Xylella fastidiosa
(Pierce's disease of grapevines)

Pictures

Picture	Title	Caption	Copyright
Title Symptoms on grape vine Caption Pierce's disease in California (USA) showing late season leaf scorching and cane decline from tips. Copyright A.H. Purcell	Symptoms on grape vine	Pierce's disease in California (USA) showing late season leaf scorching and cane decline from tips.	A.H. Purcell
Title Symptoms on oak leaves Caption Oak leaf scald symptoms, Washington D.C. (USA). Copyright Stanley Kostka	Symptoms on oak leaves	Oak leaf scald symptoms, Washington D.C. (USA).	Stanley Kostka
Title Symptoms on oleander leaves Caption Oleander leaf scorch (California USA) may not show distinct marginal necrosis in cool climates. Copyright A.H. Purcell	Symptoms on oleander leaves	Oleander leaf scorch (California USA) may not show distinct marginal necrosis in cool climates.	A.H. Purcell
Title Symptoms on orange leaves Caption Chlorotic lesions on leaves characteristic of variegated chlorosis in sweet orange (Brazil). Copyright A.H. Purcell	Symptoms on orange leaves	Chlorotic lesions on leaves characteristic of variegated chlorosis in sweet orange (Brazil).	A.H. Purcell
Title Symptoms on orange fruits Caption Sweet oranges from trees with advanced variegated chlorosis (outer fruits) are smaller and with harder rinds than normal (centre). Copyright A.H. Purcell	Symptoms on orange fruits	Sweet oranges from trees with advanced variegated chlorosis (outer fruits) are smaller and with harder rinds than normal (centre).	A.H. Purcell
Title Symptoms of Pierce's disease on grape leaves Caption Pierce's disease in 'Pinot noir' grape. Marginal scorching is preceded by concentric reddening and chlorosis. Note bare leaf petioles. Copyright A.H. Purcell	Symptoms of Pierce's disease on grape leaves	Pierce's disease in 'Pinot noir' grape. Marginal scorching is preceded by concentric reddening and chlorosis. Note bare leaf petioles.	A.H. Purcell
Title Disease vector, the blue-green sharpshooter|Graphocephala atropunctata Caption The blue-green sharpshooter (G. atropunctata) is the principal vector for Pierce's disease in coastal California, USA.|The blue-green sharpshooter (Graphocephala atropunctata) is the principal vector for Pierce's disease in coastal California (USA). Copyright A.H. Purcell	Disease vector, the blue-green sharpshooter|Graphocephala atropunctata	The blue-green sharpshooter (G. atropunctata) is the principal vector for Pierce's disease in coastal California, USA.|The blue-green sharpshooter (Graphocephala atropunctata) is the principal vector for Pierce's disease in coastal California (USA).	A.H. Purcell
Title Disease vectors: O. fascialis and H. similis Caption The larger Oncometopia fascialis and smaller Hortensia similis illustrate the diversity of size and coloration of Brazilian sharpshooters. Copyright A.H. Purcell	Disease vectors: O. fascialis and H. similis	The larger Oncometopia fascialis and smaller Hortensia similis illustrate the diversity of size and coloration of Brazilian sharpshooters.	A.H. Purcell
Title Homalodisca coagulata, a disease vector Caption H. coagulata (14mm) is common on citrus in Florida and recently in California (USA). Copyright A.H. Purcell	Homalodisca coagulata, a disease vector	H. coagulata (14mm) is common on citrus in Florida and recently in California (USA).	A.H. Purcell

Identity

Preferred Scientific Name

• Xylella fastidiosa (Wells et al., 1987)

Preferred Common Name

• Pierce's disease of grapevines

International Common Names

• English: alfalfa dwarf; almond leaf scorch; citrus variegated chlorosis; dwarf lucerne; leaf scorch disease; oleander leaf scorch; pear leaf scorch; pecan fungal leaf scorch; pecan leaf scorch; periwinkle wilt; phony disease of peach; plum leaf scald
• Spanish: enfermedad de Pierce (grape); pecosita (citrus, Argentina)
• French: chlorose variégée; des agrumes (citrus); maladie de Pierce (grape); nanisme de lucerne

Local Common Names

• Brazil: amarelinho (citrus); requeima do cafeeiro (coffee)

EPPO code

• XYLEFA (Xylella fastidiosa)

Summary of Invasiveness

Taxonomic Tree

• Domain: Bacteria
•     Phylum: Proteobacteria
•         Class: Gammaproteobacteria
•             Order: Xanthomonadales
•                 Family: Xanthomonadaceae
•                     Genus: Xylella
•                         Species: Xylella fastidiosa

Notes on Taxonomy and Nomenclature

Xylella fastidiosa (Wells et al., 1987) is the xylem-limited bacterium causing Pierce's disease of grapevine and other plant diseases. Different strains of the same species cultured from different hosts by the same techniques cause disease in other plant hosts. Two such diseases are phony disease of peach and plum leaf scald, which were previously listed and described separately by EPPO (1986). Another strain causes citrus variegated chlorosis in South America. Relationships between strains are still in the process of being categorized. Most attempts to characterize strains have used molecular methods (Chen et al., 1995; Hendson et al., 2001; Schuenzel et al., 2005) rather than plant host range studies, which are limited by quarantine restrictions and the unusually large range of plants that many strains of X. fastidiosa can infect.

X. fastidiosa taxonomy has recently been revisited in view of available genetic diversity data based on a multi-locus sequence typing approach (Yuan et al., 2010). X. fastidiosa can be divided into four generally accepted subspecies which have evolved in distinct geographical regions with each subspecies showing a high degree of host specificity (Almeida and Nunney, 2015). X. fastidiosa subsp. fastidiosa, thought to be native to southern Central America (Nunney et al., 2010), is associated primarily with Pierce’s disease of grapevines and almond leaf scorch. X. fastidiosa subsp. multiplex, thought native to temperate and subtropical North America, is associated with scorch disease in a wide range of trees, including phony peach disease and plum leaf scorch. X. fastidiosa subsp. pauca, thought to be native to South America, is associated with strains causing disease in citrus and coffee (Nunney et al., 2012). X. fastidiosa subsp. sandyi, believed to originate from the southern region of the USA (Yuan et al., 2010), is associated with oleander leaf scorch.

A fifth subspecies X. fastidiosa subsp. tashke was proposed to include isolates associated with leaf scorch in Chitalpa tashkentensis, an ornamental landscaping tree (Randall et al., 2009). However, the phylogenetic placement of this strain is still in doubt and the subspecies is not generally accepted.

A further subspecies, X. fastidiosa subsp. morus, was proposed for a strain associated with mulberry leaf scorch (occurring in the eastern USA and California). Multi-locus sequence typing places this strain in a group distinct from the four currently described subspecies (Nunney et al., 2014).

An isolate associated with pear leaf scorch in Taiwan was classified as a new genotype of X. fastidiosa based on 16S rDNA sequencing (Leu and Su, 1993; Su et al., 2012, 2014). However, multi-locus sequence typing suggests this strain is substantially distinct from all other known genotypes. Almeida and Nunney (2015) suggest that this strain would be better assigned to a new species.

Complete genome sequences are available for citrus (Simpson et al., 2000), grape (Van Sluys et al., 2003), almond and oleander (Bhattacharyya et al., 2002; Van Sluys et al., 2002) strains. Host range and cross-inoculation studies are still needed to determine host-specialized forms (pathovars) within X. fastidiosa (Purcell and Hopkins, 1996). For example, Brazilian citrus and coffee strains were shown to cause disease in grape (Li et al., 2002), although grape disease caused by X. fastidiosa in Brazil has not been observed. The grapevine-virulent strains do not infect peach, whereas the strains virulent in peach do not cause disease in grapevine (Hopkins, 1988). The information here refers principally to the fairly well characterized grapevine, almond, citrus and coffee strains. It only very briefly attempts to cover the diseases caused by X. fastidiosa sensu lato on other hosts.

Description

X. fastidiosa is a fastidious Gram-negative, xylem-limited bacterium, rod-shaped with rippled cell walls. It is strictly aerobic (microaerophilic), non-flagellate, does not form spores and measures 0.1-0.5 x 1-5 µm. The peach strain was given by Nyland et al. (1973) as 0.35 x 2.3 µm. See also Bradbury (1991). Thread-like strands (fimbriae) attached to the polar ends of bacterial cells can be observed in electron microscopy (Mircetich et al., 1976) and scanning electron microscopy (Feil et al., 2003b). These probably function in bacterial attachment and 'twitching' movement (Meng et al., 2005).

Distribution

The distribution given is for the grapevine, peach, coffee and citrus pathogens. Apparently some strains of X. fastidiosa sensu lato (oak strains) occur farther north in North America (Hartman et al., 1996; Goodwin and Zhang, 1997).

Grapevines with symptoms of Pierce's disease in Kosovo, former Yugoslavia, were confirmed as harbouring grape-virulent stains of X. fastidiosa (Berisha et al., 1996). These were tolerant grape varieties capable of harbouring populations of X. fastidiosa with mild symptoms. This record is considered dubious and to date there are no reports of natural spread of Pierce's disease to other vines.

An isolated record from almonds in India (Jindal and Sharma, 1987) is based on a test described in the 1970s; it requires confirmation by more modern methods. In Taiwan pear leaf scorch is caused by a strain of X. fastidiosa (Leu et al., 1993, 1998). Multi-locus sequence typing suggests that this strain is genetically dissimilar to described X. fastidiosa genotypes and would be assigned a new subspecies or even a new species (Almeida and Nunney, 2015).

Güldr et al. (2005) suggested the occurrence of almond leaf scorch in Turkey, however this has not been confirmed by any other studies or surveys. According to the NPPO of Turkey (2014), this record should be considered as invalid.

The citrus disease has been reported from Argentina (Brlansky et al., 1991) and spread within Brazil, from Sao Paulo and Minas Gerais, as first reported in 1987, to north-eastern Brazil by 1996 (Laranjeira et al., 1996). The grapevine disease has been reported from Venezuela (Jimenez, 1985; Hernandez and Ochoa, 1994).

Pierce's disease has been confirmed in all states along the Gulf of Mexico from Florida to Texas; New Mexico, Arizona and California; northern Mexico and Costa Rica, but probably throughout Central America; Venezuela.

Phony peach has been confirmed in south-eastern USA from Florida north to North Carolina and west as far as Missouri and eastern Texas. Records for Montana (CABI/EPPO, 2006) and Nebraska (Sherald, 1993b) require further confirmation.

Plum leaf scorch is reported in Paraguay, Argentina, southern Brazil (Leite et al., 1997); and in the USA along the Gulf coast (Raju et al., 1982).

Coffee leaf scorch is widespread in Brazil (de Lima et al., 1996, 1998).

Tree leaf scorches are reported in the USA from Florida to New York and the Ontario Peninsula of Canada (rare, unconfirmed) and eastward to the central midwest (Kentucky, Kansas, Nebraska) and south-west as far as Texas.

See also CABI/EPPO (1998, No. 290).

Distribution Table

The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

History of Introduction and Spread

Phony disease of peach spread within the south-eastern USA from the 1890s until about 1930 (Turner and Pollard, 1959), and the spread of citrus variegated chlorosis disease of orange throughout Brazil in the 1990s (Laranjeira, 1997) was documented. The origins of these strains are unknown but are likely to be endemic to unknown regions of the Americas.

In 2013 X. fastidiosa was recorded in Europe, causing serious damage to olive groves in Puglia, Italy. It was also detected in numerous other host plants (mainly ornamentals). In 2015, the bacterium was reported on ornamental plants on the island of Corsica. The subspecies of X. fastidiosa which occurred in France (subsp. multiplex) was different to that which occurs in Italy (clustered in a clade closest to subsp. pauca (Elbeaino et al., 2014a)).

Characteristic symptoms of Pierce's disease of grapevine were observed in Taiwan in 2002. X. fastidiosa subsp. fastidiosa was subsequently identified, confirming the first report of Pierce's disease in Asia (Su et al., 2013). 

Risk of Introduction

The greatest threats are to mild winter regions with one or more of the following crops: grapevines, citrus, almond, stone fruits (Prunus spp.), coffee, oleander, lucerne or where the tree species that can be potentially affected by leaf scorch diseases occur.

EPPO considers X. fastidiosa as an A1 quarantine pest (EPPO, 1989) and it is also a quarantine pest for COSAVE. In the EPPO region, it is clear that the grapevine strain of X. fastidiosa has the potential to kill large numbers of grapevines and to make areas unfit for growing Vitis vinifera. Its vectors in North America do not occur in the EPPO region, but vector capacity is so non-specific that one could certainly expect European Cicadellinae (e.g., Cicadella viridis) or Cercopidae to transmit the bacterium if introduced. After the recent introduction and spread of the vector Homalodisca vitripennis in California, USA, this leafhopper has become extremely abundant on citrus and other crops in southern California (Sorensen and Gill, 1996). This illustrates that this exotic vector species can become abundant in Mediterranean climates, despite originating in a humid subtropical region (south-eastern USA). The main danger in the long term in Europe is that X. fastidiosa could become established in natural vegetation which would then act as a reservoir for infection of vineyards or other susceptible crops or forest trees. It is less likely that Pierce’s disease would become a problem in the production of planting material, for it is easily detected, can be prophylactically eliminated by hot-water treatment, and is rapidly self-eliminating if introduced into fields. Nevertheless, infected planting material could introduce the disease to new areas. Hoddle (2004) modelled the distribution of X. fastidiosa in California and projected the model to predict world distribution. Cold winter temperatures were seen as the limiting factor for X. fastidiosa establishment and X. fastidiosa is only likely to establish as a serious problem in the warmer parts of the EPPO region, which have winter temperatures approaching those of the southern USA. Species distribution models employed by Bosso et al. (2016a) suggest that X. fastidiosa in Italy has the potential to spread beyond the current boundaries of distribution and affect wide areas of Italy outside of Apulia. Mediterranean climates are particularly favourable for X. fastidiosa establishment and X. fastidiosa may establish within Portugal, Spain, Corsica, Albania, Montenegro, Greece and Turkey as well as all countries of northern Africa and the Middle East (Bosso et al., 2016b). The persistence of X. fastidiosa in the cooler climate of Kosovo, former Yugoslavia, over several years suggests Pierce's disease could also become established in coastal parts of southern France, and northern Italy. Information on the incidence and severity of the disease in the former Yugoslavia was not available as of early 1998. The potential natural range and severity of Pierce’s disease in Europe may depend on the distribution and biology of potential vectors and is accordingly rather difficult to assess.

The South American strain on citrus also presents a major risk, for the climatic conditions of Mediterranean countries seem favourable to its development. The reported damage in Brazil suggests potential damage even greater than for the grapevine disease. No critical evaluation of possible European vectors has yet been made, but the arguments developed above for grapevine should certainly also apply to citrus.

The peach strain is relatively less important, but X. fastidiosa still presents a definite danger for peaches, plums, almonds, oaks and, sensu lato, for other fruit and amenity trees (see Hosts) (Dunez, 1981).

Habitat

X. fastidiosa occupies habitats of insect vectors where suitable host plants occur. For citrus, habitats are chiefly commercial orchards. For Pierce's disease strains, habitats may be riparian vegetation, irrigated pastures, hay fields, or ornamental landscapes.

Hosts/Species Affected

No grapevine (Vitis spp.) species are known to be immune to Pierce’s disease strains of X. fastidiosa, but American species used as rootstocks (V. aestivalis, V. berlandieri, V. candicans, V. rupestris) and hybrids derived from them are tolerant and some may be resistant, as is V. rotundifolia (Goheen and Hopkins, 1988). Almonds and lucerne can be hosts of the grapevine strains, but the diseases caused by X. fastidiosa in these three crop species are independent within California, USA, suggesting as yet unidentified biological differences (Purcell, 1980b). A very high percentage (>75% of those tested) of crop, wild plant and weed species can carry Pierce’s disease strains of the bacterium without symptoms (e.g. wild grasses, sedges, lilies, various bushes and trees) (Raju et al., 1983; Hopkins and Adlerz, 1988; Hill and Purcell, 1995b). It is likely that in most symptomless host species, X. fastidiosa multiplies to lower populations and moves systemically less often than in pathological hosts. For example, blackberry (Rubus spp.) can be a systemic host, but the bacterium multiplies in mugwort (Artemisia douglasiana) without systemic movement (Hill and Purcell, 1995b). Hosts can be classified as propagative or non-propagative, systemic or non-systemic, and symptomatic or non-symptomatic (Purcell and Saunders, 1999b). Propagative, systemic hosts are the best hosts for efficient vector acquisition of bacteria, but vectors can acquire the bacterium from non-systemic hosts. Acquisition efficiency is proportional to the populations of live bacterial cells within plant tissues (Hill and Purcell, 1997).

Peach (Prunus persica) strains of X. fastidiosa cause peach phony disease (Wells et al., 1983), which also attacks Prunus salicina (causing leaf scald). All cultivars, forms and hybrids of peach are attacked, whether on their own roots or other rootstocks. Plums (Prunus domestica), almonds (P. dulcis), apricots (P. armeniaca) and the wild P. angustifolia were reported susceptible to phony disease before the association with X. fastidiosa was established. This reported range partly overlaps that of the grapevine-infecting strains. Various perennial weeds of orchards, such as Sorghum halepense, may act as reservoirs for the peach-infecting strain (Yonce, 1983; Yonce and Chang, 1987), but the plant host range of Prunus strains from the south-eastern USA has not been investigated extensively. Pierce's disease strains also cause almond leaf scorch disease (Davis et al., 1980), but the almond strains infect grape in low populations and without causing disease (Almeida and Purcell, 2003).

X. fastidiosa in the wide sense also causes leaf scorch in Acer rubrum (Sherald et al., 1987), Morus rubra (Kostka et al., 1986), Platanus occidentalis (Sherald, 1993a,b) (wilt and leaf scorch), Quercus rubra (Chang and Walker, 1988), Ulmus americana and Vinca minor (stunt). Strains from Ulmus and from P. occidentalis are not reciprocally infectious (Sherald, 1993a). The bacteria involved are not known to be transmissible to grapevine. Diseases of numerous woody ornamental plants in southern California, USA, including olive, date palm and rosemary, have been associated with X. fastidiosa but a causal relationship is still unproven (Wong and Cooksey, 2004). Until their relationships and pest significance have been clarified, they can all be regarded as potentially dangerous for Europe and the Mediterranean region.

X. fastidiosa causes citrus variegated chlorosis in Brazil (Lee et al., 1991; Chang et al., 1993; Hartung et al., 1994) and Argentina (Brlanksy et al., 1993). The disease affects mostly sweet oranges (Citrus sinensis); it has been observed especially on cultivars Pera, Hamlin, Natal and Valencia. It occurs on trees propagated on all commonly used rootstocks in Brazil: C. limonia, C. reshni and C. volkameriana. The disease has not been observed on C. latifolia or mandarins (C. reticulata), even when the trees were planted in severely affected orange groves (Li et al., 2000). The effectiveness of removing diseased citrus trees to prevent further spread of variegated chlorosis in citrus (Rodas, 1994) strongly suggests that most spread of this disease is from tree to tree within the crop. Control measures require the production of disease-free nursery trees in protected environments.

Citrus blight in Florida, USA, has been associated with X. fastidiosa (Adlerz et al., 1989; Hopkins et al., 1996); however the preponderance of evidence suggests that it is not the cause of blight (Derrick and Timmer, 2000).

Plum leaf scald is an important crop-limiting disease caused by X. fastidiosa from Brazil through Argentina. The South American plum leaf scald strains appear to differ from those in North America, as there are no reports of phony disease of peach in South America. The plum leaf scald strains in Brazil may have wide plant host ranges (Leite et al., 1997). A leaf scorching disease of coffee (De Lima et al., 1998) is caused by strains of X. fastidiosa that appear to be closely related to the citrus variegated chlorosis strains (Rosato et al., 1998), but its ability to cause disease in citrus (Li et al., 2001) is controversial.

In Europe and the Mediterranean region, grapevine and citrus are clearly the most significant potential crop hosts, although peach and plum are also important. Strains that cause leaf scorch diseases in oak, elm, sycamore (plane) (Hearon et al., 1980), mulberry (Kostka et al., 1986) and other tree species are also potentially damaging. Many other hosts could carry the bacterium, without necessarily being significantly affected.

X. fastidiosa has been implicated as the causal agent of olive quick decline syndrome in Europe. In 2013, X. fastidiosa subsp. pauca was associated with quick decline syndrome on olive, almond and oleander in Europe (southern Italy, Apulia region) (European Food Safety Authority, 2015). Symptomatic olive trees were often affected by multiple pests, including X. fastidiosa, several fungal species, and Zeuzera pyrina (leopard moth) (Nigro et al., 2013). Recent experimental evidence (Saponari et al., 2016) has confirmed X. fastidiosa as the causal agent of olive quick decline syndrome in Italy (European Food Safety Authority, 2016). In the USA a study evaluating olive as a host for X. fastidiosa concluded that subsp. multiplex was present but was not the cause of the leaf scorch and dieback symptoms observed on olive trees in California (Krugner et al., 2014). However, X. fastidiosa subsp. pauca has been implicated as a causal agent of olive plant dieback and leaf desiccation in Argentina (Haelterman et al., 2015). More recently, leaf scorch symptoms on olive trees in Brazil have been associated with X. fastidiosa subsp. pauca (Coletta-Filho et al., 2016).

The host range of X. fastidiosa based on the available peer-reviewed literature is presented in European Food Safety Authority (2015).
According to the European Food Safety Authority (2016), the current list of host plant species for X. fastidiosa consists of 359 plant species (including hybrids) from 204 genera and 75 different botanical families.

Host Plants and Other Plants Affected

Growth Stages

Symptoms

On grapevines

The most characteristic symptom of primary infection is leaf scorch. An early sign is sudden drying of part of a green leaf, which then turns brown while adjacent tissues turn yellow or red. The desiccation spreads and the whole leaf may shrivel and drop, leaving only the petiole attached. Diseased stems often mature irregularly, with patches of brown and green tissue. In later years, infected plants develop late and produce stunted chlorotic shoots. Chronically infected plants may have small, distorted leaves with interveinal chlorosis and shoots with shortened internodes. Highly susceptible cultivars rarely survive more than 2-3 years, despite any signs of recovery early in the second growing season. Young vines succumb more quickly than do older vines. More tolerant cultivars may survive chronic infection for more than 5 years (Hewitt et al., 1942; Goodwin and Purcell, 1992).

On peaches

Young shoots are stunted and bear greener, denser foliage (due to shorter internodes) than healthy trees. Lateral branches grow horizontally or droop, so that the tree seems uniform, compact and rounded. Leaves and flowers appear early, and leaves remain on the tree longer than on healthy trees. Affected trees yield increasingly fewer and smaller fruits until, after 3-5 years, they become economically worthless (Hutchins, 1933).

On citrus

Trees can start showing the symptoms of variegated chlorosis from nursery size up to more than 10 years of age. Younger trees (1-3 years) become systemically colonized by X. fastidiosa much faster than do older trees. Trees more than 8-10 years old are not usually totally affected, but rather have symptoms on the extremities of branches. Affected trees show foliar chlorosis resembling zinc deficiency with interveinal chlorosis. The chlorosis appears on young leaves as they mature and may also occur on older leaves. Newly affected trees show sectoring of symptoms, whereas trees which have been affected for a period of time show the variegated chlorosis throughout the canopy. As the leaves mature, small, light-brown, slightly raised gummy lesions (becoming dark-brown or even necrotic) appear on the underside, directly opposite the yellow chlorotic areas on the upper side.

Fruit size is greatly reduced; it may take 550 affected fruits to fill a field box, compared with 250 normal fruits. The sugar content of affected fruit is higher than in non-affected fruit, and the fruit has a hard rind, causing damage to juicing machines. Blossom and fruit set occur at the same time on healthy and affected trees, but normal fruit thinning does not occur on affected trees and the fruits remain small but open earlier. Since more fruits remain, total production is not greatly reduced. On affected trees of cv. Pera and other orange cultivars, fruits often occur in clusters of 4-10, resembling grape clusters. Affected trees show stunting and slow growth rate; twigs and branches die back and the canopy thins, but affected trees do not die (Chang et al., 1993a,b; Lee et al., 1991, 1993).

Control has been achieved by removing inoculum in established orange groves and using sanitary measures to prevent infection of nurseries and new groves. All symptomatic branches from trees older than 3 years are cut off up to 1 m below the most basal symptoms. Symptomatic trees less than 4 years old are removed. To prevent the infection of nursery trees, nurseries are located away from citrus plantings, sharpshooters are controlled prophylactically by insecticides, and buds are taken from trees tested free of X. fastidiosa and grown vectors in screen houses or glass houses to exclude vectors. The effectiveness of these measures (Rodas, 1994) indicates that most spread of variegated chlorosis is from tree to tree within citrus orchards (Laranjeira, 1997).

On olives

On olives, quick decline syndrome is characterised by the development of leaf scorch symptoms and desiccation of small twigs and branches. Symptoms generally initiate in the upper part of the canopy on one or two branches, and then extend to the remainder of the crown. Severely affected plants are often pruned heavily, favouring spindly new growth which also succumbs to scorch symptoms. The tree may send out suckers from the base of the plant which subsequently die back, until the root system dies entirely (Martelli, 2016a). Grafting experiments have demonstrated that it takes at least 7 months for leaf scorch symptoms to appear on the grafted plant part (European Food Safety Authority, 2015).

Symptoms are found on all known varieties of olive. Older varieties, such as Ogliarola Salentina, Cellina di Nardò and common varieties Frantoio and Coratina, appear susceptible. It is suggested that the variety Leccino seems less susceptible, although records are based on field observations and are yet to be experimentally confirmed. Apparent variation in olive varietal susceptibility may be the result of differences in disease vector pressures in the areas where the disease is present (European Food Safety Authority, 2015).

Vectors

Vector feeding causes no visible damage. Xylem feeders are prodigious feeders, consuming hundreds of times their body volumes per day in xylem sap. Most non-xylem-feeding leafhoppers produce a sugary or particulate excrement, but that of xylem feeders is watery, drying to a fine whitish powder (brochosomes) where abundant (Rakitov, 2004). The excrement of froghopper nymphs takes the form of persistent bubbles or 'froth'; that surrounds the body of the insect, presumably to provide protection from natural enemies.

List of Symptoms/Signs

Biology and Ecology

X. fastidiosa proliferates only in xylem vessels, in roots, stems and leaves. The vessels are ultimately blocked by bacterial aggregates and by tyloses and gums formed by the plant, although disease induction may not be due simply to water blockage (Goodwin et al., 1988). Pierce's disease strains of the bacterium are efficiently acquired by vector insects, with no latent period, and persist in infective adult insects indefinitely (Severin, 1949). In tests made during the 1940s in California, USA, 75 of 100 tested plant species proved to be hosts from which vectors could acquire the pathogen by feeding (Freitag, 1951). Additional studies with culturing and targeted gene amplification (PCR) of X. fastidiosa revealed additional symptomless hosts (Purcell and Saunders, 1999b; Costa et al., 2004; Wistrom and Purcell, 2005). Most of these hosts have only very mild (slight stunting) or no symptoms when infected.

Winter climate is a key factor in delimiting the areas where X. fastidiosa can persist from one season to the next. Pierce's disease and phony disease only occur in areas with a mild winter, presumably in relation to survival of the bacterium in dormant plants (Purcell, 1980a). Experimental cold therapy of diseased grapevines suggests that freezing temperatures can eliminate the bacterium directly from plants (Purcell, 1980a). Wet winters promote survival of high vector populations and favour disease spread in regions with dry summers. In temperate climates with regular freezing winter temperatures, infections of X. fastidiosa established in grapevines during the early growing season are most likely to persist until the following year (Purcell, 1981; Feil et al., 2003a). In California, USA, there is no evidence of vine to vine spread of chronic infections, probably because when bacteria first appear in new foliage (Smart et al. 1998), the chances of establishing infections that will survive the subsequent winter are small. For this reason, vectors that survive the winter may be especially important in establishing early season infections. The lack of potential vectors that overwinter as adults and thus can introduce new infections into woody plants may explain the absence of natural spread or establishment in temperate climate regions such as Europe.

X. fastidiosa is reported to be transmitted to seedlings from infected fresh seed in citrus (Li et al., 2003). This should be taken into account when importing citrus seed for propagation but is not likely to present a risk for introducing the bacterium via commercial fruit. The bacterium is sensitive to dry conditions commonly found in most seeds, but tests of seed transmission have only been reported for citrus. It tends to multiply rapidly in infected grapevines. Infected vines are conspicuous the year after infection and are easily destroyed or die within one to several years, depending on vine cultivar and age. Newly planted vines that are infected by grafting die within a year. In non-systemic hosts such as willow, X. fastidiosa dies within weeks of infecting a xylem cell via vector inoculation (Purcell and Saunders, 1999). Bacterial populations are maintained in natural vegetation by vector transmission to and latent multiplication in wild plants.

On citrus, the variegated chlorosis disease appears to spread from tree to tree within citrus groves (Laranjeira, 1997; Laranjeira et al., 1998). The 9-12 months incubation before symptoms appear in orange trees facilitates the spread of infected nursery trees and probably explains the rapid movements of the disease across Brazil within a decade (Coletta-Filho et al., 2000). Regulations in Brazil now require that nursery trees are produced under screens to prevent infection. The vectors of citrus strains appear to have the same vector group specificity (suctorial xylem feeders) as grapevine strains, but transmission trials indicate that vector transmission is much less efficient in citrus compared with grape (Lopes et al., 1996; Roberto et al., 1996; Yamamoto et al., 2002).

Vectors

Virtually all sucking insects that feed predominantly on xylem fluid are potential vectors (Purcell, 1989). Leafhoppers (Cicadellidae) in the subfamily Cicadellinae (sharpshooters) and spittle bugs or froghoppers (Cercopidae) are by far the most common species of known vectors within the natural range of X. fastidiosa in North America. As previously predicted, cicadas (Cicadidae) are vectors as well (Paião et al., 2002). Cicadella viridis (Cicadellinae) and the meadow spittle bug, Philaenus spumarius (Cercopidae), are common and widespread in central and southern Europe (Pavan and Gambon, 2003) and reported to occur on grape (Hering, 1966). In California, USA, all tested members of the subfamily Cicadellinae (including Carneocephala fulgida, Draeculacephala minerva and Graphocephala atropunctata) were vectors of the grapevine strain (Hewitt et al., 1949). Homalodisca vitripennis, H. insolita, Oncometopia orbona, Graphocephala versuta and Cuerna costalis are reported vectors of the peach strain (Turner and Pollard, 1959; Yonce, 1983). All these are xylem-feeding, suctorial insects which acquire the bacterium rapidly when feeding (less than 2 h). The bacterium adheres to the mouthparts and is released directly from them when the insect feeds again (Purcell et al., 1979). It multiplies in the vector but does not circulate in its haemolymph, nor does it require a latent period before transmission (unlike a phytoplasma). Very few live cells in the vector's head are needed for efficient transmission (Hill and Purcell 1995a). Transmission is usually from wild, generally symptomless, hosts to cultivated hosts (grapevines, peaches) rather than between cultivated hosts, though the latter can occur. Feeding preferences of G. atropunctata for different grapevine cultivars have been noted, but these seem to not have a role in field susceptibility (Purcell, 1981). A study of X. fastidiosa vectors on olive trees in Italy suggests that potential vectors may include the phloem-feeder Euscelis lineolatus (Elbeaino et al., 2014b). Further studies are needed to confirm transmission.

The biology of the vectors is important in understanding the epidemiology of the disease. In California, USA, species such as D. minerva and C. fulgida inhabit permanent pastures alongside vineyards, or live on weeds within them. Irrigation and weed control practices which produce foci of preferred host plants, including Cynodon dactylon and Echinochloa crus-galli, increase vector populations and the spread of the bacterium (Purcell and Frazier, 1985). Other species, such as G. atropunctata, multiply on grapevine but overwinter on a variety of other wild hosts, chiefly in riparian vegetation.

Means of Movement and Dispersal

X. fastidiosa is dispersed by its vectors on a local scale. Vectors could also be carried internationally on plants, or fruits, of grapevine, peach or other plants. Tests of grape fruit clusters as an acquisition source for feeding vectors resulted in no transmission by an efficient vector (Purcell and Saunders 1995). Vector eggs are inserted into plant tissues, making visual detection difficult. The bacterium is not passed through the eggs of the vectors. Immature vectors (nymphs) do not retain infectivity after moulting but can rapidly reacquire the bacterium by feeding on infected plants. The bacterium could be spread in planting material, but this has not been considered a major risk for grapevine in North America, where such material does not survive long enough to present a hazard (Goheen and Hopkins, 1988). Hot-water treatments (50°C for 20 min, 45°C for 180 minutes) eliminate viable bacteria from dormant cuttings (Goheen et al., 1973). X. fastidiosa has presumably reached the limit of its natural distribution in America, so that infected planting material presents a relatively minor risk of introduction and establishment. The situation in the EPPO region is quite different, because large areas of susceptible grapevines are at risk, and the bacterium could readily be introduced on grapevine planting material or in a wide range of species of symptomless plant hosts from which vector spread may be possible. Rooted cuttings from grapevines with Pierce’s disease can appear viable and healthy for 3 months, and yet test positive for X. fastidiosa (Montague et al., 2016). Vines infected with X. fastidiosa therefore have the ability to produce asexually propagated cuttings, and potentially contaminate non-infected vineyards. Of greatest importance in preventing the establishment of X. fastidiosa diseases in Europe is to prevent the introduction and establishment of a vector that overwinters as an adult, thus being able to carry the pathogen through the winter and establish infections during spring. A prime candidate is the leafhopper Homalodisca vitripennis, which rapidly invaded California, USA, and shortly thereafter became abundant in French Polynesia and Hawaii. This sharpshooter has an extremely wide host range, and climate-matching models predict it could become established in southern Europe and in subtropical and tropical Africa and Asia (Hoddle, 2004).

Vector transmission

Introduction of new vectors can radically change the epidemiology of diseases caused by X. fastidiosa, as demonstrated in southern California in the late 1990s (Blua et al., 1999; Purcell and Saunders, 1999a). Vector abundance, host plant preferences, and other behaviour (flight, transmission efficiency) are key components of the rate of spread of X. fastidiosa.

European Food Safety Authority (2015) provides a list of the known the vectors of X. fastidiosa in the Americas, and potential vectors of the bacterium in Europe. Only one vector species, Philaenus spumarius, has been proved to be able to transmit the strain of X. fastidiosa involved in the outbreak in Apulia, Italy (Saponari et al., 2014). This species is the only confirmed vector identified so far in Europe.

Agricultural practices

Planting of X. fastidiosa-free trees in new citrus groves is a key control component of citrus variegated chlorosis in Brazil. Movement of vegetative propagative materials may introduce the bacterium over long distances.

Pathway Vectors

Plant Trade

Wood Packaging

Vectors and Intermediate Hosts

Impact

X. fastidiosa precludes a profitable commercial production of susceptible bunch grapes (Vitis vinifera) in most of the south-eastern USA, where the pathogen is endemic in natural vegetation, vectors abound, a mild winter climate allows good bacterial survival, and temperatures during the spring and summer support rapid bacterial growth. It causes severe localized losses in California and western Texas, USA, and Mexico. Peach and plum crops in the coastal plain of the Gulf of Mexico and the southern Atlantic states (Florida, Georgia, South Carolina, Alabama, Mississippi, Louisiana) in the USA are severely affected by phony disease.

Losses to X. fastidiosa caused by tree leaf scorches in a growing number of tree species (oaks, mulberry, maple, sweet gum, sycamore (plane), elm) do not ordinarily include direct mortality and have not been calculated, but are probably substantial. Sycamore leaf scorch has destroyed young plantations for sycamore pulp wood (Leininger et al., 2001). During the 1990s, a strain of X. fastidiosa that causes a lethal disease of oleander in California (Hendson et al., 2001), and the rapid dissemination of citrus strains in Brazil illustrated the rapidity with which new strains can spread.

Citrus variegated chlorosis causes major losses in Brazil and the Missiones district of Argentina. According the Fundecitrus sampling (http://www.fundecitrus.com.br/english/est_cvc_us.html#inc_cvc), three major citrus regions had 44-63% of commercial trees with fruit symptoms in 2005. It will probably ultimately affect citrus production in all South American citrus east of the Andes. Plum leaf scorch causes the loss of entire orchards in Brazil and Paraguay within several years after the disease first appears in orchards.

Coffee leaf scorch has caused uncalculated losses, especially in some newer coffee cultivars. It has the potential to become a major new problem in regions with high populations of xylem sap-feeders, all of which are likely to be vectors.

In the USA, within the main areas where X. fastidiosa occurs naturally (coastal plains of the Gulf of Mexico), Vitis vinifera and V. labrusca cannot be cultivated because they are rapidly infected due to high rates of natural spread. As a consequence, only selections of V. rotundifolia (muscadine) and specially bred resistant hybrids can be cultivated. The same situation exists throughout tropical America. In California, however, X. fastidiosa occurs only in 'hot spots'. V. vinifera has to be cultivated outside these hot spots. There have been considerable losses in the past, before this situation was clarified. Vector habitats can be eliminated as a preventative measure, but this is not possible in all situations. Insecticide treatment against its vectors has been only partially successful (Purcell, 1979). Antibiotic treatment of grapevines against X. fastidiosa is not effective enough for commercial use and has unfavourable health and environmental characteristics. The recent establishment in California of an invasive species, Homalodisca vitripennis, dramatically increased the risks of Pierce's disease losses (Blua et al., 1999; Purcell and Saunders, 1999a).

Pierce's disease is thus a major constraint on grapevine production in the USA and tropical AmericaIt does not occur in all grapevine-producing areas of the USA largely because of climatic constraints. However, the incidence of the disease can dramatically increase with the introduction of new vectors, as illustrated in California with H. vitripennis.

By contrast, phony disease of peach does not kill trees or cause dieback, but it does significantly reduce the size and number of fruits. An analysis of biophysical effects on peach trees (Anderson and French,1987) found the disease was extremely important in the south-eastern USA in the 1940s, when about half of the trees in 5-year-old orchards were often found to be affected and older orchards entirely so. However, the efficient control methods now available (insecticides, destruction of infected trees, elimination of wild host plants around orchards) allow better control, except in areas where incidence is very high.

The impact of X. fastidiosa and olive quick decline syndrome in Italy is yet to be fully determined. However, it is estimated that the infection (as of October 2015) covers about 10,000 ha of arable land, accounting for about one million infected trees. Olive/oil production is a primary asset to the Apulia region of Italy (Martelli et al., 2016). 

Environmental Impact

No ecological changes have been documented. Pierce's disease may limit the distribution of grape species in eastern North America, as all native grape species in the south-eastern USA are tolerant of X. fastidiosa, and the endemic grape species in north-eastern North America are susceptible. Sycamore (Platanus) populations in the southern USA are more tolerant or resistant than are more northerly sycamore populations. These trends may occur in other, as yet, unstudied forest species.

The European Food Safety Authority identified two separate categories of environmental consequences: the direct and indirect impact on the host plants themselves, and the indirect impact caused by the control methods implemented against the disease, in particular insecticide treatments. 

Impact: Biodiversity

No quantitatively documented impacts on biodiversity have been reported, but diseases of forest trees (oak, sycamore, maple, liquidamber) in eastern North America may affect forest biodiversity (including faunal diversity) where these diseases are most severe. The intensive use of insecticide treatments implemented to limit disease transmission and control the insect vector is likely to have numerous far reaching consequences for the environment, for example through modification of food webs (European Food Safety Authority, 2015).

Threatened Species

Social Impact

Pierce's disease precludes the commercial culture of bunch grapes (Vitis vinifera) in the south-eastern USA and limits profitable commercial peach culture near the Gulf of Mexico and south Atlantic coast. There may be similar but still unevaluated impacts on other crops such as lucerne and plum. Citrus variegated chlorosis disease is not present in over a third of the main orange crop in Brazil, causing losses in the world's largest crop of sweet orange (Fundecitrus, 2006). The intensive use of insecticide treatments implemented to limit disease transmission and control the insect vector is likely to have numerous far reaching consequences for the environment, for example, through modification of food webs (European Food Safety Authority, 2015).

Risk and Impact Factors

• Pathogenic

Diagnosis

The most sensitive and reliable detection method is polymerase chain reaction (Minsavage et al., 1994). Positive results have been obtained with lucerne, peach, oak, citrus, oleander, plum and numerous grape and almond strains with the Minsavage et al. primer. ELISA is less sensitive and problems have arisen with false positives. Culturing on PW medium (Davis et al., 1983) provides definitive proof of living bacteria in a plant, estimates of populations of viable bacteria (Hill and Purcell, 1995a), and facilitates later strain identification.

Work by Pooler et al. (1997) allows a much larger sized sample of plant tissue to be processed for PCR and avoids plant inhibitors, which are probably the biggest obstacle to using PCR to detect X. fastidiosa in plant materials, in addition to the irregular distribution of the bacterium within plants making it very easy to miss in the small tissue samples used for PCR. Some plants have inhibitors of PCR that a typical DNA extraction procedure would not completely avoid.

Li et al. (2013) have recently developed two TaqMan-based assays, one targeting the 16S rDNA signature region for the identification of X. fastidiosa at the species level and the other specific identification of the citrus variegated chlorosis (CVC) strains (Li et al., 2013).

Detection and Inspection

Symptoms are not reliable for detection of infected plants in transit.

X. fastidiosa can be detected microscopically (light or electron) in vessels in cross-sections of petioles (French et al., 1977) or by examining xylem sap squeezed from symptomatic stems or petioles or flushed from stems or petioles onto microscope slides (De Lima et al., 1998). Flushing of xylem sap from shoots with a pressure chamber allows the testing of larger sample sizes and avoids inhibitors for PCR (Bextine and Miller, 2004). Methods such as grafting to susceptible indicator plants or vector tests (Hutchins et al., 1953) are still available, and may have their place in certification schemes in which woody indicators are routinely used. X. fastidiosa can also be isolated onto suitable selective media (Davis et al., 1978, 1983; Raju et al., 1982; Wells et al., 1983). The identity of cultured bacteria can be confirmed by SDS-PAGE (Bazzi et al., 1994). Serological methods are less sensitive (10- to 100-fold) than culture but are the easiest means of detecting and identifying the bacterium, by ELISA or use of fluorescent antibodies (French et al., 1978; Walter, 1987; Hopkins and Adlerz, 1988; Sherald and Lei, 1991). Strains differ in quantitative reaction to antisera and in ease and efficiency of culture. DNA hybridization probes and PCR primers specific to X. fastidiosa have been developed (Firrao and Bazzi, 1994; Minsavage et al., 1994). X. fastidiosa can also be detected in its insect vectors (Yonce and Chang, 1987). The characterization and identification of strains chiefly employs molecular genetic methods (e.g., Chen et al., 1992; Hendson et al., 2001; Coletta-Filho et al., 2003), and can be expected to remain indefinitely in a state of change.

Different diagnostic methods used or developed for the detection and identification of X. fastidiosa are detailed in Janse (2009). Recent advances in detection include on-site molecular detection using real-time loop-mediated isothermal amplification (Yaseen et al., 2015).

Similarities to Other Species/Conditions

Zinc deficiency may cause similar patterns of chlorosis in grape and citrus but are distinctively different in pattern to an experienced observer. Diseased plants do not respond to zinc fertilization. In grape, esca (France, Italy, Spain) or measles (USA) has leaf scorching symptoms similar to Pierce's disease, but esca normally occurs early in the summer (June, July in Europe) following at least several days of hot weather, whereas Pierce's disease symptoms begin to appear after fruits begin to colour (verasion).

Prevention and Control

Phytosanitary Measures

Grapevine-growing countries should prohibit or severely restrict importation of grapevine planting material from countries where X. fastidiosa occurs. As recommended by EPPO (1990), if planting material is imported under licence, it should be maintained in post-entry quarantine for 2 years and shown to be free from the pest. Imported plants and fruits should be free from vectors, possibly by use of an appropriate treatment. A temperature treatment has been shown to eliminate the bacterium (45°C for at least 3 h) (Goheen et al., 1973), and may have potential as a phytosanitary measure.

Citrus-growing countries should similarly prohibit or severely restrict importation of citrus planting material from South America. Peach and other Prunus material from a country where the peach or plum strain occurs should come from a reliable certification scheme, with particular emphasis on preventing re-infection of healthy material via the vectors.

While the hazard presented by X. fastidiosa in other hosts (oak, plane, maple and others) still has to be evaluated, inspection services should be aware that these hosts and the many symptomless hosts also present a certain risk.

Chemical Control

Chemical control of Xylella diseases has not been successful in the field. Tetracycline drenches cause a temporary remission of symptoms in potted grapevines (Hopkins and Mortenson, 1971).
 

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Contributors

19/07/16 Reviewed by:

Rebekah Robinson, Royal Horticultural Society, RHS Garden Wisley, Woking, UK

Distribution Maps