Berkeley, CA 94720. Accepted for publication 30 June 2016. ABSTRACT Cornara, D., Sicard, A., Zeilinger, A. R., Porcelli, F., Purcell, A. H., and by P. spumarius increased with plant access time, similarly to insect vectors Almeida, R. P. P. 2016. Transmission of Xylella fastidiosa to grapevine in another family (Hemiptera, Cicadellidae). Furthermore, a positive by the meadow spittlebug. Phytopathology 106:1285-1290. correlation between pathogen populations in P. spumarius and trans- mission to plants was observed. Bacterial populations in insects were one There is little information available on Xylella fastidiosa transmission to two orders of magnitude lower than those observed in leafhopper by spittlebugs (Hemiptera, Cercopoidea). This group of insect vectors vectors, and population size peaked within 3 days of plant access period. may be of epidemiological relevance in certain diseases, so it is important These results suggest that P. spumarius has either a limited number of sites to better understand the basic parameters of X. fastidiosa transmission in the foregut that may be colonized, or that fluid dynamics in the by spittlebugs. We used grapevines as a host plant and the aphrophorid mouthparts of these insects is different from that in leafhoppers. Altogether Philaenus spumarius as a vector to estimate the effect of plant access time our results indicate that X. fastidiosa transmission by spittlebugs is similar on X. fastidiosa transmission to plants; in addition, bacterial population to that by leafhoppers. In addition, the relationship between cell numbers in estimates in the heads of vectors were determined and correlated with plant vectors and plant infection may have under-appreciated consequences to infection status. Results show that transmission efficiency of X. fastidiosa pathogen spread. The bacterium Xylella fastidiosa is an economically important of plant pathogens. Machaerotids are tube-building insects that plant pathogen that is present throughout the Americas, Europe have not been shown to transmit X. fastidiosa but are vectors of (Italy and France), Asia (Taiwan), and the Middle-East (Almeida Ralstonia syzygii, a xylem-colonizer that causes Sumatra disease of and Nunney 2015). The lifestyle of X. fastidiosa requires the clove trees (Eden-Green et al. 1992). Insects in the other three colonization of insect and plant hosts; in addition, natural dispersal families have been shown to transmit X. fastidiosa. Severin (1950) is solely mediated by insect vectors (Chatterjee et al. 2008). demonstrated that three aphrophorids (Philaenus spumarius [syn. Therefore, knowledge about insect and plant colonization, as well Philaenus leucophthalmus], Aphrophora angulata,andAphrophora as plant-to-plant transmission can guide the development of control permutata)andoneclastopterid(Clastoptera brunnea) were vectors strategies for diseases caused by X. fastidiosa. Traditionally, of X. fastidiosa. Purcell (1980) and Saponari et al. (2014) also research has focused on how this pathogen colonizes host plants, confirmed that P.spumarius was a vector of this bacterium to plants. with some but more limited attention given to insect hosts. In In addition, Clastoptera achatina (Clastopteridae) and Lepyronia addition, some of the key parameters of X. fastidiosa vector quadrangularis (Aphrophoridae) were shown to transmit X. fastidiosa transmission have been determined. to pecans (Sanderlin and Melanson 2010). Severin (1950) referred to Insect vectors belong to three groups of xylem sap-feeding P. spumarius as P. leucophtalmus; he also stated that five varieties insects, the sharpshooter leafhoppers (Hemiptera: Cicadellidae of the meadow spittlebugs were tested (leucophtalmus, pallidus, Cicadellinae), spittlebugs (Hemiptera: Cercopoidea), and cicadas fabricii, marginellus,andimpressus). In 1961, the Commission (Hemiptera: Cicadoidaea). There are only two reports of cicadas as of Zoological Nomenclature decided that the valid specific name vectors (Krell et al. 2007; Paia˜o et al. 2002), and because of the for this taxon was spumarius and not leucophtalmus; the poly- limited information more research is required on the role of these morphism and variation of wing markings generated confusion in insects in X. fastidiosa spread. The first identified X. fastidiosa the nomenclature (Yurtsever 2000). vectors were sharpshooter leafhoppers (Hewitt and Houston 1946; Severin (1950), however, was the only study to provide informa- Hewitt et al. 1942). Frazier and Freitag (1946) demonstrated that tion on the characteristics of transmission other than vector identifi- several leafhopper species transmitted X. fastidiosa, information cation. In that study it was shown that P. spumarius transmission of which decades later led Frazier (1965) to propose that xylem sap X. fastidiosa lacked a detectable latent period (shortest period tested of feeding insects should be considered vectors of this pathogen until 2 h) and that the bacterium was persistently retained in adults (up to proven otherwise; this proposal still stands (Almeida and Nunney 76 days). The transmission of X. fastidiosa to plants by sharpshooter 2015). The superfamily Cercopoidea has five families, Aphrophor- leafhoppers has similar characteristics; it lacks a latent period (Purcell idae, Cercopidae, Clastopteridae, Epigydae, and Machaerotidae. and Finlay 1979) and is persistent in adults (Almeida and Purcell Epigyds have, to our knowledge, not been studied as insect vectors 2003b; Hill and Purcell 1995a). Additional work with leafhoppers has shown that X. fastidiosa is not transovarially (Freitag 1951) or transtadially transmitted (Almeida and Purcell 2003b; Purcell and Corresponding author: R. Almeida; E-mail address: [email protected] Finlay 1979). The lack of latent period, transovarial, and transtadial transmission, suggest that the retention site of X. fastidiosa is in the *The e-Xtra logo stands for “electronic extra” and indicates that one supplementary table is published online. foregut of leafhopper vectors, which was first shown using microscopy by Purcell et al. (1979). Recent work by Cornara et al. (2016) also http://dx.doi.org/10.1094/PHYTO-05-16-0202-R documented X. fastidiosa-like cells in the foregut of the aphrophorid © 2016 The American Phytopathological Society P. spumarius. The observed lack of X. fastidiosa genotype–vector Vol. 106, No. 11, 2016 1285 species specificity among leafhoppers has not been analyzed for needle inoculated (Almeida and Purcell 2003a). Every plant was spittlebugs, but these insects transmit X. fastidiosa strains belonging to inoculated at 5 and 20 cm from the base with a 5-µl drop of a 109 at least three different subspecies (Sanderlin and Melanson 2010; CFU/ml suspension (population assessed by dilution plating) in Saponari et al. 2014; Severin 1950), suggesting that this is also a sodium-citrate-phosphate (SCP) buffer with a number 1 entomo- conserved trait. Despite the lack of research on the Cercopoidea as logical pin. Plants were watered daily and fertilized once every vectors of X. fastidiosa, the limited information available suggests that month (Osmocote Plus 15-9-12). Source plants were tested for parameters of plant-to-plant transmission are similar to those described X. fastidiosa by culturing 1 month after inoculation, then pruned to for sharpshooter leafhoppers. 20 cm in height. One month after pruning, X. fastidiosa population Two important parameters affecting the spread of X. fastidiosa in the distal third of the plants was determined by culturing; plants diseases, however, are pathogen transmission efficiency (over time) with petiole samples with 3 to 6 × 106 CFU/ml (Hill and Purcell and rate (one time point), both of which vary based on host 1997) and 30 cm tall were used as source plants. Three-month-old plant–insect–pathogen combinations (Lopes et al. 2009; Purcell cuttings of V. vinifera Cabernet Sauvignon grown in 3 gallon- 1981). Transmission can also be affected by within plant feeding capacity pots in a mix of Supersoil, sand, and perlite (2:1:1), preferences by insect vectors (Daugherty et al. 2010) or vector watered daily, and fertilized monthly (Osmocote Plus 15-9-12), discrimination against disease symptomatic plant tissue (Zeilinger were used as recipient plants. We pruned the cuttings to 20 cm and Daugherty 2014). There are no data on spittlebug-X. fastidiosa height, also removing lateral shoots, 1 week prior to insect access. transmission efficiency (i.e., how the frequency of transmission Transmission efficiency. We tested how X. fastidiosa trans- events changes over time). In addition, the diagnostic and mission efficiency by P. spumarius on grapevines varied in relation quantification of X. fastidiosa cells in the foregut of insect vectors to durations of acquisition access period (AAP) and IAP. Five AAP has been challenging to perform until the more recent advent of and IAP treatments were used: 1.5; 4.5; 12; 24; and 48 h, each with molecular diagnostic tools for this purpose. Currently available data 30 independent replicates, keeping for each treatment a
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