1 Vectors of Xylella fastidiosa around the world: an overview
2
3 Daniele Cornara1§, Marina Morente1#, Anna Markheiser2#, Nicola Bodino3#, Tsai Chi-Wei4, Alberto 4 Fereres1, Joao Roberto Spotti Lopes5
5
6 Author affiliation:
7 1 Instituto de Ciencias Agrarias. Consejo Superior de Investigaciones Cientificas. ICA-CSIC. Calle 8 Serrano 115 dpdo, 28006 Madrid (Spain) 9 2 Julius Kühn-Institut, Federal Research Centre for Cultivated Plants, Institute for Plant Protection in 10 Fruit Crops and Viticulture, Siebeldingen, Germany
11 3 Institute for Sustainable Plant Protection - National Research Council of Italy, IPSP-CNR, Strada delle 12 Cacce 73, I-10135 Torino, Italy
13 4 Department of Entomology, National Taiwan University, Taipei, Taiwan
14 5 Department of Entomology and Acarology, Luiz de Queiroz College of Agriculture (Esalq), University 15 of São Paulo, Piracicaba, Brazil
16
17 § Corresponding author: [email protected], [email protected]
18 # These authors equally contributed to the work 19 Abstract
20 Long been considered restricted to the American continent, the bacterium Xylella fastidiosa has overcome
21 the geographical barriers due to global trading, and is now present in several countries across Europe and
22 Asia. The bacterium is transmitted by xylem-sap feeding insects likely without specificity. Therefore, once
23 introduced into an environment with suitable climatic conditions, X. fastidiosa short range dispersal may
24 rely on different vector taxa, being xylem-sap feeding apparently the only feature required for
25 transmission. Sharpshooter leafhoppers (Hemiptera: Cicadellidae: Cicadellinae) represent the best-studied
26 group of vectors of the bacterium. However, establishment of X. fastidiosa into new ecosystems lead
27 possibly to new interactions with vector taxa others than sharpshooters, and to novel epidemiological
28 scenarios. The critical analysis of similarities and differences among geographically distant outbreaks,
29 each with its own vectors guilds and patterns of pathogen spread, might open new perspectives for a better
30 understanding of vector-bacterium interaction, as well as for effective disease control. Therefore, the main
31 aim of this review is to provide the readers with an overview on vectors of X. fastidiosa around the world,
32 comprising the better-characterized North American, South American and Taiwan pathosystems, as well
33 as the ongoing research in Europe. This organic collection would permit to reflect on differences and
34 similarities among geographically and ecologically different bacterium outbreaks. Such critical analysis
35 and comparison of vector role in diverse epidemiological contexts is essential for developing an effective
36 bacterium control strategy.
37 38 Introduction
39 What is a vector? We would like to open this manuscript with a question that legitimately could raise up
40 in the mind of the reader of a review on “vectors” of Xylella fastidiosa. Many parasites and pathogens
41 responsible for some of the most important diseases in humans, agriculture and nature are routinely
42 described as “vector-borne”. According to Purcell (1982), a vector is a specific organism that transmits a
43 pathogen; a continuum of interactions, ranging from mutually beneficial to deleterious, may define the
44 relationship between a plant pathogen and its vector. Alternatively, a vector could be defined as: i) a host
45 within a multi-host transmission cycle; ii) the most mobile host in a transmission cycle of two or more
46 hosts (Wilson et al. 2017). The key defining feature of vector transmission is that every pathogen
47 generation (i.e. passing from one infected host to another infected host) involves contact with the vector
48 (Gandon 2004); this continuous interaction possibly shape pathogen evolution. Many evolutionary and
49 ecological models oversimplify much of the complexity of vectors: vectors are indeed often treated as
50 mobile syringes rather than organisms in their own right, and their broader ecology and behavior are
51 frequently ignored in transmission experimental schemes (Wilson et al. 2017; Del Cid et al. 2018). In
52 contrast, presence, abundance, and behavior of insect vectors in relation to infected and healthy plants,
53 are fundamental regulators of pathogen spread (Sylvester 1954; Irwin and Ruesink 1986; Mauck et al.
54 2018). Indeed, vector behaviour has profound ecological and evolutionary implications for the pathogens
55 they transmit, as the latter rely nearly entirely on their vectors for passage to new hosts (Stafford et al.
56 2011). This is especially true for the bacterium X. fastidiosa, whose natural short-range spread depends
57 exclusively on xylem-sap feeding insects (Frazier 1965), which are found in some groups of
58 Auchenorrhyncha. All the members of Cercopoidea (commonly known as froghoppers or spittlebugs) and
59 Cicadoidea (cicadas), as well as the leafhoppers (Membracoidea: Cicadellidae) of the subfamily
60 Cicadellinae (also known as sharpshooters), are considered preferentially xylem-sap feeders (Novotny
61 and Wilson 1997). Insects that feed preferentially on mesophyll or phloem, occasionally feed on xylem 62 (Pompon et al. 2011; Saguez et al. 2015), but are not able to transmit X. fastidiosa (Purcell, 1980). The
63 bacterium can be transmitted by grafting techniques and stem cuttings, which are commonly used for
64 propagation of fruit trees; other modes of spread independent of vectors, e.g. by pruning shears (Krell et
65 al. 2007), are considered unlikely (EFSA 2015). X. fastidiosa is a gram-negative xylem-limited gamma-
66 proteobacterium (Xathomonadales: Xanthomonadaceae), whose host list embraces 563 plant species
67 belonging to 82 families (EFSA 2018). While the bacterium behaves as a harmless endophyte in the
68 majority of its host plants (Purcell and Saunders 1999; Baccari and Lindow 2011), it causes disease
69 symptoms (mostly leaf scorch and dieback) on economically important crops (Purcell 1997). The
70 symptoms are thought to be the outcome of bacterial growth and clogging up of xylem vessels (Hopkins
71 1989). Sicard et al. (2018) suggests the bacterium is associated to a large number of plant species as
72 commensalist, but a limited number of clades and bacterial genotypes are responsible for, and specific to,
73 a small number of plant diseases. X. fastidiosa is unique as a vector-borne bacterium, since it is persistent
74 and propagative but not circulative within its insect vector (Hill and Purcell 1995). The transmission is
75 neither transstadial (Purcell and Finlay 1979) nor transovarial (Freitag 1951). After acquisition, the
76 bacterium is retained on the cuticular lining of the insect foregut, mostly in the part of the pre-cibarium
77 proximal to the cibarium (Almeida and Purcell 2006). Presence of X. fastidiosa cells inside the pre-
78 cibarium has been correlated with successful inoculation (Almeida and Purcell 2006). Bacterial cells
79 binding and successive foregut colonization is not a trivial process: it has been proposed that most of the
80 X. fastidiosa cells ingested by the vector are swallowed without being retained, as a result of the strong
81 turbulence originated within the foregut during sap ingestion (Dugravot et al. 2008; Retchless et al. 2014).
82 Once inside the foregut, X. fastidiosa has a generation time of 7-8 hours, with a multiplication rate that
83 remains constant up to four days, followed by a slow down due to limited space for colonization (Killiny
84 and Almeida 2009). However, bacterial multiplication and extensive colonization of the foregut appears
85 to be not necessary for transmission, since sharpshooters can inoculate healthy plants shortly (1-2 h) after 86 the onset of acquisition on infected plants (Purcell and Finlay 1979). Vectors of X. fastidiosa, long been
87 treated merely as pathogen carriers, should on the contrary be re-considered as hosts, whether primary or
88 alternative, of an organism “living in two worlds” (Chatterjee et al. 2008). Indeed the bacterium, through
89 a recently identified chitinase, exploits vector cuticular chitin as food source for multiplication (Killiny et
90 al. 2010; Labroussaa et al. 2017). Effects of this exploitation on vector behavior and performances deserve
91 further investigation. The mechanism underlying X. fastidiosa inoculation to the host plants is one of the
92 essential question mark of this fascinating pathosystem (Almeida 2016a). As demonstrated by Houston et
93 al. (1947), infection of the host plant occurs only when the vector is given access to the xylem vessels.
94 Backus (2016) proposed that X. fastidiosa is inoculated through a mechanism of salivation-egestion;
95 although many indirect evidences support this theory, a conclusive proof is still missing (Almeida 2016a).
96 Long-range dispersal of the bacterium mainly relies on trading of contaminated plant materials (EFSA,
97 2018); once introduced in a new environment with suitable abiotic conditions, the bacterium requires the
98 presence of efficient vectors for its short-range spread (Fereres 2015). Available data demonstrate that
99 insect vectors are capable of transmitting different bacterial strains without specificity (Almeida and
100 Nunney 2015; Esteves et al. in press). Therefore, independently from the genotype being introduced, any
101 environment with suitable climatic conditions should be considered at risk if competent vectors are
102 present. Moreover, climate change could broaden the suitable geographic range, making possible the
103 establishment of the bacterium in areas previously unsuitable (Godefroid et al. 2018). X. fastidiosa
104 remained until recently restricted to American continent (Almeida and Nunney 2015); Brazilian and USA
105 outbreaks, where sharpshooters play the key role as vectors in epidemiology, are the best characterized so
106 far. However, in the last decades, X. fastidiosa has been reported in several countries outside America:
107 India (Jindal and Sharma 1987), Turkey (Guldur et al. 2005), Taiwan (Su et al. 2013), Iran (Amanifar et
108 al. 2014) and several European countries (Berisha et al. 1998; Saponari et al. 2013; Denance et al. 2017;
109 Olmo et al. 2017; EFSA 2018) (Fig. 1). Evidences collected so far (Saponari et al. 2014; EFSA 2015; 110 Cornara et al. 2017a; Cornara et al. 2017b; Cruaud et al. 2018; EFSA 2018) suggest that, at least in Europe,
111 vectors others than sharpshooters, i.e. spittlebugs, cercopids, and cicadas, might play the key role in
112 bacterium epidemiology. Research on previously disregarded vector taxa, and comparison with the long
113 studied sharpshooters-X. fastidiosa relationship, might open new possibilities in order to deeply
114 understand the overall vector-bacterium interaction, and develop sustainable and effective disease control
115 strategies.
116 Therefore, the main aim of this review is to provide the readers with an overview on vectors of X.
117 fastidiosa around the world, comprising both the better-characterized North American, South American
118 and Taiwan pathosystems, and the more recent ongoing research in Europe. This organic collection would
119 also permit to reflect on differences and similarities among geographically and ecologically different
120 bacterium outbreaks. Such critical analysis and comparison of vector role in diverse epidemiological
121 contexts is essential for developing an effective bacterium control strategy.
122
123 124 Europe
125 In Europe, Berisha et al. (1998) first reported the detection of X. fastidiosa on grapevine in Kosova,
126 although the finding was never further confirmed. In 2012, the bacterium was detected in France, on coffee
127 plants confined in a containment facility (Jacques et al. 2015), but no further spread has been reported.
128 The first reported bacterium establishment in Europe took place in Apulia, South Italy (Saponari et al.
129 2013). In 2010, olive trees (Olea europaea) growing on the west coast of Salento Peninsula (Apulia, Italy),
130 began to decline because of a hitherto unknown disease consequently named “Olive Quick Decline
131 Syndrome” (OQDS) (Martelli et al. 2016). Following Saponari et al. (2013) detection, on 21th October
132 2013, Apulian Phytosanitary Service notified European Commission (EC) that the quarantine bacterium
133 X. fastidiosa had been detected in olive trees in Gallipoli (Lecce) (Almeida 2016 b). Results from genome
134 sequencing have shown that the bacterium has been likely introduced from Costa Rica (Giampetruzzi et
135 al. 2017). Southern Italian strain corresponds to genotype ST53, an introgression of X. fastidiosa
136 subspecies pauca genome into the genome of subsp. fastidiosa, which had been firstly reported by Nunney
137 et al. (2014). Apulian finding prompted a large-scale survey all around Europe, that led to successive
138 bacterium detection in Corsica, Balearic Islands, mainland France, mainland Spain, and Germany
139 (Denance et al. 2017; Olmo et al. 2017; EFSA 2018) (Fig. 2). In this review we will try to organically
140 collect and discuss observations carried out on proved/potential vectors within the European outbreaks
141 currently spotted and described. X. fastidiosa is considered as “transient-under eradication” in all the
142 European outbreaks detected so far, except for Southern Apulia, Corsica, and Balearic Islands, where the
143 current status is “present with a restricted distribution”. The outbreak in Germany is currently considered
144 eradicated (EFSA 2018). However, wherever in Europe X. fastidiosa is present or introduced, indigenous
145 xylem-sap feeders are present and may act as vectors (EFSA 2018). Only few species of sharpshooters
146 are present throughout the European countries, with a limited distribution (Wilson et al. 2009). Hence
147 spittlebugs and cicadas, previously disregarded in outbreaks other than the European ones, seem likely to 148 play the key role in X. fastidiosa epidemiology in Europe. A list of candidate vectors present across the
149 European detected bacterium outbreaks is provided in S. 1 (supplementary material); cicadas species have
150 been excluded since their vector competence is still uncertain (EFSA 2015).
151 To date, bacterial epidemiology has been described only for the Southern Italian outbreak so far, and only
152 focusing on olive orchards. No transmission studies have been carried out in other European countries,
153 and only data on molecular detection of the bacterium in candidate vectors are available (EFSA 2018).
154 By the way, all the data converge toward the hypothesis that the meadow spittlebug Philaenus spumarius
155 L., 1758 (Hemiptera: Aphrophoridae) could be one of the most important bacterial vectors in all the
156 epidemics described so far (EFSA 2018). The meadow spittlebug, an insect extremely polyphagous and
157 widespread all over the continent (Cornara et al. 2018), is responsible for the spread of the bacterium
158 inside cultivated olive orchards of South Italy, with olives serving either as reservoir or as recipient plant
159 of the bacterium (Cornara et al. 2017a). Nymphs, characterized by reduced mobility and usually common
160 on herbaceous plants belonging to Asteraceae, Fabaceae, Apiaceae and Geraniaceae families, likely play
161 no role in bacterial epidemiology (Dongiovanni et al. 2018a; Morente et al. 2018a). Surveys conducted in
162 South Italy, Portugal, Spain and Greece (Cornara et al. 2017a; Bodino et al. 2018; Dongiovanni et al.
163 2018b; Milonas et al. 2018; Morente et al. 2018a; Reis et al 2018) highlighted a similar trend of P.
164 spumarius population in olive orchards: after emergence on ground cover, the adults move to olive plants.
165 Pasture mowing or a general decrease in succulence of herbaceous hosts could underlie the dispersal
166 toward olive canopies (Goidanich 1954; Pavan 2006; Cornara et al. 2017a). Spittlebug adults tend to
167 aggregate on green succulent tissues (Wiegert 1964; Mangan and Wutz 1983). The aggregation,
168 maintained within certain levels to avoid competition, ensures a bottom up effect, for example overcoming
169 physical barriers to feed on xylem (Wise et al. 2006; Sanderlin and Melanson 2010; Cornara et al. 2018).
170 Aggregation of several possibly infective individuals on the same tissue may increase the probability of
171 systemic infection and reduce the incubation time (Daugherty et al. 2009; Krugner et al. 2012). 172 Furthermore, within-field vector aggregation could underlie the aggregated pattern of bacterial infections
173 observed in olive orchards (Montes-Borrego et al. 2017). During summer, spittlebug population density
174 within the olive orchard dramatically decreases, likely as a result of insect dispersal and search for over-
175 summering hosts, such as Quercus sp., Lentiscus sp., Myrtus sp., Juniperus sp., Lavandula sp., among
176 others (Cornara et al. 2017a; Bodino et al. 2018; Dongiovanni et al. 2018a; Milonas et al. 2018; Morente
177 et al. 2018a; Reis et al 2018). This dispersal could be epidemiologically relevant, determining a spillover
178 of X. fastidiosa from cultivated olive groves to wild areas: infective insects moving outside the cultivated
179 orchard could transmit the bacterium to unmanaged ecosystems, creating new and hardly detectable
180 bacterium reservoirs. Spittlebugs active dispersal seems to be primarily limited by their short-range flight
181 (Cornara et al. 2018). P. spumarius has been reported to move more than 30 m with a single flight and up
182 to 100 m within 24 h (Weaver & King 1954; Cornara et al. 2018). Recently, dispersal capabilities of P.
183 spumarius were studied through a Mark-Release-Recapture experiment carried out during summer and
184 autumn in olive groves and meadow agroecosystems in Apulia (South Italy) and Piedmont (North Italy),
185 respectively (Plazio et al. 2017). During this study, the authors reported a mean dispersal of 60-70 meters
186 from the release point either on olive plants or meadow within approximately 15 days. In contrast with
187 these observations, recent preliminary studies conducted with flight mill highlighted that P. spumarius
188 could have the innate potential to fly longer distances (ranging from 100 to ca. 1000 meters with a single
189 flight) (Lago, unpublished data). Passive movements of spittlebug through the wind, and through
190 “hitchhiking” with vehicles, are also possible and may allow the dispersal of infected insects over long
191 distances (Wiegert 1964; Halkka et al. 1971; Cornara et al. 2018). Successively, at the end of summer, the
192 spittlebug tends to move back to the cultivated orchards for oviposition, with individuals been collected
193 also on olive suckers. Infective individuals re-entering the cultivated orchards, attracted by the green
194 succulent suckers, could infect/re-infect olive plants, with a higher transmission efficiency compared to
195 younger adults (Bodino et al. 2018). Further xylem-sap feeding species, other than the meadow spittlebug, 196 were collected from olive canopies in Southern Italy and Spain: cicadas, mainly Cicada orni L., 1758
197 (Hemiptera: Cicadidae), and Neophilaenus campestris Fallen, 1805 (Hemiptera: Aphrophoridae) (Cornara
198 et al. 2017a; Morente et al. 2018a). Regarding C. orni, in a recent unpublished natural infectivity test,
199 three out of 160 cicadas tested positive to X. fastidiosa by qPCR, while no transmission to olive recipient
200 plants occurred (Cornara et al. 2018). Nevertheless, even in case C. orni natural infectivity with X.
201 fastidiosa and transmission competence were confirmed, the cicada’s role could be limited to secondary
202 infection within a yet infected orchard. Indeed, the normal flight activity of almost all cicadas is limited
203 to short flights in case of disturbances (Nickel and Hildebrandt 2003; Simões and Quartau 2007). N.
204 campestris has been recently proven to be a competent vector of X. fastidiosa to olive, together with the
205 South Italian endemism P. italosignus Drosopoulos & Remane, 2000 (Hemiptera: Aprophoridae) (EFSA
206 2018). N. campestris’ role in bacterial epidemiology in olive orchards appears unlikely (EFSA 2018).
207 Indeed, species belonging to the genus Neophilaenus are usually associated to Poaceae in dry grasslands
208 (Nickel and Remane 2002). N. campestris tends to prefer monocots such as Avena sp. and Bromus sp.
209 Very few individuals can be occasionally collected on olive canopies, in correspondence with spittlebug
210 dispersal toward over-summering hosts, mainly conifers as Pinus halepensis (Mazzoni et al. 2005; Lopes
211 et al. 2014; Morente et al. 2018a). Despite its minor or no importance in bacterial transmission to olive,
212 N. campestris could be relevant for maintenance of bacterial inoculum in wild areas bordering cultivated
213 orchards during dispersal and oversummering. Therefore, future research should focus on wild areas
214 surrounding cultivated orchards, seeking for bacterial reservoirs, and characterizing vectors ecology and
215 dynamic in such areas. P. spumarius competence in transmitting the bacterium to plants other than olive
216 has been demonstrated under controlled conditions (Cornara et al. 2017b). Nevertheless, without field
217 observations on pathogen epidemiology, neither bacterial detection within vector nor transmission tests
218 under controlled conditions could prove or disprove insect role in bacterial spread (EFSA 2018). As
219 mentioned above, almost no epidemiological data are available for outbreaks others than the Southern 220 Italian one. Regarding mainland France, only faunistic studies were produced so far (EFSA 2018). On the
221 contrary, a large range of potential vectors have been identified in Corsica, although only P. spumarius
222 individuals were found infected with X. fastidiosa as determined by PCR. According to Cruaud et al.
223 (2018), the key plant in X. fastidiosa epidemiology across the island is Cistus monspeliensis, which is also
224 reported by the authors as the main host plant for either nymphs or adults of P. spumarius. Nevertheless,
225 considering the meadow spittlebug polyphagy, the epidemiological frame described so far for Corsica
226 appears scattered and incomplete, and deserve further investigation. Considering Balearic Islands
227 outbreaks, several bacterial genotypes threatening different economically important crops such as olive,
228 grapevine, fig and almond, have been spotted (Olmo et al. 2017). Among the xylem feeders sampled and
229 tested for X. fastidiosa from the first detection (2016) to date, i.e. P. spumarius, N. campestris, and N.
230 lineatus L., 1758 (Hemiptera: Aphrophoridae), none has proven to be infected with the bacterium. Balearic
231 Islands outbreak differs in many ways from the two outbreaks detected in mainland Spain, i.e. Alicante
232 (Valle de Guadalest, East coast) and Madrid (Villarejo de Salvanes, central Spain), where only one
233 bacterial strain is apparently present (subspecies multiplex, strain ST6) (EFSA 2018). In Alicante, where
234 almond is apparently the only economically important crop harboring X. fastidiosa, the bacterium has
235 been detected in P. spumarius (27% of the individuals tested) and N. campestris (1.2%), which were
236 sampled across infected almond orchards (EFSA 2018). The nymphs of both spittlebug species have been
237 observed starting from April on ground cover within cultivated almond orchards; adults were found on
238 almond canopies starting from mid-May (Morente et al. 2018b). As previously remarked, no transmission
239 studies have been conducted so far, thus no conclusion about epidemiology can be drawn. Nevertheless,
240 given the high transmission efficiency of X. fastidiosa to almond by P. spumarius (Purcell 1980), it can
241 be hypothesized that the meadow spittlebug in almond orchards of Alicante could play a role similar to
242 the one in olive orchards of Southern Italy. In Madrid, X. fastidiosa has been detected on olive trees cv.
243 Picual; the outbreak is currently supposed to be eradicated (EFSA 2018). Morente et al. (2018a) found P. 244 spumarius and N. campestris to be associated with olive canopies in Madrid province, although at far
245 lower extent than population densities observed in South Italy. Currently no data, neither molecular nor
246 transmission tests, are available for this outbreak. The main differences between the Madrid and the
247 Southern Italian outbreaks are apparently three: i) the different climatic conditions, with winter
248 temperatures in South Italy milder than central Spain; ii) the possible low pathogenicity to olive of the
249 strain detected in Madrid compared to the ST53 established in Italy (see Krugner et al. 2014); iii) the
250 lower vector population density found in Madrid olive orchards compared to the one reported by Cornara
251 et al. (2017a) for South Italy. These three factors could account for the current limited spreading of X.
252 fastidiosa across Madrid province. Regarding Germany, strain ST1 (subspecies fastidiosa) was found in
253 2016 in the region of Saxony (Pausa, Center-East), at one location in isolated plants of Nerium oleander,
254 Rosmarinus officinalis, Streptocarpus hybrids and Erysimum hybrids kept in a greenhouse (EFSA 2018).
255 Although the outbreak is considered nowadays eradicated, the detection of the Pierce’s disease strain has
256 been perceived as a serious threat to German viticulture. Therefore, surveys in German vineyards aimed
257 at characterizing potential vectors of X. fastidiosa to grape were suddenly started after the first bacterial
258 detection, and are currently ongoing (Markheiser et al. 2018). Apparently, the fauna of xylem-feeders
259 associated to German vineyards (at least in the area where X. fastidiosa was detected) appears to be more
260 variegated than that reported for other crops in Spain, Italy or France. Beside the predominant spittlebug
261 species P. spumarius, other xylem-feeders were found in surveyed vineyards, namely N. campestris, N.
262 lineatus, Aphrophora alni Fallen, 1805 (Hemiptera: Aphrophoridae), Evacanthus interruptus L., 1758
263 (Hemiptera: Cicadellidae: Evacanthinae), E. acuminatus Fabricius, 1794 and Cicadella viridis Latreille,
264 1802 (Hemiptera: Cicadellidae: Cicadellinae), as well as the froghopper Cercopis vulnerata, Leach 1815
265 (Hemiptera: Cercopidae) (Markheiser et al. 2017). Except for Evacanthus spp., all these species were
266 collected on grapevine plants; an estimation of population abundance is ongoing (Markheiser et al.
267 unpublished). P. spumarius has been demonstrated to be an efficient vector of X. fastidiosa to grapevine 268 (Severin 1950; Cornara et al. 2016). Regarding the other six species found to be associated to grapevine,
269 no data are available in literature on their vector competence. Neophilaenus spp. role in bacterium
270 transmission to grape seems unlikely, given that the spittlebugs are generally associated with Poaceae
271 (Braasch 1960). Nevertheless, N. campestris was collected together with P. spumarius on sprouting
272 grapevines in Southern Italy (Cornara, pers. obs.). Considering C. viridis, Balachowsky (1941) observed
273 that nymphs of this species migrate from trees, on which they hatch, to grass fields where they feed on
274 the basal part of the plant, e.g. on Polygonum fagopyrum, Phragmites sp., Cyperus sp., Arundo sp. and
275 Juncus sp. (Whalley 1958; Tay 1972). On the contrary, females lay eggs on different host plants, among
276 which grapevine (Goidanich 1938; Betram and Mannheins 1939: Balachowsky 1941; Schindler 1960;
277 Dirimanov and Kharizanor 1964; Tay 1972; Nickel and Remane 2002; Mazzoni 2005). Therefore,
278 theoretically C. viridis could spread the bacterium to a large range of cultivated and wild host species
279 during dispersal for oviposition, including grapevine. A. alni is assumed to feed on several broad-leaved
280 trees and shrubs, especially in wild areas, including Alnus sp., Elaeagnus sp., Myrica gale, Acer sp.,
281 Castanea sativa, Quercus sp., fruit trees (Prunus avium and P. dulcis), and grapevine (Thompson 1999;
282 Mazzoni 2005; Kunz et al. 2011; Markheiser et al. 2018). Therefore, at least at a theoretical level, A. alni
283 could be relevant in X. fastidiosa transmission to economically important crops, including grape, and
284 transmission studies with this candidate vector are urgently required. Another xylem-feeder, namely
285 Graphocephala fennahi Young, 1977 (Hemiptera: Cicadellidae), characterized by a more restricted
286 distribution compared to the other species previously described, was also collected on grapevine, although
287 only occasionally (Markheiser et al. 2017). Hamilton (1983) reported the sharpshooter to feed exclusively
288 on leaves and buds of Rhododendron sp. in the Nearctic region, whereas in Europe records of the insect
289 refer to a broad spectrum of plant species. Adults were observed on Acer platanoides, Platanus sp. Tilia
290 sp., Ilex aquifolium, Hedera helix, Robina pseudoacacia, Rumex acetosa, Azalea sp., Pyris japonica and 291 Forsythia sp. (Moacos 1953; Olthoff 1986; Sergel 1987). Overall, considering these reports, G. fennahi’s
292 role in X. fastidiosa spread within German vineyards seems unlikely.
293
294
295 296 North America
297 Most of the background on X. fastidiosa transmission by vectors come from studies carried out in North
298 America, mainly focusing on the pathosystem of the Pierce’s disease (PD) of grapevine in California
299 (Rapicavoli et al. 2018). Many reviews thoroughly describe North American main vector species of the
300 fastidious bacterium, together with their biology, bionomic, role in bacterium epidemiology and control
301 strategies (Purcell and Frazier 1985, Redak et al. 2004; Almeida et al. 2005a; Janse and Obradovic 2010;
302 among others). Therefore, here we provide just a brief summary about the current state of knowledge
303 about vectors of X. fastidiosa in North America, in order to permit the comparison among the other
304 geographical areas that is the main focus of the review. As remarked above, the main vectors of X.
305 fastidiosa to different crops in North America are sharpshooters (Hewitt et al. 1942; Frazier and Freitag
306 1946; Houston et al. 1947; Delong and Severin 1949). Because of the low vector specificity and high
307 diversity of Cicadellinae species in tropical and temperate regions of the Americas, some crops affected
308 by X. fastidiosa are visited by numerous hopper species that can act as vectors (Redak et al. 2004). These
309 numbers probably depend more on how many species have been tested than on how many species are
310 capable of transmitting X. fastidiosa (Almeida et al. 2005a). Except for the report by Sanderlin and
311 Melanson (2010) of Pecan Leaf Scorch in southeastern USA, spittlebugs involvement in bacterial
312 epidemiology is considered marginal, and they might just play a role in inoculum maintenance (Almeida
313 et al. 2005a). However, Purcell’s investigations on Almond leaf scorch (ALS) led to conflictive results
314 about possible role of P. spumarius in ALS spread, with low spittlebug abundance in surveyed orchards
315 compensated by very high bacterium transmission efficiency (Purcell 1980). The most important vectors
316 of X. fastidiosa to different economically important crops in North America are: Cuerna costalis
317 Fabricious, 1803 (Hemiptera: Cicadellidae), Draeculacephala minerva (known as green sharpshooter)
318 Ball, 1927 (Hemiptera: Cicadellidae), Graphocephala atropunctata (known as blue-green sharpshooter,
319 BGSS) Signoret, 1854 (Hemiptera: Cicadellidae), G. versuta Say, 1830, Homalodisca insolita Walker, 320 1858 (Hemiptera: Cicadellidae), H. vitripennis (known as glassy-winged sharpshooters, GWSS) Germar,
321 1821, Oncometopia nigricans Walker, 1851 (Hemiptera: Cicadellidae), O. orbona Fabricius 1798 , and
322 Xyphon (formerly Carneocephala) fulgida (known as red-headed sharpshooter) Nottingham, 1932
323 (Hemiptera: Cicadellidae) (Janse and Obradovic 2010). A list of host plants and distributions of insect
324 vectors involved in the transmission of X. fastidiosa in Southern United States is reported by Overall and
325 Rebek (2017).
326 Among the vectors associated with PD , H. vitripennis is nowadays considered the most important because
327 of its high mobility, extreme polyphagy and wide distribution on various crops that are susceptible to X.
328 fastidiosa (Redak et al. 2004), even though its relatively inefficient transmission rate (Almeida and Purcell
329 2003). Nevertheless, the relatively low bacterium transmission efficiency is compensated by a very high
330 population density, built by the insects inside cultivated orchards, which reach levels up to 1-2 million
331 individuals/ha (Phillips 1998; Coviella et al. 2006). H. vitripennis is the only confirmed invasive vector
332 of X. fastidiosa (Almeida and Nunney 2015), native to the Southeast of the United States and North
333 Mexico (Young 1958; Turner and Pollard 1959). Furthermore,the species is thought to be relevant for
334 spreading of other X. fastidiosa-mediated diseases such as Oleander Leaf Scorch (OLS), Almond Leaf
335 Scorch (ALS), Phony Peach Disease (PPD) and Plum Leaf Scald (PLS) (Hernandez-Martinez et al. 2007;
336 2009). The species has a very broad host range, with more than 70 host plant species belonging to 35
337 families, including avocado, citrus, macadamia, and many woody ornamentals, e.g. Fraxinus sp.,
338 Lagerstroemia sp. and Rhus sp. (Redak et al. 2004; Almeida et al. 2005a).
339 G. atropunctata is also an important PD vector, although somewhat restricted to coastal areas of
340 California, where vineyards are bordered by riparian woods, which serve as overwintering habitats for
341 this sharpshooter (Purcell 1975). The BGSS is important for primary spread of X. fastidiosa from wild
342 vegetation bordering the vineyard to grapevine plants during early spring; secondary vine-to-vine spread
343 mediated by this vector, if occurring, does not lead to chronic infections (Purcell and Hopkins 2002; Redak 344 et al. 2004). Indeed, BGSS tends to settle and feed on the apical part of new succulent grapevine shoots;
345 therefore, infections that take place after inoculation by BGSS later than May are much less likely to move
346 down to woody tissues and to persist after winter pruning (Purcell 1975; Feil and Purcell 2001; Daugherty
347 et al. 2010). On the contrary, GWSS tendency to feed on woody tissues, and capability to inoculate even
348 dormant grapevines, potentially lead to chronic infections of X. fastidiosa even after summer or fall
349 inoculations, thus exponentially increasing the importance of bacterium secondary vine-to-vine spread
350 (Almeida and Purcell 2003; Almeida et al. 2005b). Moreover, H. vitripennis’ active movements among
351 several habitats and host plants allow rapid spread of X. fastidiosa over a wide area, whereas movements
352 of G. atropunctata are more limited to riparian vegetation and neighbouring vineyards (Blua et al. 2001;
353 Redak et al. 2004). Alfalfa (Medicago sativa), planted near to almond and grape, may play a role in the
354 epidemiology of PD and ALS disease, since it may act as either bacterium or vectors reservoir, both BGSS
355 and GWSS (Sisterson et al. 2010).
356 D. minerva and X. fulgida are more closely associated with PD epidemics in vineyards neighbouring
357 irrigated pastures and alfalfa fields in the Central Valley of California (Hewitt et al. 1942; Winkler et al.
358 1949). Observations that the worst outbreaks of PD were invariably in vineyards or portions of vineyards
359 near permanent pastures, alfalfa fields, or permanent irrigation ditches led early investigators to
360 concentrate on these habitats as possible sources of insect vectors. Neither D. minerva nor X. fulgida,
361 however, were ever found frequently on grape. Grapevine apparently was only an occasional or
362 "accidental" host plant that, nonetheless, could be infected after exposure to infective individuals (Frazier
363 1943; Delong and Severin 1949; Winkler et al. 1949). Early studies by Weimar (1933; 1937) concluded
364 that the frequency of irrigation exerted a "marked effect" in increasing the incidence and severity of the
365 disease. The author suggested that frequent irrigation produces luxuriant stands of grass weeds, probably
366 including Echinochloa crusgalli and Cynodon dactylon, triggering the built up of abundant populations
367 of both the insect species. 368 In central Florida, O. nigricans is thought to be a more important vector of PD than H. vitripennis because
369 it develops larger populations on grapevines in early spring (Adlerz and Hopkins 1979). Contrary to
370 epidemiology observed in California, spread of PD in Florida depends primarily on secondary spread
371 vine-to-vine (Adlerz and Hopkins 1979). Climatic factors seem to underlie the observed difference:
372 Florida has warm night and long growing seasons that support uninterrupted multiplication by X.
373 fastidiosa, thus even late inoculation might lead to chronic infections; in California, cool nights below
374 15°C could interrupt bacterial growth, shorter growing season, grapevine dormancy and limit the
375 establishment of chronic infections to early spring inoculations (Feil and Purcell 2001; Hopkins and
376 Purcell 2002).
377
378
379
380 381 South America
382 Plum leaf scald (PLS) was the first disease caused by X. fastidiosa reported in South America, initially in
383 Argentina (Fernandez-Valiela and Bakarcic 1954; Kitajima et al. 1975) and decades later in Paraguay and
384 Southern Brazil (French and Kitajima 1978; Kitajima et al. 1981). PLS is considered one of the most
385 limiting factors for plum production in Southern states of Brazil (Eidam et al. 2012). Despite the severity
386 of PLS disease, X. fastidiosa gained notoriety as a plant pathogen in South America only when it was
387 shown to be the causal agent of a disease of sweet orange trees named Citrus Variegated Chlorosis (CVC)
388 (the same disease was called “Pecosita” in Argentina) (Rossetti et al. 1990; Brlansky et al. 1991; Chang
389 et al. 1993). CVC rapidly spread to all citrus growing regions of Brazil in the 1990´s and reached average
390 incidences of up to 43% in Sao Paulo State, the major citrus growing region (Bové and Ayres 2007). All
391 sweet orange varieties were found to be susceptible to CVC; on the contrary, most mandarins are tolerant,
392 whereas limes and lemons are resistant (Laranjeira et al. 2005). During a search for alternative hosts of
393 CVC in northern São Paulo state, coffee plants were also found infected with X. fastidiosa, showing a
394 typical branch atrophy characterized by internode shortening, reduction in fruit and leaf size, premature
395 senescence and fall of leaves at the basal portion of the stems (Paradella Filho et al. 1997). The Koch´s
396 postulates were fulfilled showing that the bacterium is the causal agent of this disease, which was named
397 as Coffee leaf scorch (CLS) (Lima et al. 1998). Further surveys showed that the bacterium is widespread
398 in coffee plantations of several regions of Brazil (Rocha et al. 2010). Recently, X. fastidiosa was found in
399 association with leaf scorching symptoms in olive trees in Argentina (Haelterman et al. 2015) and
400 Southeastern Brazil (Coletta-Filho et al. 2016), causing a disease similar to OQDS in Italy. In Brazil, the
401 disease is widely distributed in orchards of the states of Minas Gerais and São Paulo (Safady et al. in
402 press). All strains of X. fastidiosa infecting citrus, coffee and olives in South America belong to subsp.
403 pauca, whereas most plum-infecting strains belong to subsp. multiplex and a few of them to pauca
404 (Almeida et al. 2008; Haelterman et al. 2015; Coletta-Filho et al. 2017). 405 After X. fastidiosa was confirmed as the causal agent of CVC (Chang et al. 1993), various surveys of
406 Auchenorrhyncha species associated with affected crops were conducted in Brazil and Argentina in order
407 to describe the community of xylem-sap feeders and identify potential vectors of the pathogen. Most
408 xylem-sap feeders trapped in the surveyed crops were sharpshooters, followed by cercopids (Paiva et al.
409 1996; Yamamoto and Gravena 2000; Hickel et al. 2001; Ott et al. 2006; Coelho et al. 2008; Giustolin et
410 al. 2009; Miranda et al. 2009; Ringenberg et al. 2010 and 2014; Schneider et al. 2016). The few cercopid
411 species were grass feeders more commonly found on the ground vegetation. A high diversity of genera
412 and species of sharpshooters was reported in citrus, coffee, grape and plum orchards, but marked
413 variations in species composition was found between ground vegetation and crop canopy, among different
414 crops or for a same crop in different regions. In the major citrus growing region of Brazil (São Paulo
415 State), sampling with suction traps showed that some sharpshooter species are trapped mostly on the citrus
416 canopy, such as Acrogonia citrina Marucci and Cavicchioli, 2002 (Hemiptera: Cicadellidae) (previously
417 identified as A. terminalis), Dilbopterus costalimai Young, 1977 (Hemiptera: Cicadellidae) and O. facialis
418 Signoret, 1854 (Hemiptera: Cicadellidae) (Paiva et al. 1996). Conversely, other sharpshooters e.g.
419 Ferrariana trivittata Signoret, 1854 (Hemiptera: Cicadellidae), Hortensia similis Walker, 1851
420 (Hemiptera: Cicadellidae), Plesiommata corniculata Young, 1977 (Hemiptera: Cicadellidae), and
421 Sonesimia grossa Signoret, 1854 (Hemiptera: Cicadellidae) are much more frequent on the ground
422 vegetation than on the citrus canopy (Paiva et al 1996; Yamamoto and Gravena 2000). In Northeastern
423 Brazil, different sharpshooter species predominate in citrus and grape orchards (Miranda et al. 2009;
424 Ringenberg et al. 2014) compared to Argentina (Dellapé et al. 2016) and southern and southeastern Brazil
425 (Yamamoto and Gravena 2000; Ott et al. 2006; Ringenberg et al. 2010). The reported variations in species
426 composition and prevalence in communities of sharpshooters indicate that surveys for candidate vector
427 species should be done in every region or crop system affected by X. fastidiosa (Lopes and Krugner 2016). 428 Despite the high number of xylem-sap feeders that are potential vectors of X. fastidiosa in South America,
429 few species are considered key vectors of this pathogen in the affected crops (Lopes and Krugner 2016).
430 The relevance of a particular species as a vector depends not only on its competence to transmit the
431 pathogen, but also on ecological and behavioral attributes that will maximize its role in the natural spread
432 of the related diseases (Purcell 1985; Almeida et al. 2005). In transmission assays, 15 species of
433 sharpshooters have been confirmed as vectors of X. fastidiosa in citrus (Roberto et al. 1996; Yamamoto et
434 al. 2002 and 2007; Dellapé et al. 2016; Lopes and Krugner 2016) and four in coffee (Marucci et al. 2008),
435 with transmission efficiencies ranging from 1 to 30%. For CVC, citrus is the main (if not the only) source
436 of inoculum for primary and secondary spread of CVC (Laranjeira et al. 1998). Although some weeds
437 common in the ground vegetation of citrus orchards were found to be infected with X. fastidiosa, there is
438 still no transmission or epidemiological evidences that they serve as important inoculum sources for CVC
439 (Lopes et al. 2003). Therefore, sharpshooter species that predominate on citrus, such as A. citrina, D.
440 costalimai and O. facialis (Coelho et al. 2008; Giustolin et al 2009), are considered key vectors of X.
441 fastidiosa in São Paulo State (Redak et al. 2004; Almeida et al. 2005a). These three species lay eggs and
442 develop as nymphs up to the adult stage on citrus (Almeida and Lopes 1999; Paiva et al. 2001; Milanez
443 et al. 2001), and their immatures are often found on young branches of citrus trees in the state of Sao
444 Paulo (Gravena et al. 1998). In addition, field-collected insects of these species transmitted X. fastidiosa
445 to healthy citrus seedlings, showing their natural infectivity with the bacterium (Lopes and Krugner 2016).
446 Another sharpshooter species, Bucephalogonia xanthophis Berg, 1879 (Hemiptera: Cicadellidae), is
447 particularly important as the most frequent one in young citrus orchards (0-2 years old) (Yamamoto et al.
448 2001), and one of the most efficient vectors of CVC strains of X. fastidiosa in laboratory assays, together
449 with Macugonalia leucomelas Walker, 1851 (Hemiptera: Cicadellidae) (Lopes and Krugner 2016;
450 Esteves et al. in press). Epidemiological studies indicate higher risks of infection of X. fastidiosa during
451 spring and summer, when young citrus flushes and population peaks of sharpshooter vectors are more 452 frequent in the orchards (Roberto and Yamamoto 1998; Laranjeira et al. 2003; Coelho et al. 2008). The
453 landscape composition is another important risk factor, with higher rates of CVC spread in orchards
454 surrounded by older infected groves (Laranjeira et al. 1998), and higher vector species diversity and
455 population on forest edges, where breeding hosts of various sharpshooters species are likely present
456 (Coelho et al. 2008; Giustolin et al. 2009).
457 For other diseases caused by X. fastidiosa in South America, there is little information on vectors and
458 bacterium epidemiology. For CLS and PLS, disease spatial analyses showed a random distribution of
459 infected plants at early stages of epidemics and a switch to aggregated pattern at higher incidences,
460 indicating that secondary spread occurs (Rocha et al. 2010; Ferreira et al. 2016). Interestingly, aggregation
461 occurred mostly within rows, indicating preferential spread to adjacent trees in the same row for both
462 diseases. In the case of PLS, disease started mostly at the borders of the orchards, suggesting entrance of
463 vectors from adjacent vegetation (Ferreira et al. 2016), but the primary sources of inoculum and vector
464 species involved have not yet been determined. Interestingly, some plum genotypes show moderate to
465 high levels of field resistance to PLS (Dalbó et al. 2018). For olive leaf scorch in Brazil, vector species
466 and X. fastidiosa strains associated with the disease are still under investigation, and no epidemiological
467 data are available.
468 469 Taiwan
470 Pierce’s disease of grapevine was first reported in Taiwan in 2002 (Su et al. 2013); this case is considered
471 the first X. fastidiosa outbreak in the Asian continent. Sequences analysis of 16S rRNA and the 16S-23S
472 intergenic transcribed region (ITS) indicates that Taiwanese strains of X. fastidiosa are closely-related to
473 the PD strains isolated in the US (Su et al. 2013). In addition to PD, in 1980s, a X. fastidiosa-elicited
474 disease named pear leaf scorch (PLS) occurred in the areas where pear cv. Hengshan is grown in Taiwan
475 (Leu and Su 1993). The causal agent of PLS has been proposed to be classified as a new species belonging
476 to the genus Xylella, i.e. X. taiwanensis (Su et al. 2016).
477 According to field surveys, no confirmed vectors of PD in the US are present in vineyards and surrounding
478 areas in Taiwan (Su et al. 2011). X. fastidiosa-infected grapevines are often close to X. fastidiosa-infected
479 weeds that suggests PD in Taiwan is transmitted by native vector species (Su et al. 2011).
480 Five xylem feeder species, collected in the surrounding shrubs and weeds near PD occurring vineyards,
481 were found infected with X. fastidiosa, as determined by PCR: Kolla paulula Walker, 1858 (Hemiptera:
482 Cicadellidae), Bothrogonia ferruginea Fabricius, 1787 (Hemiptera: Cicadellidae:), Xyphon sp.,
483 (Hemiptera: Cicadellidae: Cicadellinae), Anatkina horishana Matsumura, 1912 (Hemiptera:
484 Cicadellidae), and Poophilus costalis Walker, 1851 (Hemiptera: Aphrophoridae) (Su et al. 2011; Lin and
485 Chang 2012). Two sharpshooter species, K. paulula and B. ferruginea, were demonstrated to be capable
486 of transmitting X. fastidiosa to grapevine (Lin and Chang 2012, Chang et al. 2014, Tuan et al. 2016). The
487 two sharpshooters showed a bacterial acquisition rate from infected grapevines ranging from 42 to 83%;
488 their inoculation rates, comprised between 6.7 and 28.5%, greatly varies depending on vector species,
489 source plant cultivars, and recipient plant cultivars (Chang et al. 2014; Tuan et al. 2016). Tuan et al. (2016)
490 observed that K. paulula and B. ferruginea transmission efficiency of X. fastidiosa to grapevine is lower
491 than the values reported for G. atropunctata and H. coagulata (Hill and Purcell 1995; Almeida and Purcell 492 2003). No transmission experiments with Xyphon sp. and A. horishana have been carried out. Regarding
493 the froghopper P. costalis, only 1% of the specimens collected during surveys in PD occurring vineyards
494 in Taiwan tested positive for X. fastidiosa by PCR; however, the small size of the transmission experiments
495 conducted so far does not allow to draw conclusions on the role of P. costalis in X. fastidiosa epidemiology
496 (Lin and Chang 2012). Similarly, two specimens of K. paulula collected during surveys in PLS occurring
497 peach orchards in Taiwan tested positive for X. taiwanensis by PCR that suggests it is a potential insect
498 vector for PLS (Shih et al. 2013).
499 K. paulula is a common insect species inhabiting in shrubs and weeds near vineyards in Taiwan. The host
500 plants of K. paulula are Vitis spp., Mikania micrantha, Bidens pilosa var. radiata, Ageratum houstonianum,
501 and Commelina diffusa (Su et al. 2011). The population size of K. paulula is affected by host plants,
502 temperature, rainfall, and typhoon (Shih et al. 2013). Because the generation time of K. paulula is around
503 1.5 months (Tuan et al. 2016), monthly mowing is suggested for the insect vector control at PD high risk
504 areas (Shih et al. 2013).
505
506 507 Conclusions
508 The expansion of the geographic range where X. fastidiosa is present, and its introduction and
509 establishment in Europe, represents both a problem and an opportunity. Looking at the problem, European
510 outbreaks can be considered an emergency capable of leaving an undeletable trace in the history of
511 phytopathology, as it was for potato famine in Ireland, blight of American chestnut in USA, and grapevine
512 phylloxera in France (Almeida, 2016b). Actually, it is impossible to precisely estimate the economic loss
513 associated with pathogen spread; considering olive affected by OQDS in Southern Italy, Sardaro et al.
514 (2015) estimated in 111-119 euros the cost per infected plant, to which about 64 euros/plant should be
515 added when considering the expense associated with the loss of landscape benefits. Moreover, the authors
516 calculated an increase in management costs of about 31% in relation to mandatory control practices
517 imposed by European Commission. Nevertheless, especially considering the case of OQDS in Southern
518 Italy, X. fastidiosa introduction is far beyond any economic consideration; two other aspects should be
519 considered when analyzing its impact. The first is the damage to Salento landscape and to the historical
520 heritage represented by its centenary olive trees. As highlighted by Almeida (2016b), "olive tree is tightly
521 linked to Salento people; it is their heritage, an indivisible part of who they are". The second is the social
522 turmoil in response to compulsory removal of infected olive trees requested by European Commission to
523 halt bacterial spread. Social turmoil triggered a general mistrust of science and scientists working on the
524 epidemic, which attracted foreign press and became an interesting research field for anthropologists
525 (Colella et al. 2016). Looking at the other side of the coin, invasions of new areas where X. fastidiosa
526 could create new biotic associations, represent a unique opportunity for understanding how to ease the
527 threat the bacterium poses to agriculture and landscape. As remarked by Almeida (2016a), research on X.
528 fastidiosa has been discontinuous, and can be divided in three periods, each driven by a unique set of
529 factors. European outbreaks might represent the fourth period, thus an opportunity to increase our
530 knowledge on epidemics driven by the fastidious bacterium. X. fastidiosa transmission efficiency is 531 impacted by various factors: vector species, pathogen genotype, host plant species during acquisition and
532 inoculation, bacterial population within the plant and in different tissues in the same plant, vector host
533 range and within-host tissue preference, disease symptoms, temperature, vector and host plant biology
534 and ecology, seasonality, and crop management practices (reviewed in Sicard et al. 2018). Each bacterium
535 epidemic is characterized by its own, peculiar, combination of such factors. For example, while in PD in
536 Napa Valley X. fastidiosa spread from wild vegetation toward the vineyard is the key feature of bacterial
537 epidemiology, secondary spread where affected crop is the main bacterial source is the characteristic
538 shared by CVC in Brazil and OQDS in Italy. As a consequence, strategies applied to contain PD cannot
539 be effective against CVC and OQDS. Overall, the background on vectors and bacterial epidemiology
540 generated in well-characterized bacterial pathosystems, such as those in the Americas, is an essential
541 source for developing effective disease control strategies. However, X. fastidiosa epidemics in the
542 Americas showed how new bacterial outbreaks should be managed on a case-by-case basis, looking at all
543 the aspects of the multifaceted bacterium-vector-host interaction. Furthermore, vector-X. fastidiosa
544 interaction and the mechanisms leading to bacterium acquisition and inoculation remain the most poorly
545 understood aspects of the entire transmission process (Labroussaa et al. 2017). Almost all the background
546 on such aspects come from studies carried out with sharpshooters, and in the context of PD of grapevine
547 in California. However, research on new epidemics such as those that are being reported in Europe, where
548 the bacterium is transmitted by previously disregarded vector taxa, might fill our knowledge gap and open
549 new perspectives for a sustainable X. fastidiosa control.
550 Eventually, differences and similarities in X. fastidiosa transmission by vectors among geographically
551 distant bacterium outbreaks might shed the light on poorly known aspects of the complex vector-
552 bacterium-host plant interactions. All these data will contribute to deepening our knowledge about
553 diseases mediated by X. fastidiosa, prevent further spread of the fastidious bacterium, and ease its impact
554 on agriculture and landscape. 555 Acknowledgements
556 DC, AM and NB have been financially supported by research grants in the frame of European Union
557 Horizon 2020 research and innovation program under grant agreements no. 727987 XF-ACTORS (Xylella
558 Fastidiosa Active Containment Through a multidisciplinary-Oriented Research Strategy). MM received a
559 research grant in the frame of European Union Horizon 2020 research and innovation program under grant
560 agreements no. 635646 POnTE (Pest Organisms Threatening Europe). JRSL received a research
561 fellowship from National Council for Scientific and Technological Development (CNPq)/Brazil (No.
562 310554/2016-0).
563
564 Author Contribution
565 DC and AF: coordination 566 DC, AM, MM, NB: Europe and North America 567 JRSL: South America 568 TCW: Taiwan 569 DC, AM, MM, NB, TCW, JRSL and AF reviewed and edited the manuscript. 570 AF and JRSL secured funding. 571 All authors read and approved the manuscript. 572
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990 991 Fig. 1 Global distribution of X. fastidiosa. Colored in red the countries where X. fastidiosa has been 992 reported.
993 994 Fig. 2 Outbreaks of X. fastidiosa around Europe. *= natural infectivity determined by molecular 995 methods; **= competent vectors of X. fastidiosa as determined by transmission tests under controlled 996 conditions; ***= epidemiologically relevant vector.
997 998 S.1 Candidate vectors of X. fastidiosa present across the detected bacterial outbreaks: distribution 999 and host plants. Cicadas’ species have been excluded since their vector competence has still to be 1000 determined.
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