Xylella fastidiosa (Pierce's disease of grapevines)

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.

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.

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).