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Cofemersimir.gob.mx005_Janse_S35 9-09-2010 12:06 Pagina 35 Journal of Plant Pathology (2010), 92 (1, Supplement), S1.35-S1.48
Edizioni ETS Pisa, 2010 XYLELLA FASTIDIOSA: ITS BIOLOGY, DIAGNOSIS, CONTROL AND RISKS
J.D. Janse1 and A. Obradovic2
1 Department of Laboratory Methods and Diagnostics, Dutch General Inspection Service, PO Box 1115, 8300 BC Emmeloord, The Netherlands 2 Plant Pathology Department, University of Belgrade, Serbia strains from the ornamental tree Chitalpa tashkentensis.
Vectors are mainly sharpshooters and froghoppers or The bacterium Xylella fastidiosa, a xylem-inhabiting, spittlebugs (Cicadellidae) that lack a latent period, and vector-transmitted, Gram-negative, very slow growing have no transstadial or transovarial transmission of the bacterium, was cultured and properly described for the bacterium. The pathogen shows persistence in the vec- first time in 1987 in the USA as the cause of Pierce's dis- tor adults, and ability to multiply in the foregut. In ease (PD) of grapevine, Vitis vinifera (disease observed North America main vectors (for PD unless indicated) already in 1884) and as the cause of phony peach dis- are Cuerna costalis (PPD), Draculacephala minerva ease (PPD) in peach, Prunus persica (disease observed (green sharpshooter) important also in ALS in Califor- in 1890 in the USA) and in 1993 in Brazil as the cause nia; Graphocephala atropunctata (blue-green sharpshoot- of citrus variegated chlorosis (CVC) or citrus X disease.
er), most important before the introduction of the glassy Moreover, it was found that the bacterium also causes a winged sharpshooter; G. versuta (PPD); Hordnia circel- number of so-called leaf scorch diseases in Prunus spp.
lata, most efficient; Homalodisca vitripennis [formerly (including almond leaf scorch or ALS in Prunus amyg- H. coagulata (glassy-winged sharpshooter or GWSS)]; dalus and plum leaf scald or PLS in Prunus domestica), H. insolita (PPD), Oncometopia nigricans, O. orbona Acer spp., Carya illinoinensis (pecan), Coffea arabica (PPD), Xyphon fulgida [formerly Carneocephala fulgida (CLC, in Brazil isolated in 1995 and also pathogenic to (red-headed sharpshooter)]. CVC vectors in Brazil are Citrus), Hedera helix, Morus rubra, Nerium oleander Acrogonia terminalis, that lays eggs externally on leaves, (OLS), Platanus occidentalis, Quercus spp., and Ulmus Dilobopterus costalimai and Oncometopia fascialis. Local americana. It infects also Medicago sativa (alfalfa dwarf) possible vectors for Europe are Cicadella viridis and and Vinca major (wilting symptoms). Many wild plants Philaenus spumarius (meadow spittle bug). X. fastidiosa may carry the pathogen with, but more often without is an emerging threat in the south-west USA, mainly due showing symptoms, such as grasses, sedges and trees. A to recent establishment of H. vitripennis, providing list of main hosts is presented. All these diseases are not much more efficient transmission than local vectors, seed-borne and occur mainly in tropical/subtropical ar- and leading to very serious outbreaks of PD in eas, although leaf scorch diseases also occur in much grapevine, ALS and OLS. GWSS probably first entered colder climate, e.g. oak leaf scorch in eastern North California as eggs in plants. The eggs are deposited into America up to Canada. Several pathogenic varieties of plant tissues. In Central and South America X. fastidiosa the bacterium have been described, that are often host- has become very noxious due to the rapid expansion specific (e.g., the PD strain will not cause disease if in- (most likely via distribution of infected planting materi- troduced to peach or plum). The following subspecies al) of CVC in Citrus, leading to more than a third of all have been described: (i) Xylella fastidiosa subsp. fas- trees in the area having symptoms of CVC, and CLC in tidiosa (erroneously named X. f. subsp. piercei), PD and coffee. For Europe there are until now only a few un- LSA, strains from cultivated grape, alfalfa, almond, and confirmed reports of the presence of X. fastidiosa in maple; (ii) X. fastidiosa subsp. multiplex, PPD, PLS, grapevine from Kosovo [erroneously mentioned as strains from peach, elm, plum, pigeon grape, sycamore Slovenia in Janse (2006)] and in France, based on dis- and almond; (iii) X. fastidiosa subsp. pauca, CVC, ease symptoms observation. Since X. fastidiosa has more strains from citrus and probably those from coffee that 150 hosts and many of them, including Vitis plant- (CLC); (iv) X. fastidiosa subsp. sandyi, strains from Ner- ing material, were and are imported, risk of introduc- ium oleander (OLS); (v) X. fastidiosa subsp. tashke, tion (especially in latent form) must not be underesti-mated. Absence of the diseases caused by X. fastidiosawill mainly be due to the absence of suitable vectors.
Corresponding author: J.D. Janse However, introduction of the pathogen and vectors with Fax: +31.527.635411E-mail: firstname.lastname@example.org plant material can not be excluded for certain. More- 005_Janse_S35 9-09-2010 12:06 Pagina 36 S1.36 Xylella fastidiosa a threat for Europe? Journal of Plant Pathology (2010), 92 (1, Supplement), S1.35-S1.48
over, also local Cicadellidae (see above) could become only properly described, classified and named Xylella (potential) vectors. Therefore, X. fastidiosa has the A1 fastidiosa in 1987 (Wells et al., 1987). Already in the quarantine status in the EPPO region and H. 1940's sharpshooter leafhoppers and spittlebugs were vitripennis, that has a very large host range and also identified as vectors of PD and PPD (Severin, 1949).
feeds on almond, peach and plum, was recently put on Once the bacterium was described and more easily cul- the EPPO alert list. As in the more northern parts of tured, X. fastidiosa was found in large number of other the USA, Vitis varieties in Europe are very susceptible hosts, with or without symptoms. The most important to X. fastidiosa and this is really a risk should a vector are the so-called leaf scorch and scald diseases of Prunus that could survive the winters of southern Europe be- spp. (including almond leaf scorch or ALS in Prununs come established, also in wild hosts (e.g. wild and do- amygdalus and plum leaf scald or PLS in Prunus domes- mestic plums and wild cherry are symptomless reser- tica), Acer spp., Carya illinoinensis (pecan), Coffea arabi- voirs in the USA) and cause spring infections that ca (coffee leaf scorch or CLS), in Brazil (isolated in 1995 would most likely to persist over the years. The same and also pathogenic to Citrus), Hedera helix, Morus risk holds true for Citrus (sweet oranges, mandarins, rubra, Nerium oleander (oleander leaf scorch or OLS, and tangerines) and other hosts, such as almond, plum Grebus et al., 1996), Platanus occidentalis, Quercus spp., and peach that are widely grown in south-east and Ulmus americana. Furthermore the bacterium was south-west Europe, especially in the warmer Mediter- found in Medicago sativa (alfalfa dwarf), Vinca major ranean basin (where a disease-favourable combination (wilting symptoms), and in avocado Persea americana of warm nights, regular rainfall/high humidity and long (Montero-Astúa et al., 2008). Many wild plants were growing season, is present). Possible ways to prevent in- found to carry the pathogen (often latent only), such as troduction and to control eventual outbreaks are indi- grasses, sedges and trees (Freitag, 1951; Blake, 1993; cated. The conclusion is that X. fastidiosa is a real and Hartman, 1991, 1992, 2003; Hernandez-Martines et al., emerging threat for Europe, not only for Vitis and Cit- 2007; Raju et al., 1983). rus but also for stone fruits (almond, peach and plum) In 1987 in Brazil, a rapidly spreading disorder, simi- and oleander (e.g. GWSS likes to feed on oleander), lar to PD, called citrus variegated chlorosis (CVC) or that is difficult to prevent from entering and difficult to citrus X disease of Citrus, was observed and X. fas- control once established, deserving more attention than tidiosa was also isolated from diseased trees in 1993 up till now. Resistance in European grapes is scarce or (Chang et al., 1993). Characterization of X. fasdidiosa even absent. Vector control proved not to be very effec- culminated in whole genome sequencing, and a citrus tive in the USA. Cultural practices to keep plants in op- strain of X. fastidiosa actually was the first plant patho- timum condition are of importance, but not sufficient genic bacterium from which the whole genome was se- and the use of avirulent strains for cross-protection is quenced. The sequences of three Xylella strains (from still in its infancy.
almond, oleander and citrus) are now available at Inte-grated Genomics. Till now, diseases caused by X. fas-tidiosa have only been reported from North and South INTRODUCTION AND HISTORY
America (especially Brazil). In Europe, there is only oneunconfirmed report from Kosovo (Berisha et al., 1998).
In the 1880's a ‘mysterious' vine disease destroyed ca.
However, it can not be excluded that the pathogen is 14,000 ha of grapes (Vitis spp.) and ca. 50 wineries had present on a low scale and goes still undetected because to close down in the Los Angeles area in California.
of unfamiliarity with the symptoms and (still) lack of ef- This disease was described in detail in 1887 by N.B.
ficient vectors. This because (wild) grape rootstocks Pierce (1856-1916) and was later named after him: from North America have been imported on a large Pierce's disease (PD) of grapevine. Now, 125 years later, scale to Europe for their resistance to phylloxera since PD is still a main concern for grape and wine producers the end of the nineteenth century. Moreover, the import in southern USA (especially California, Texas and Flori- of other of its many hosts (Table 1) could have lead to da). For a long time the causal agent could not be cul- incidental introductions that still go unnoticed. Given tured outside the host and was generally regarded as a this situation and the recent outbreak in California due virus or a non-culturable bacterium (Rickettsia-like or- to the introduction of H. vitripennis as a new vector, an ganism or RLO). A related disease was recorded in overview and preliminary risk evaluation of this impor- peach (Prunus persica) in 1890 in the USA, with out- tant pathogen appears desirable. breaks (mainly in Georgia) in 1929, 1951 and 1976 andwas named phony peach disease (PPD). The causal agent of PD was isolated from grape in SYMPTOMS AND TRANSMISSION
pure culture for the first time in 1978 (Davis et al.,1978). However, this xylem-inhabiting, vector-transmit- Grapevine. First symptoms are sudden drying of
ted, Gram-negative, very slow growing bacterium, was large parts of a green leaf. These parts become brown 005_Janse_S35 9-09-2010 12:06 Pagina 37 Journal of Plant Pathology (2010), 92 (1, Supplement), S1.35-S1.48
Janse and Obradovic S1.37 necrotic and the surrounding tissues become yellow to Table 1. Natural host plants of X. fastidiosa in which the
red. The necrosis is often present at the leaf margins pathogen was surely identified (source: http://www.cnr.
(Fig. 1A). Scorched (burnt-like) leaves usually drop berkeley.edu/xylella/). For a complete list of hosts, see thesame site.
from the distal and not from the usual basal end of thepetiole, leaving bare petioles attached to canes, often well after normal leaf fall. PD can be confused with oth- Acacia longifolia er disorders such as salt toxicity, boron, copper or phos- Acer macrophyllum phorus deficiency. In later stages, more yellowing occurs California buckeye and leafs shrivel and drop. Defoliation, shoot dwarfing and cane stunting, as well as dehydration of fruit clus- Avena fatua ters may occur. Irregular patches of brown and green tissue can be found on the canes. The trees may be re- Bromus rigidus duced in growth, stunted and have a low and short pro- American beautyberry duction which may lead to plant death. Main (persistent) vectors are Xyphon fulgida (= Car- Citrus sinensis Cynodon dactylon neocephala. fulgida), Draeculacephala minerva, Grapho- Cytisus scoparius cephala atropunctata, Homalodisca vitripennis and On- cometopia nigricans in North America. Possible vectors Duranta repens in southeast Europe are Cicadella viridis and Philaenus spumarius (meadow spittle bug) (Redak et al., 2004). Aust. brush-cherry Peach. First symptoms are stunted young shoots that
Fraxinus dipetala have earlier, more numerous and darker green leaves than normal. Moreover they show early blooming and Hedera helix both leaves and flowers remain on the shoots longer than normal. Twigs on diseased trees have shortened in- ternodes and increased lateral branching. Lateral branches grow horizontally or droop. Fruit production Medicago hispida is severely impaired and fruits are small and early ripen- Melilotus sp. ing. Trees that will be infected before bearing will never Oenothera hookeri be productive. Symptom development is often slow (up to 18 months or more after infection) and may be pres- ent in one scaffold limb or in the entire tree. An ex- tremely dry summer seems to delay symptom develop- ment for at least a year. Phony-infected leaves are gener- ally broader, slightly more flat, and stay on the tree Prunus sp. longer in the fall. Phony-infected trees when completely Quercus agrifolia infected appear uniform across the top, a hedged look Quercus lobata (Fig. 1D). Trees are generally not killed but are more Rosa californica California wild rose susceptible to other diseases and arthropods. Main (per- Rosa californica California wild rose sistent) vectors are H. vitripennis, H. insolita, Oncome- topia orbona, Graphocephala versuta and Cuerna costalis.
Rubus ursinus California blackberry Rubus ursinus California blackberry Citrus. Symptoms can be observed especially on
Rumex crispus sweet orange trees from nursery up to 10-year-old (older trees show just a few diseased branches). Plants do not Sambucus mexicana usually die. Small interveinal chlorotic spots (slightly Sambucus mexicana raised and gummy on upper side and brown on lower side of the leaf) on leaves in parts of a tree or all over the tree, very similar to zinc deficiency symptoms. In later Trifolium repens var. latum stages brown necrotic spots develop on the lower side of California bay or laurel the leaf, corresponding to the chlorotic areas on the up- Uritca dioica ssp.gracilis per side. Wilting may occur. Fruits remain small, have Veronica sp. higher sugar content and a harder rind than normal and Vinca major greater periwinkle ripen earlier (Fig. 1B) Water stress or senescence may Vitis californica Calif. wild grape Vitis rupestris aggravate the symptoms. A chronic form of the disease Vitis vinifera 005_Janse_S35 9-09-2010 12:06 Pagina 38 S1.38 Xylella fastidiosa a threat for Europe? Journal of Plant Pathology (2010), 92 (1, Supplement), S1.35-S1.48
Fig. 1. A. Typical leaf scorch symptoms, caused by Xylella fastidiosa subsp. fastidiosa on a grapevine leaf (source: http://www.pdg-
wss.net/Board_Info/FAQs.htm) B. Typical symptoms on leaves (variegated spots) and fruits (dwarf growth) of Citrus caused by
Xylella fastidiosa subsp. pauca (source: A.H. Purcell). C. Severe symptoms of leaf scorch on a Platanus occidentalis (sycamore)
caused by X. fastidiosa subsp. fastidiosa (source: A.H. Purcell). D. Symptoms of Phony peach disease on Prunus persica (peach),
reduced growth of the tree on the left (source: http://www.aces.edu/mt/peachipm/archives/001409.php).
shows stunting and dieback of twigs (Crop Protection Coffee. First symptoms appear on young shoots as
Compendium, 2005; EPPO, 2004). The bacterium also large scorched areas on the top or at the margins of ma- occurs in the roots (Hopkins et al., 1991). Medium and ture leaves. Dwarf growth of new shoots, small, pale long distance dissemination is by infected planting ma- green to yellow leaves, shoot dieback, and overall plant terial. Out of the 11 sharpshooter vectors found in stunting occur. Fruit size and yield are impaired. Symp- Brazil, Acrogonia citrina, Bucephalogonia xanthophis, toms are severe under conditions of water stress, but Dilobopterus costalimai, Macugonalia leucomelas, and trees generally do not die or only after some years (Lima Oncometopia fascialis are the most important. Since et al., 1998).
they are the most common on citrus, these hosts are themost important source of inoculum (Almeida et al., Other hosts. The symptoms caused by X. fastidiosa in
2005). Although the pathogen is considered not to be other hosts resemble by and large those described above, seed borne, transmission from seeds to seedlings of namely: early symptoms are a slight chlorosis or bronz- sweet orange has been reported (Li et al., 2003).
ing along the leaf margin or tip that intensifies and thatmay become water-soaked before browning and drying.
005_Janse_S35 9-09-2010 12:06 Pagina 39 Journal of Plant Pathology (2010), 92 (1, Supplement), S1.35-S1.48
Janse and Obradovic S1.39 These symptoms are first found on a few branches, later on almost all foliage. The affected area is delineated by anarrow chlorotic band that becomes especially clear in X. fastidiosa is a Gram-negative, strictly aerobic, autumn. A premature defoliation takes place with new xylem-inhabiting, non-flagellated pathogen with a malformed leaves formed. Abnormally shaped fruit may growth optimum of 26-28°C. It moves downstream, but also be formed and stems may show internal and exter- also upstream in plants. The upstream movement is pos- nal discoloration, dieback and abnormal growth, leading sible with long type IV pili (twitching motility). In ad- to eventual death of the host. Transmission to other vanced stages of infection, sap blocking biofilms are hosts is largely unknown. Based on epidemiological in- formed both in the host plant and in the foregut of the formation available from intensive studies of diseases in- vectors. Type I pili play the most important role in cited by X. fastidiosa in economically important crops, it biofilm formation and aggregation of cells. The biofilms is assumed that the main type of transmission of this in plant and vector differ in composition and they are bacterium in minor crops or host plants in spontaneous actively (signal-based) produced by the pathogen. (Li et flora is by insect vectors feeding on more than one plant al., 2007; Meng et al., 2005). In the vector biofilm the species. Giving the fact that there are thousands of insect bacterial cells are pearly attached (Newman et al., species potential vectors worldwide, studying of their 2004). The pathogenicity of Xylella fastidiosa shows potential role and efficiency in the pathogen transmis- similarities to that of Xanthomonas campestris pv.
sion is an important part of pest risk assessment within a campestris: it produces a wide variety of pathogenicity particular geographical region.
factors for host-specific colonization such as a large Fig. 2. A. Cells of X. fastidiosa in biofilms polarly attached on the cuticle of foregut (source: A. Almeira) B. Cells of X. fastidiosa in
xylem vessels (source: A. Almeira). C. The glassy-winged sharpshooter Homalodisca vitripennis (formerly H. coagulata), a vector of
Xylella fastidiosa (source: http://www.apsnet.org/bookstoretitles/EPPCD/Images/3-14.htm). D. Philaenus spumarius (meadow
spittle bug) a potential vector of X. fastidiosa, occurring in Europe (source: EPPO).
005_Janse_S35 9-09-2010 12:06 Pagina 40 S1.40 Xylella fastidiosa a threat for Europe? Journal of Plant Pathology (2010), 92 (1, Supplement), S1.35-S1.48
number of fimbrial and afimbrial adhesins for attach- It appears that most of xylem-feeding Cicadellidae ment. The exopolysaccharidal slime (EPS) is similar to species can be or are vectors in nature (Purcell, 1989), the xanthan gum produced by Xanthomonas campestris where probing behaviour (e.g. preference for young pv. campestris. It does not have a type III secretion sys- shoots or, as in H. vitripennis, preference of woody tis- tem; however, genes for a type II secretion system for sues, even transmitting the bacterium to dormant vines, export of exoenzymes that degrade the plant cell wall leading to winter-persisting populations of the and allow the bacterium to colonize the plant xylem pathogen) and foregut morphological characteristics de- were determined. In some aspects (biofilm formation) termine the efficiency of bacterial transmission (Almei- X. fastidiosa is more similar to animal pathogens da et al., 2005; Hopkins and Purcell, 2002). It has been (Machado et al., 2001; Chatterjee et al., 2008). Biofilm determined that for PD, alfalfa dwarf and CVC 27, 22 formation and attachment (Fig. 2A) are under control and 11 species of Cicadellinae were vectors of X. fas- of the GacA gene, which plays a similar role in other tidiosa (Redak et al., 2004). Some 39 species of 19 gen- phytopathogenic bacteria. It is also involved in physio- era of Cicadellinae (sharpshooters) and 5 species of Cer- logical processes that may enhance the adaptation and copidae (spittlebugs) have been reported as vectors.
tolerance of X. fastidiosa to environmental stresses and Vectors have been mainly identified in North America.
the competition within the host xylem (Shi et al., 2009), The most important are (for PD, unless indicated) in The bacterium can enter neighbouring vessels through North America: Cuerna costalis (PPD); Draeculacephala pits, after degradation of the pith membranes, which is minerva (green sharpshooter) important also for ALS in apparently also triggered by a diffusible signal from the California; Graphocephala atropunctata bacterium (Newman et al., 2004). The bacterium is also sharpshooter), most important, before GWSS, see fur- present in roots and can therefore be transmitted by ther; G. versuta (PPD); Hordnia circellata, most effi- root grafting. Vessels can become occluded by dense cient; Homalodisca vitripennis (Fig. 2C); H. insolita colonization (Fig. 2B) and high frequencies of blocked (PPD); Oncometopia nigricans, O. orbona (PPD); vessels are associated with disease symptom develop- Xyphon (formerly Carneocephala) fulgida (red-headed ment. EPS and polygalacturonase also play a role in the sharpshooter). For CVC in Brazil: Acrogonia terminalis, break down of pit membranes and xylem occlusion lays eggs externally on leaves; Bucephalogonia xan- (Roper et al., 2007a). EPS also entraps hydrolytic prod- thophis; Dilobopterus costalimai and Oncometopia fas- ucts that can be utilised by the bacteria as carbon cialis. Local possible vectors for Europe are Cicadella source (Roper et al., 2007b). viridis and Philaenus spumarius (meadow spittle bug) X. fastidiosa has been found in a latent state in many symptomless hosts, i.e. mugwort (Artemisia douglasiana) Although not all X. fastidiosa transmitting vectors and watergrass (Echinochloa cruz-galli), that serve as a play an important role in transmission from wild hosts source of inoculum for vectors (Hopkins and Purcell, to crops, it was found in California that inoculum pres- 2002), although they did not move systemically in most ent in weed hosts (herbs and shrubs) in adjacent ripari- of the symptomless hosts. Systemic movement was an woods facilitated spread of PD into vineyards in ear- found in symptomless blackberry (Rubus procerus). X. ly spring, when the blue-green sharpshooter, G. atrop- fastidiosa is irregularly distributed in infected tissues unctata (that overwinters as adult) apparently played an (Hopkins and Adlerz, 1988), thus longer plant access important role (Hopkins and Purcell, 2002). Adlerz and time may increase chances of the vector probing infect- Hopkins (1979) found that Oncometopia nigricans (Walker) was a more important vector in central Floridathat H. vitripennis because of larger population forma-tion in early spring. Vectors that overwinter as eggs or BACTERIUM -VECTOR RELATIONSHIP
nymphs are thought to be less important in the dissemi-nation of the disease. It was therefore theorized that X. X. fastidiosa is transmitted persistently by xylem-sap fastidiosa does not yet occur in Europe due to absence sucking insect vectors as follows: (i) acquisition from a of vectors that survive winter as adults and, even if in- source plant; (ii) attachment and retention to vector's fected, could not cause extensive spread due to absence foregut cuticle; (iii) detachment and inoculation into a during the critical early spring period. (Purcell, 1997). new host. Vectors are mainly sharpshooters and spittle- Transmission efficiency by vectors may vary. H. vit- bugs (Cicadellidae), have no transstadial or transovarial ripennis for example transmits much more efficiently transmission (nymphs shed cuticle) and the bacterium from grape to grape than from almond to almond (Hop- does not need a latent period. Once infected with X. fas- kins and Purcell, 2002). Efficiency of CVC vectors is tidiosa, insects remain infective with the pathogen, which low (less than 10%), further information in Redak et al. multiplies in the foregut and the bacterium becomes per- (2004). H. vitripennis is considered now one of the most sistent in adult insects. Only a few bacterial cells are re- important vectors responsible for spreading of X. fas- quired for transmission (Hill and Purcell, 1995). tidiosa-caused diseases in south-east United States, espe- 005_Janse_S35 9-09-2010 12:06 Pagina 41 Journal of Plant Pathology (2010), 92 (1, Supplement), S1.35-S1.48
Janse and Obradovic S1.41 cially California, such as PD and oleander leaf scorch, armeniaca and plum leaf scald or PLS in P. domestica), but also ALS, PP and PLS, furthermore inhibiting the Acer spp., Carya illinoinensis (pecan), Coffea arabica successful culture of V. vinifera L. and V. labrusca L. In (CLC, in Brazil isolated in 1995 and pathogenic also to the mild winters of California, H. vitripennis transmits Citrus), Hedera helix, Morus rubra (American the pathogen also to dormant vines. H. vitripennis has a mulberry), Nerium oleander (OLS), Platanus occidentalis very broad host range. It has been found on more than (sycamore, Fig. 1C), Quercus spp. (oak), Ulmus ameri- 70 plant species in 35 families including: avocado, cit- cana (elm tree). Furthermore it induces diseases of Med- rus, macadamia, and many woody ornamentals, e.g.
icago sativa (alfalfa dwarf), Catharanthus roseus (peri- Fraxinus, Lagerstroemia and Rhus. (Almeida et al., 2005; winkle) and Vinca major (both wilting symptoms), Redak et al., 2004).
stunting of Ambrosia artemisifolia (ragweed). Many wildplants may carry the pathogen with, but more oftenwithout, showing symptoms, such as grasses, sedges and BACTERIUM-HOST PLANT RELATIONSHIP
trees. A list of hosts from which X. fastidiosa was isolat- ed is presented in Table 1. Some tree species found to be infected based on PCR Several pathogenic varieties of X. fastidiosa have asays are Acer negundo, Aesculus x hybrid, Celastrus or- been described, that are often host-specific [e.g. the PD biculata and Cornus florida (McElrone et al., 1999).
strain will not cause disease if introduced to peach or Hartman et al. (2002) detected the pathogen in oak plum; PD, ALS and alfalfa dwarf are caused by the species, including Quercus coccinea (scarlet oak), Celtis same strains. PPD and PLS strains can be reciprocally occidentalis (hackberry), M. rubra and M. alba (white graft-transmitted. Peach strains, however, do not cause mulberry) in Kentucky (USA) that has a temperate cli- disease in grape and grape strains do not infect peach, mate. In the USA native wild plums, especially Prunus furthermore OLS strain does not infect grape and vice angustifolia (chickasaw plum) were found to be inocu- versa. But both PD and OLS strains infect almond. Rec- lum reservoirs for X. fastidiosa facilitating spread of iprocal transmission between elm and sycamore leaf PPD. A leaf scorch described in 1990 in Taiwan on scorch strains was negative. A CVC strain of X. fas- Pyrus pyrifolia (Japanese pear) cv. Hengshan in particu- tidiosa produced leaf scorch disease in coffee, and CVC lar, and P. serotina (Asian pear), was found to be caused and coffee strains can cause disease in grape under by a bacterium very similar (but deviating from North greenhouse conditions (Hopkins and Purcell, 2002). X. and South American strains serologically and in house- fastidiosa shows a certain host-specialization and other keeping gene sequences) to X. fastidiosa (Leu and Su, variations that warranted the following subspecific divi- 1993; Chen et al., 2006). Asian pears have recently been sion (Schaad et al., 2004; Hernandez-Martinez et al., introduced in central Europe (Romania) and Japanese 2007): (i) X. fastidiosa subsp. fastidiosa (erroneously pears, or nashis, were planted as a novelty crop in named X. f. subsp. piercei, see Schaad et al., 2004), PD southern Europe in the 1980's. and ALS, strains from cultivated grape, alfalfa, almond, Other natural hosts are Ambrosia artemisiifolia, Am- maple (Acer), cherry, Spanish broom (Genista), one pelopsis arborea, Baccharis halimifolia, Callicarpa ameri- strain from western redbud (Cercis occidentalis); (ii) X. cana, Citrus jambhiri, Fragaria vesca var. californica, f. subsp. multiplex, PPD, PLS, strains from peach, elm, Montia linearis, Parthenocissus quinquefolia, Quercus fal- plum, pigeon grape (Vitis aestivalis), sycamore cata, Q. laurifolia, Q. nigra, Rhus sp., Rubus procerus, (Platanus), almond (one strain), olive, sweetgum (Liq- Sambucus canadensis, Solidago fistulosa, Vinca minor and uidambar), Ginkgo, crape myrtle (Lagerstroemia indica), Vitis rotundifolia (Hopkins and Purcell, 2002).
one strain from western redbud; (iii) X. f. subsp. pauca, For a full lists of the different types of hosts, see CVC, strains from Citrus and probably those from cof- fee, Coffea (CLC); (iv) X. f. subsp. sandyi, strains fromNerium oleander (OLS), daylily (Hemerocallis spp.), Geographical distribution. Diseases incited by X. fas-
Jacaranda and Magnolia (Hernandez-Martinez et al., tidiosa occur mainly in tropical/subtropical areas, al- 2007); (v) X. f. subsp. tashke, strains from the ornamen- though leaf scorch diseases also occur in much colder tal tree Chitalpa tashkentensis; (vi) mulberry (Morus climate, e.g. oak leaf scorch up to Canada (Table 2). The spp.) and heavenly bamboo (Nandina domestica) strains, geographical distribution according to the latest find- not yet allocated to subspecies (Hernandez-Martinez et ings (see http://www.eppo.org/) is as follows: al., 2007).
EPPO and EU region: absent. Unconfirmed reports on imported grapevine material from USA in France Host range. Apart from the already mentioned dis-
and from Kosovo (EPPO Reporting Service 500/02, eases PD, PPD and CVC, it was found that X. fastidiosa 505/13 and 1998/9; Berisha et al., 1998); also causes a number of so-called leaf scorch diseases in Asia: India [on almonds (Jindal and Sharma, 1987); Prunus spp. (including almond leaf scorch or ALS in P. not confirmed recently] and Taiwan [pear leaf scorch, a 005_Janse_S35 9-09-2010 12:06 Pagina 42 S1.42 Xylella fastidiosa a threat for Europe? Journal of Plant Pathology (2010), 92 (1, Supplement), S1.35-S1.48
bacterium similar to X. fastidiosa, questionable serologi- root sections and immersing them in acidified methanol cal relatedness (Leu et al., 1993)]; (1 ml concentrated HCI in 100 ml absolute methanol).
North America: Mexico, USA (Alabama, Arizona, Infected roots show purplish spots within a minute or California, Florida, Georgia, Louisiana, Mississippi, two where vessels contain bacteria.
Missouri, Montana, North Carolina, Oklahoma, South X. fastidiosa is a slow-growing (fastidious) bacterium Carolina, Texas; oak scorch found in Kentucky and as that does not grow on many common culture media, far north as New York and West Virginia); but some good selective media are available, such as Central America and Caribbean: Costa Rica, proba- PD2, PW, CS20 or BCYE (Schaad et al., 2001).
bly most countries in Central America, also for CLS Colonies on the most frequently used Periwinkle medi- (Aguilar et al., 2005) and OLS (Monter-Astua et al., um (PW) are circular with entire margins, convex, opalescent-white, reaching 0.7-1.0 mm diameter after 2- South America: CVC has been reported from Ar- 3 weeks. Isolation can be performed by blotting ex- gentina (Brlansky et al., 1991), and Brazil (São Paulo, pressed sap (after surface sterilisation) on media, by Minas Gerais, Rio de Janeiro; rapidly spreading), PD re- placing pieces of infected vascular tissue in PW broth, ported from Venezuela (Jimenez, 1985) and plum leaf shaken and subsequently plated on agar medium or vac- scald in most South American areas where Prunus salici- uum extracted. Isolation from insects is by surface ster- na is grown. ilisation, dissection of the head which is homogenised insterile PBS and suspension plated onto media. Platesshould be kept up-side-down and sealed with parafilm, DETECTION AND IDENTIFICATION
and media should be checked for up to a month for typ-ical colonies, which should be subcultured on nutrient Cells of X. fastidiosa are small and narrow (0.2-0.4 x agar and selective media, only colonies growing on the 1.0-4.0 µm) and therefore only visible using at least dark latter should be subjected to further identification tests.
field or phase contrast microscopy. Bacteria can be PD and PPD (and other) type of strains can be differen- found in infected tissues most easily in sap/ooze of leaf tiated by growth on PD2 (PD strains positive, others veins or vessels of petioles of scorched leaves or negative) and PW BCYE/CS-20 agar (PPD strains posi- trunk/branch vascular tissue of non-leaf scorched symp- tive, PD strains negative), ELISA using different antis- tomatic trees. With PPD, roots should be investigated.
era and PCR (Schaad et al., 2001). A full account on For preliminary confirmation of pathogen presence in isolation and detection by tissue extract PCR is given in fresh plant tissue, one ml of KOH 0.1 M can be vacuum drawn trough vessels and a resulting drop placed under the microscope. When the symptoms are not very defi- DNA extraction from insects can be performed with nite the disease can be further recognised by cutting immuno-magnetic separation, or using a DNA extrac- Table 2. Geographical distribution according to X. fastidiosa host/strain type (EPPO website, http://www.eppo.org/),
and data sheet Xyllela fastidiosa (EPPO, 1992).
Strain type of Xyella fastidiosa* North and Central Americas, Peru, unconfirmed report from Kosovo Almond leaf scorch Argentina, USA, California, Peach-plum strains Phony peach South-eastern USA South-eastern USA Citrus variegated chlorosis (‘pecosita' in Argentina, Argentina, Brazil ‘amarelinho' in Brazil)Coffee leaf scorch Oak leaf scorch (related to peach strains) Sycamore leaf scorch Mulberry leaf scorch Widespread in South America, Paraguay, Brazil Pecan leaf scorch Oleander leaf scorch USA, California and Florida * For differentiation into subspecies, also related to hosts, see under "Biology" 005_Janse_S35 9-09-2010 12:06 Pagina 43 Journal of Plant Pathology (2010), 92 (1, Supplement), S1.35-S1.48
Janse and Obradovic S1.43 Table 3. PCR Primers useful for detection of Xylella fastidiosa.
Minesavage et al., 1994 Unique E.coli R 1 fragment Minesavage et al., 1994 Firrao and Bazzi, 1994 Firrao and Bazzi, 1994 tion kit such as the DNeasy Tissue kit (Qiagen, USA) or Table 4. A multiplex PCR for detection of all X. fastidiosa
the Genomic DNA Purification kit (Fermentas, USA).
strains both in plant tissue and insects, using primers against The latter performed well in the study of Bextine et al.
X. fastidiosa gyrase b gene and 16 S rRNA genes.
To detect X. fastidiosa, three specific primers sets can be used. For the PD strain the RST primers can be used (Minesavage et al., 1994) (Table 3). Non-grapevine strains can be detected by XF primers (Firrao andBazzi, 1994). A multiplex PCR for detection of all X. fastidiosa strains both in plant tissue and insects, using primers against X. fastidiosa gyrase b gene and 16S rRNA genes was developed by Rodrigues et al. (2003) CGATACTGAGTGCCAATT TGC (Table 4). Another multiplex PCR was developed by CTCCTCGCGGTTAAGCTA C Hernandez-Martinez (2006). Primers ALM1 and ALM2yielding a 521 bp fragment from almond strains that be-long to X. f. subsp. multiplex, and XF2542-L and XF2542-R, resulting in a 412-bp fragment from PD andcertain almond strains, were combined. Real-time PCR Since X. fastidiosa is "localized" on the American was developed by Oleivera et al. (2002) using the continent, the rest of the world is focused on implemen- primers and probe reported in Table 5. A highly effi- tation of quarantine and phytosanitary procedures in or- cient (as compared to classical PCR) combined agar ab- der to prevent "escape" of the pathogen from its place sorbent and bio-PCR for grape and citrus strains was of origin. Considering the wide host range, numerous developed by Fatmi et al. (2005). insect vectors, latent nature, global movement of plant A pathogenicity test with a pure culture of X. fas- material, these preventive administrative measures tidiosa can be performed by hypodermic syringe/needle should be fortified by other prophylactic actions based injection of a sterile PBS suspension of bacteria into the on the experience from countries suffering from this vascular system. For PPD strains a root inoculation is bacterium. As chemical curative control of the bacteri- advisable (Schaad et al., 2005). An improved biotest on um is not possible, control of diseases caused by X. fas- tobacco was described by Francis et al. (2008), using tidiosa in the countries of origin concentrate on preven- Nicotiana tabacum cv. SR1 (Petite Havana), yielding tion, by use of resistant varieties, cultural and hygienic symptom expression already after 15 days with a final measures and chemical and biological vector control.
evaluation 4 to 6 weeks after inoculation. The tobacco These other methods, however, are often only partly leaves show typical scorch symptoms (see also Lopes et successful. Reasons are e.g. that X. fastidiosa has many al. (2000). A complete diagnostic protocol including symptomless hosts, including weeds, ornamentals and flow scheme of tests necessary for diagnosis, including other crops and possibly also still unknown vectors. Re- confirmatory host test is given by EPPO (EPPO, 2004).
moval of diseased trees is only partly successful becauseof introduction of the pathogen from neighbouring ar- Table 5. Primers used in the Real-time PCR protocol developed by Oliveira et al. (2002).
AGATGAAAACAATCATGC AAA 5'GCG CAT GCC AAG TCC ATA TTT 005_Janse_S35 9-09-2010 12:06 Pagina 44 S1.44 Xylella fastidiosa a threat for Europe? Journal of Plant Pathology (2010), 92 (1, Supplement), S1.35-S1.48
eas. Purcell (1980) showed that PD infected plants Cultural practices. Stress is often a determining fac-
could be cured from X. fastidiosa in cold winters. Fur- tor in the development of symptoms once a plant has thermore bacterial populations in shoots were negative- become infected with X. fastidiosa. Cultural practices ly correlated with cumulative hours below -5°C (Hen- should therefore be directed towards healthy, well neberger et al., 2004). Cross-protection with weakly or growing plants and adequate nutrition. Iron deprivation avirulent strains of X. fastidiosa has been successful in possibly provides a way to reduce disease severity by different grapevine cultivars, including Cabernet sauvi- preventing biofilm formation in the xylem vessels gnon and Vidal blanc, to some extent, especially with (Toney and Koh, 2006). The following cultural practices strain EB92-1. The bacteria are inoculated by pin-prick- have proved to be effective (source: http://edis.ifas.
ing or drilling and syringe injection (Hopkins and Pur- ufl.edu/in174): (i) cultivar selection (mainly for grape); cell, 2002; Hopkins, 2005).
(ii) removal of diseased trees in two to five-year oldpeach orchards, this extends productive orchard life; Host resistance. Unfortunately most cultivars of Eu-
(iii) survey for the disease in June and July, pruning after ropean (V. vinifera), American (V. labrusca) and hybrid diseased tree removal, with avoidance of heavy summer grapes are susceptible to Pierce's Disease. However, re- pruning; (iv) rouging wild plums and cherries or other sistance to PD was found in Vitis species native to hosts, within ca. 400 m of an orchard; (v) establishing south-eastern US. The grape industry in this area of the new plantings, which should not include both peaches country is based on these resistant Vitis species. Musca- and plums, not closer than 400 m to existing orchards dine grapes (V. rotundifolia) are often highly resistant or (never planting near infected orchards); (vi) weed con- tolerant and much used in the south-eastern US (Hop- trol in and around orchards; (vii) elimination of woods, kins and Purcell, 2002). Resistance was found in differ- especially oaks, near orchards when possible; (viii) no ent grapevine genotypes such as Muscadinia routine spraying with insecticides for leafhopper popu- rotundifolia, Vitis arizonica/candicans, V. arizonica/gir- lations will not substantially decrease. diana, V. candicans, V. girdiana, V. nesbittiana, and V.
shuttleworthii following artifical inoculation. However,V. vinifera, V. aestivalis and V. champinii developed very RISKS AND CONCLUSIONS
high X. fastidiosa concentrations in their vascular tissues(Fritschi et al., 2007).
X. fastidiosa is an emerging threat in the south-west US, due to recent establishment of the glassy-winged Vector control. When there are recent introductions
sharpshooter vector (H. vitripennis), leading to very se- of vectors, vector control by biological agents and insec- rious outbreaks of PD in grapevine and also ALS and ticides is an important way to slow fast spread of the in- OLS, due to a much more efficient transmission of this sect, as is was performed in California after the intro- sharpshooter than local vectors. GWSS probably first duction of H. vitripennis. Egg parasitoids like Gonato- entered California as eggs in plants. The eggs are de- cerus sp. may be used, but their populations decrease posited into plant tissues. H. vitripennis is native to the strongly during winter when egg production of vectors southeast USA and northeast Mexico; it recent invaded is low and therefore the first generation vectors (which of California (USA) and Tahiti (Hoddle, 2004). It was is very important in disease transmission) usually is only first detected in southern California in 1989 (Sorensen slightly parasitized. Moreover the industrial production and Gill, 1996), and caused outbreaks of Pierce's dis- of parasitoids is not easy. Systemic insecticides, especial- ease in this state since 1997 with high incidences (25- ly neonicotinoids (imidacloprid), natural defence system 97% of the plants infected, although often initially enhancers (systemic acquired resistance or SAR), such symptomless). The risk of introduction of H. vitripennis as harpin, a protein from Erwinia amylovora and repel- for Europe can be formulated as follows: lents, such as kaolin, a formulation of aluminum silicate, (i) very broad host range, more than 70 plant species are used in vineyards but are only partly successful in 35 families including: avocado (Persea americana), cit- (Almeida et al., 2005; Tubajika et al., 2007). The use has rus, Macadamia, and many woody ornamentals (e.g.
been tried of genetically manipulated bacteria found in Fraxinus, Lagerstroemia, Rhus). For a full list of hosts the foregut of vectors and in xylem tissue of grape (as see http://edis.ifas.ufl.edu/in174. The adult stage is per- an endophyte), viz. Alcaligenes xylosoxidans subsp. deni- sistently infected by the bacterium, transmitting it trificans as an agent that blocks transmission of X. fas- throughout the whole life and disperses widely with tidiosa (Bextine et al., 2005), but its usefulness is ques- short hopping flights that enhance the spread of X. fas- tionable because the bacterium would mainly block sec- tidiosa (Blua and Morgan, 2003); ondary transmission (grape to grape), whereas primary (ii) risk of introduction with imported hosts (recent infection would originate from nongrape hosts that are introductions reported from California, Arizona, usually not reacting with symptoms or are non treatable.
French Polynesia, and Hawaii); (iii) efficient vector of X. fastidiosa to grapevine, al- 005_Janse_S35 9-09-2010 12:06 Pagina 45 Journal of Plant Pathology (2010), 92 (1, Supplement), S1.35-S1.48
Janse and Obradovic S1.45 mond, and oleander in California and of PPD and PLS be formulated as follows: in south-east USA; (i) bacterium irregularly distributed in host tissues (iv) highly mobile and widely distributed in various and sometimes difficult to detect, often occurring in a crops (Redak et al., 2004), although there is a relatively inefficient transmission of X. fastidiosa (Almeida and (ii) detection techniques are often not sensitive. As an example: direct PCR assays of grape and citrus 13% (v) precludes the culture of V. vinifera L. and V. labr- and 33% positive, Agar absorbent-PCR, 97% and usca L. in south-east USA and can inoculate dormant 100% positive for grape and citrus, respectively (Fatmi grapevines in winter (Almeida et al., 2005).
et al., 2005); In Central and South America X. fastidiosa has be- (iii) massive importations of wild grape rootstocks come very noxious due to the rapid expansion (most from America to Europe (Phylloxera-resistant) provide likely via distribution of infected planting material) of opportunity to introduce X. fastidiosa; CVC in Citrus, leading to more than a third of all trees (iv) wide range of (symptomless) hosts of X. fas- in the area having symptoms of CVC and CLC in cof- tidiosa should have allowed periodic introductions of the bacterium into Europe; For Europe there are until now only a few uncon- (v) many Cicadellidae transmit X. fastidiosa, includ- firmed records of X. fastidiosa on grapevine from Koso- ing some European species such as Cicadella viridis and vo [erroneously mentioned as Slovenia in my book Phy- P. spumarius (meadow spittle bug); tobacteriology, Principles and Practice (Janse, 2006)] (vi) it is unknown if in Europe there are vectors sur- and France. The finding of X. fastidiosa in grape materi- viving winter as adults, able to spread the disease once it al originating from Kosovo (Berisha et al., 1998) prompted Serbian authorities to do pest risk assess- (vii) vectors may overwinter unnoticed as adults in ment. Although the location of origin of tested material woods and weeds adjacent to vineyards. For instance, was not accessible, in 2005/06 the Serbian Ministry of G. atropunctata from riparian woods causes X. fastidiosa Agriculture carried out surveys of vineyards in the re- infections early in the spring in California (Purcell and gion neighbouring Kosovo. The purpose of this survey Saunders, 1999). Some spittlebugs vectors, not found was to collect plants showing symptoms resembling PD on grapevines, occur on herbs and shrubs nearby vine- and to detect X. fastidiosa in suspicious material. Sam- yards and alfalfa fields (DeLong and Severin, 1950).
pling was performed in late summer-early autumn and They may maintain inoculum in weed hosts; material was subjected to laboratory analysis according (viii) the apparent absence of X. fastidiosa in Europe to the detection procedure recommended by EPPO till now may be due to lack of vectors that overwinter as (EPPO, 2004). Results of this analysis showed no indi- adults that could establish early season infections (Pur- cation of X. fastidiosa presence in the tested samples (A.
cell, 1997), but due to recent climatic changes, the Obradovic, unpublished information). Mediterranean basin climatic conditions may be more Since X. fastidiosa has more that 150 hosts and for congenial to certain vectors than initially thought (Hod- many of them, including Vitis, planting material is im- ported, the risk of introduction (especially in latent (ix) cold winters may cure PD (demonstrated in pot- form) must not be underestimated. Absence of the dis- ted grapevines) (Purcell, 1980). Nevertheless, inoculum eases caused by X. fastidiosa will mainly be due to the sources important for epidemics to develop from pri- absence of suitable vectors. However, introduction of mary spread may build up unnoticed and will cause epi- the pathogen and vectors with plant material can not be demics when hosts, vectors and pathogen find the ideal excluded. Moreover also local Cicadellidae (see above) conditions. In California adjacent riparian woods, alfal- could become potential vectors. Due to its potential fa fields, and pastures serve as major reservoirs of X. fas- risks and absence in the region X. fastidiosa is on the A1 tidiosa (Hopkins and Purcell, 2002); Quarantine list of EPPO and H. vitripennis, which has a (x) in Central and South America X. fastidiosa has very large host range and feeds on almond, peach and become very noxious due to the rapid expansion (most plum, was recently put on the EPPO alert list. H. vit- likely via distribution of infected planting material) of ripennis could easily be introduced or perhaps has al- CVC in citrus.
ready been introduced via its many host plants (nursery As in the more northern parts of the USA, Vitis vari- productions, cut flowers, propagating material, fruits) eties in Europe are very susceptible to X. fastidiosa and into the EPPO region. Of course, it should be investi- this is really a risk when a vector would become estab- gated how much these and local vectors are adapted not lished that could survive the winters in South Europe only to transmission, but also to their new hosts and en- and would also establish in wild hosts (e.g. wild and do- vironments. Many known vectors do not play a substan- mestic plums and wild cherry are symptomless reser- tial role in disease outbreaks in certain crops (Redak et voirs in the USA) and cause spring infections that are al., 2004). Further risks of X. fastidiosa for Europe can most likely to persist over the years. The same risk holds 005_Janse_S35 9-09-2010 12:06 Pagina 46 S1.46 Xylella fastidiosa a threat for Europe? Journal of Plant Pathology (2010), 92 (1, Supplement), S1.35-S1.48
true for citrus (sweet oranges, mandarins, and tanger- Establishment of a genetically marked insect-derived sym- ines) and other hosts, such as almond, plum and peach biont in multiple host plants. Current Microbiology 50: 1-7.
that are widely grown in southeast and southwest Eu- Blake J.H., 1993. Distribution of Xylella fastidiosa in oak, rope, especially in the warmer Mediterranean basin, maple, and sycamore in South Carolina. Plant Disease 77:
where a disease-favourable combination of warm nights, regular rainfall/high humidity and long growing season Blua M.J., Morgan D.W.J., 2003. Dispersion of Homalodisca coagulata (Hemiptera: Cicadellidae), a vector of Xylella fas- In a computer simulation program (CLIMEX) study tidiosa, into vineyards in southern California. Journal of concerning climatic conditions and possibilities of Economic Entomology 96: 1369-1374.
spread of X. fastidiosa, Hoddle (2004) concluded: Brlansky R.H., Davis C.L., Timmer L.W., Howd D.S., Contr- ‘CLIMEX predicted that cold stress accumulation eras J., 1991. Xylem-limited bacteria in citrus from Ar-gentina with symptoms of citrus variegated chlorosis. Phy- would exclude Pierce's disease-causing strains of X. fas- topathology 81: 1210.
tidiosa from France and northern and central grape pro- Chang C.J., Garnier M., Zreik L., Rossetti V., Bové J.M., ducing areas of Spain and Italy. This result is incongru- 1993. Culture and serological detection of the xylem-limit- ous with Pierce's disease reports from Kosovo in the ed bacterium causing citrus variegated chlorosis and its Balkans and may suggest that cold-tolerant strains of X. identification as a strain of Xylella fastidiosa. Current Mi- fastidiosa that cause Pierce's disease exist which could crobiology 27: 137-142.
exhibit invasion potential and establish in areas of Eu- Chatterjee S., Almeida R.P.P, Lindow S., 2008. Living in two rope contrary to results reported here. When observing Worlds: The plant and insect lifestyles of Xylella fastidiosa.
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paring climatic conditions of those areas and California, Chen J., Su C.C., Chang C.J., 2006. Multigenic sequence com- especially with those of the Mediterranean basis, we are parison of Xylella fastidiosa pear leaf scorch strains from pretty sure that even without a possible change towards Taiwan to strains from Americas. Phytopathology 96: 23.
cold-tolerant strains (for which there is no evidence Crop Protection Compendium 2005. http://www.adbi.org/ yet), X. fastidiosa has too many chances for establishing itself in Europe and the Mediterranean basin.
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Progestin-only pills for contraception (Review) Grimes DA, Lopez LM, O'Brien PA, Raymond EG This is a reprint of a Cochrane review, prepared and maintained by The Cochrane Collaboration and published in The Cochrane Library2013, Issue 11 Progestin-only pills for contraception (Review)Copyright © 2013 The Cochrane Collaboration. Published by John Wiley & Sons, Ltd.
This leaflet provides information on azathioprine and will answer any questions you have about the treatment. Arthritis Research UK produce and print our booklets entirely from charitable donations. Azathioprine is a type of drug known as a disease-modifying anti-rheumatic drug, or DMARD. These drugs have the effect of dampening down the underlying disease process, rather than simply treating symptoms. Azathioprine reduces the activity of the immune system (the body's own defence system), so it's always used with care.