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Vector Transmission of Xylella Fastidiosa: Applying Fundamental Knowledge to Generate Disease Management Strategies

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Vector Transmission of Xylella Fastidiosa: Applying Fundamental Knowledge to Generate Disease Management Strategies SPECIAL FEATURE ON INSECT TRANSMISSION OF PLANT PATHOGENS Vector Transmission of Xylella fastidiosa: Applying Fundamental Knowledge to Generate Disease Management Strategies RODRIGO P. P. ALMEIDA,1 MATTHEW J. BLUA,2 JOA˜ O R. S. LOPES,3 4 AND ALEXANDER H. PURCELL Ann. Entomol. Soc. Am. 98(6): 775Ð786 (2005) ABSTRACT Xylella fastidiosa is a xylem-limited bacterium transmitted to plants by xylem sap- feeding insects. This pathogen has a wide host range, causing disease in crops such as grape, citrus, almond, and coffee; ornamental plants; and trees. Sharpshooter leafhoppers are the major vectors of X. fastidiosa to crops of economic importance. Transmission characteristics include the lack of a latent period, no transstadial or transovarial transmission, persistence in adults, and multiplication in the foregut of vectors. Various factors inßuence vector transmission of X. fastidiosa, including the distribution and density of bacterial populations in host plants, insect host range and plant preference, season of inoculation, and climatic conditions. The ecology of vectors can affect epidemics, as demonstrated by the large increase in PierceÕs disease of grapevine incidence in California after the introduction of Homalodisca coagulata (Say). Disease control strategies should incorporate basic knowledge of transmission biology, vector ecology, and other interactions involved in X. fastidiosa diseases. We discuss basic aspects of X. fastidiosa transmission by vectors, the ecology of insects in relation to transmission and disease spread, and how basic research can be applied to the development of management strategies for a X. fastidiosa disease. KEY WORDS Hemiptera, Cicadellidae, bacteria, plant disease, bioÞlm INSECTS THAT INGEST PRIMARILY xylem sap belong to four (Fig. 1). Epidemics of citrus variegated chlorosis families within the Hemiptera: Cicadellidae (subfam- (CVC) in Brazil and new outbreaks of PierceÕs disease ily Cicadellinae, sharpshooter leafhoppers), Cercopi- (PD) of grapevines in California driven by Homalo- dae (spittlebugs), Machaerotidae (tube-building disca coagulata (Say) (Blua et al. 1999, Hopkins and spittlebugs), and Cicadidae (cicadas). In general, Purcell 2002), and the availability of genome se- these insects cause little damage to plants. Some ci- quences of four strains of X. fastidiosa (Simpson et al. cadas can damage foliage or debilitate plants by suck- 2000; Bhattacharyya et al. 2002a,b; Van Sluys et al. ing signiÞcant amounts of xylem sap when large 2003), are among the major reasons for such emerging broods emerge, whereas spittlebugs can affect pasture interest. This recent research has rapidly advanced grasses or sugarcane. Sharpshooters rarely damage knowledge of X. fastidiosa biology and epidemiology. plants directly (Andersen et al. 2003) but are eco- Recent reviews evaluate various aspects of X. fastid- nomically important as vectors of the plant pathogenic iosa diseases, including genomics (Van Sluys et al. bacterium Xylella fastidiosa. Grape, almond, citrus, 2002), vector ecology and disease epidemiology coffee, peach, and many forest tree species are among (Redak et al. 2004), and case studies (Purcell and Feil a large list of economically important plants in which 2001, Hopkins and Purcell 2002). We focus this review X. fastidiosa induces disease (Purcell 1997). Many on X. fastidiosa transmission by vectors, the ecology of other agronomic, ornamental, and wild plants are also the interactions, and how this knowledge can be in- hosts of the pathogen, most without expressing symp- corporated into disease management strategies. toms (Hopkins and Purcell 2002). X. fastidiosa Transmission Characteristics. Initial Worldwide, research involving X. fastidiosa and its studies on PD in vineyards suggested that the diseaseÕs vectors has increased dramatically in recent years etiological agent was an insect-borne virus (Hewitt et al. 1946). After Newton PierceÕs observations in the late 1800s and the devastation caused by the disease to 1 Department of Plant and Environmental Protection Sciences, southern California vineyards (Pierce 1892), interest University of Hawaii at Manoa, Honolulu, HI 96822. 2 Department of Entomology, University of California, Riverside, in PD diminished until an outbreak of the disease in CA 92521. the Central Valley of California during the 1930s and 3 Departamento de Entomologia, Fitopatologia and Zoologia Agrõ´- early 1940s (Hewitt et al. 1949). Researchers during cola, ESALQ/Universidade de Sa˜o Paulo, SP, Piracicaba, SP 13418- the 1940s identiÞed sharpshooter leafhoppers and 900, Brazil. 4 Department of Environmental Science, Policy and Management, spittlebugs as vectors (Houston et al. 1947; Severin University of California, Berkeley, CA 94720. 1949, 1950). 0013-8746/05/0775Ð0786$04.00/0 ᭧ 2005 Entomological Society of America 776 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 98, no. 6 vector competency (Purcell and Finlay 1979). Longer access periods result in higher transmission efÞciency. X. fastidiosa is irregularly distributed in infected tis- sues (Hopkins 1989), thus longer plant access time may increase chances of the vector probing infected vessels. Because X. fastidiosa must attach to the fore- gut of vectors in a fast moving environment with ßuid speed of 5Ð10 cm/s (Purcell et al. 1979), longer access periods also can increase the number of cells ingested by the insect, and, proportionally, the opportunities for attachment to occur. By contrast, two other factors may be associated with the increase in inoculation efÞciencies over time. First, attached cells in the fore- gut would have more opportunities to detach from the cuticle and be inoculated into a susceptible vessel with Fig. 1. Number of publications retrieved after a ÔXylellaÕ term was used as a keyword to search the ISI Web of Knowl- longer access times relative to shorter ones. Second, it edge (Web of Science) database in December 2004. Solid may be that cells are frequently inoculated into plants, line (empty circles) represents number of hits with ÔTitleÕ but most die before proliferating and generating dis- only option selected; dashed line (solid squares) are results ease. The number of cells inoculated and the proba- for general ÔTopicÕ search. bility of establishment would increase with access time. Both factors could operate independently. The basis of the transmission mechanism may have some The identiÞcation of a group of vectors considered similarities with that of semipersistently transmitted xylem feeders suggested that the etiological agent was (foregut-borne) viruses (Nault 1997). limited to xylem, as was later demonstrated by exper- Vector Foregut and Its Relationship to Trans- imentally blocking vector transmission to xylem tis- mission. Sharpshooters have typical hemipteran sues with a metal foil barrier (Houston et al. 1947). mouthparts adapted for feeding on liquids. The max- Davis et al. (1978) identiÞed X. fastidiosa as the eti- illary stylets interlock to form parallel food and sali- ological agent of PD. Vector ability seems to require vary canals. The mandibular stylets surround and sup- only that the insect is a xylem sap-feeding specialist. port the maxillary stylets and cut through plant Although phloem and mesophyll feeders have been tissues during probing. The mouthpart morphology of tested for X. fastidiosa transmission to plants (Purcell H. coagulata has been described in detail previously 1980), including leafhopper species known to pene- (Leopold et al. 2003). Sap enters the stylets and is trate and ingest from xylem, e.g., Euscelidius variegatus transferred to the precibarium, a narrow tube con- (Kirschbaum) (Naito 1977), none of these insect necting the food canal to the cibarium (pumping groups transmitted the pathogen. In contrast, most chamber). The precibarial valve, located about mid- Cicadellinae species tested in sufÞcient numbers were way in the precibarium, opens to admit ingested sap proven to be vectors. Observations that X. fastidiosa and closes to prevent backßow while food is pumped has little, if any, species speciÞcity within xylem-feed- to the gut. Backus and McLean (1982, 1983) described ing specialists (Purcell 1989) suggest that distinctive the morphology of the precibarial valve and a likely probing behaviors or foregut morphological charac- ingestion mechanism. The precibarium canal contin- teristics shared by xylem feeders enable bacterial ues after the valve and ends in the cibarium. The transmission. cibarium connects the precibarium to the esophagus X. fastidiosa is unique in its transmission character- or true mouth. From the esophagus, food is pushed istics among vector-borne plant pathogens in that it through the cardiac/esophageal valve into the midgut. does not require a latent period yet is persistently Sap ingestion is regulated by the precibarial and transmitted. Severin (1949) showed that adult sharp- cardiac (esophageal) valves and the cibarium dilator shooters remained infective for long periods. How- musculature, which originates at the insect clypeus ever, the lack of transstadial transmission or a latent and inserts along a medial line distal to the elastic period (Purcell and Finlay 1979) strongly suggested cibarial diaphragm (Purcell et al. 1979). Contraction that the pathogen is inoculated into plants from the of the dilator muscle raises the diaphragm to create foregut of vectors, the cuticle of which is shed at each negative pressure in the cibarium chamber, sucking in molt. Although the bacterium multiplies
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