Insect Vectors and Current Management Strategies for Diseases Caused by Xylella fastidiosa in the Southern United States

Insect Vectors and Current Management Strategies for Diseases Caused by Xylella fastidiosa in the... Xylella fastidiosa is a bacterial plant pathogen that causes Pierce’s disease of grape, citrus variegated chlorosis, phony peach disease, alfalfa dwarf, and leaf scorch of plum, blueberry, and pecan in the southern United States. Xylella fastidiosa also causes almond leaf scorch and oleander leaf scorch. This bacterial plant pathogen is transmitted by xylem-feeding insects, including sharpshooters (Cicadellidae: Cicadellinae) and spittlebugs (Cercopidae). The following paper is a review of the plant diseases caused by X. fastidiosa, its insect vectors, and management strategies in the southern United States. Key words: Cicadellidae, Cercopidae, horticultural entomology, plant pathology, vector-borne pathogens–plant Xylella fastidiosa Wells et al. (1987) is a bacterial plant pathogen cause disease in white and red mulberry (Morus alba L. and that causes Pierce’s disease of grape, citrus variegated chlorosis, M. rubra L.) should be grouped as a new subspecies; they proposed phony peach disease, plum leaf scald, alfalfa dwarf, almond leaf the name Xylella fastidiosa subsp. morus. Pear leaf scorch caused by scorch, oleander leaf scorch, and leaf scorch of blueberry, pecan, X. fastidiosa occurs in Taiwan and based on sequence variability of and many shade trees. Common symptoms include leaf scorch, char- the 16S rRNA gene and 16S-23S ITS sequences, Su et al. (2012) pro- acterized by cell death beginning at the leaf margins and separated pose that strains causing pear leaf scorch in Taiwan may belong to a from healthy tissue by a chlorotic band. Although X. fastidiosa can new subspecies and should be studied further. Xylella fastidiosa that infect >100 plant species in almost 50 families, it is not pathogenic is genetically similar to the Xylella fastidiosa subsp. fastidiosa in- in all plant hosts (Schaad et al. 2004). Xylella fastidiosa is primarily fects grapevines in Taiwan (Su et al. 2013). Interestingly, Almeida transmitted from plant to plant by an insect vector (Purcell and and Nunney (2015) suggest that the isolates from Taiwan may be a Hopkins 1996). However, the bacterium can be transmitted via in- new species. Randall et al. (2009) proposed a new X. fastidiosa sub- fected scions or rootstock of pecan (Sanderlin and Melanson 2006, species tashke that causes scorching symptoms in chitalpa trees Sanderlin 2015), pruning shears (Krell et al. 2007), or propagation (Chitalpa tashkentensis Ellis and Wisura), which is a hybrid com- of infected grape cuttings (Robacker and Chang 1992). mon in New Mexico, Arizona, and California landscapes. However, Several subspecies of X. fastidiosa are infectious to one or several additional genetic typing is needed to fully support the recognition plant species and in some cases, inhabit the plant without causing of this new subspecies and to further study the isolates in Taiwan symptoms. For instance, the subspecies that causes disease in plum (Nunney et al. 2012, Retchless et al. 2014). Almeida and Nunney will not induce symptoms in grapevines (Schaad et al. 2004). Xylella (2015) provide insight into how diseases of X. fastidiosa have fastidiosa subsp. multiplex is responsible for disease in peach, plum, emerged, with an extensive review of genetics, plant hosts, and almond, elm, pigeon grape, sycamore, and other trees. Xylella fas- worldwide distribution. tidiosa subsp. pauca causes disease in citrus and coffee, whereas Pierce’s disease limits grape production in Texas and North subsp. fastidiosa causes disease in grape, alfalfa, almond, and Carolina (Myers et al. 2007, Mitchell et al. 2009). Pierce’s disease maples (Schaad et al. 2004). Finally, subsp. sandyi is associated with has been detected in vineyards across the state of Virginia and in disease in oleander, daylily, Jacaranda spp., and magnolia vineyards that had previously been considered low risk for the dis- (Schuenzel et al. 2005, Hernandez-Martinez et al. 2007). Nunney ease (Wallingford et al. 2007). Several cases have been reported in et al. (2014) provide evidence based on multilocus sequence typing Oklahoma (Smith et al. 2009), and a recent outbreak has occurred (i.e., sequencing seven different genes) that X. fastidiosa isolates that in New Mexico (Randall et al. 2007). Bacterial leaf scorch caused V C The Authors 2017. Published by Oxford University Press on behalf of Entomological Society of America. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unre- stricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. 1 Downloaded from https://academic.oup.com/jipm/article-abstract/8/1/12/3745634 by Ed 'DeepDyve' Gillespie user on 13 July 2018 2 Journal of Integrated Pest Management, 2017, Vol. 8, No. 1 by X. fastidiosa of southern highbush blueberry (Vaccinium corym- the esophagus and cibarium (Alves et al. 2008), and must be able to bosum L.) has been reported in Georgia (Chang et al. 2009). Xylella withstand the fast flow of xylem fluid being ingested by the insect fastidiosa subspecies are able to recombine genetically, which could (Silva et al. 2011). After attachment to the cuticle of the insect fore- lead to new pathogenic subspecies and pose a threat to agriculturally gut, bacterial titers increase and cells in the center of the colony be- important crops in the southern United States (Almeida and Nunney come attached at the pole of cell, which increases the absorption of 2015). nutrients (Killiny and Almeida 2009). Almeida and Purcell (2006) detected X. fastidiosa cells on the precibarium of the blue-green sharpshooter, Graphocephala atropunctata (Signoret), and found Historical Background of Xylella fastidiosa that colonization of the precibarium was important for successful in- oculation of the plant host with bacterial cells. Jackson et al. (2008) In the late 1800s, scorch-like symptoms on grape leaves and stunted studied the glassy-winged sharpshooter, Homalodisca vitripennis growth of peach and plum were observed in the United States, Mexico, and Argentina, yet a real connection was lacking among (Germar), and found that the size of the bacterial community within these plant maladies (Pierce 1892, Turner and Pollard 1959a, Chang the foregut of this vector does not increase or decrease the inocula- and Yonce 1987). The causal agent of leaf scorch and stunting in the tion rate of the bacteria. Plant variables may affect insect transmis- infected plants was thought to be a virus owing to the difficulty in sion. Daugherty et al. (2011) found that glassy-winged sharpshooter prefers to feed on healthy grapevines, or those that are infected but culturing and graft transmissibility of the pathogen (Turner and asymptomatic versus grapevines that are symptomatic for Pierce’s Pollard 1959a, Hopkins 1977). In the 1970s, a similar rickettsia-like disease. Further, Rashed et al. (2011) found that transmission effi- organism was found to be likely responsible for leaf scorch and ciency of glassy-winged sharpshooter was not affected by differing stunted growth in grape, peach, plum, almond, periwinkle, and al- falfa, based on morphological and serological tests (Goheen et al. grape cultivars or the titers of X. fastidiosa within petioles. 1973, Hopkins et al. 1973, Hopkins 1977, McCoy et al. 1978, Raju et al. 1981). Once suspected to be a virus, a rickettsia-like organism, Insect Inoculation a mycoplasma-like organism, and even a gram-positive bacterium Xylella fastidiosa gains entry into the plant via feeding by xylem- (Schaad et al. 2004), the pathogen was isolated from grape and feeding sharpshooters (Cicadellidae: Cicadellinae) and spittlebugs described as a gram-negative, aerobic, rod-shaped bacterium (Davis (Cercopidae). These insects have piercing–sucking mouthparts charac- et al. 1978). Wells et al. (1987) described the bacterium in great de- terized by mandibular and maxillary stylets that are sheathed by the la- tail and proposed the name, Xylella fastidiosa. Xylella fastidiosa be- bium. Xylem fluid is drawn up through the stylets into the longs to the widespread family Xanthomonadaceae, which contains precibarium, then to the cibarium (i.e., sucking pump) before finally one other plant pathogenic genus of bacteria, Xanthomonas. reaching the esophagus (Backus 1988). The precibarium is a narrow Xanthomonadaceae consists of gram-negative proteobacteria and canal that spans the insect head (Backus 1988), and is the site of bacter- contains 22 genera (Mhedbi-Hajri et al. 2011). ial attachment and colonization (Almeida and Purcell 2006). Purcell and Finlay (1979) studied Draeculacephala minerva Ball and Graphocephala atropunctata (Signoret) and reported a noncirculative Biology and Insect Transmission of X. fastidiosa transmission mechanism (i.e., pathogen is not internalized) that did not Bacterial Colonization of the Host Plant require a latent period (i.e., insects were able to transmit bacteria after a 1-h acquisition period). The noncirculative transmission mechanism Xylella fastidiosa colonizes and multiplies in plant xylem, which transports water throughout the plant and is composed of vessels of was supported further by their observation that insects lost the ability dead, lignified cells that are joined by bordered pits or channels. The to transmit bacteria after molting. Xylella fastidiosa is considered to be bordered pits have a membrane that restricts large objects from propagative, as it is able to reproduce within the insect vector foregut. passing (Newman et al. 2003). Xylella fastidiosa cells will attach to In fact, it is the only known insect-transmitted pathogen that is both the vessel wall and multiply, subsequently forming a biofilm that noncirculative and propagative (Backus et al. 2009). Basedonelectrical can eventually block the passage of water, causing leaf scorch penetration graph studies of H. vitripennis, Backus et al. (2009, 2015) proposed the “ingestion-(salivation and egestion)” hypothesis to ex- (Newman et al. 2003). Xylella fastidiosa has a wide host range. However, most plant plain pathogen transmission and characterized the glassy-winged hosts are not susceptible but support low populations with little in- sharpshooter as a “flying syringe” for X. fastidiosa.In thismodel,in- tervessel movement (Purcell and Saunders 1999). Host plants of sects acquire the bacterium via ingestion of bacteria-contaminated X. fastidiosa can be grouped into three general categories based on plant juices and inoculation of the plant occurs through a combination the fate of the bacteria within that host: propagative or nonpropaga- of both salivation and egestion. Sharpshooter saliva is secreted into the tive, systemic or nonsystemic, and pathological or nonpathological. plant (salivation) and then is quickly sucked back into the anterior fore- Xylella fastidiosa is able to multiply within a propagative host, gut, where the saliva passes forcefully over the bacterial biofilm owing move between xylem vessels in systemic hosts, and cause observable to actions of the precibarial valve and cibarium pump, dislodging the symptoms in a pathological plant host (Purcell and Saunders 1999). bacteria that are subsequently egested into the plant (Backus et al. 2012, 2015). Bacterial Colonization of Insect Foregut Insect Vectors of X. fastidiosa Xylella fastidiosa colonization differs between its plant host and in- sect vectors. In plants, X. fastidiosa attaches to the xylem vessel wall The primary vectors of X. fastidiosa are in the insect family, in any orientation and forms a matrix-enclosed community. In con- Cicadellidae (Order: Hemiptera). Two tribes within this family, trast, in insects, X. fastidiosa attaches in a polar arrangement to the Proconiini and Cicadellini, are known to be xylem feeders. Many cuticle of the foregut, forming a mat-like community species from both tribes are known vectors of X. fastidiosa (Newman et al. 2004). Colonies of X. fastidiosa inhabit the foregut (Redak et al. 2004), and four species of spittlebugs (Cercopidae) and of insect vectors, specifically, the longitudinal groove that leads to cicadas (Cicadidae) are able to transmit X. fastidiosa. In addition, it Downloaded from https://academic.oup.com/jipm/article-abstract/8/1/12/3745634 by Ed 'DeepDyve' Gillespie user on 13 July 2018 Journal of Integrated Pest Management, 2017, Vol. 8, No. 1 3 is speculated that xylem-feeding leafhoppers in other subfamilies introducing the transformed bacterial symbiont, Alcaligenes xylo- can potentially transmit the bacterium (Redak et al. 2004). soxidans var. denitrificans (S1Axd), into insect foreguts by way of All members of Cicadellidae (sharpshooters) have piercing–suck- insect feeding. The bacterial symbionts have been altered genetically ing mouthparts with specialized muscles that enable them to feed on to introduce antibiotics that specifically interfere with the pathogen- xylem fluid, which possesses negative pressure potential. Thus, icity of X. fastidiosa. sharpshooters have evolved larger muscles and, therefore, enlarged Emphasis has been placed on biological control of glassy-winged clypeal regions to house those muscles (Redak et al. 2004). In add- sharpshooter in California, where its economic impact as a disease ition, minimal nutrients are present in sap fluid, adding a nutritional vector is estimated at billions of dollars in damage to almonds, hurdle for sharpshooters. This fluid is limited in organic nutrients grape, and stone fruits (Son et al. 2012). Eggs of glassy-winged including nonessential amino acids. Sharpshooters have symbiotic sharpshooter are known to be parasitized by several species in the gut bacteria that aid in providing necessary nutrients. To enhance genus Gonatocerus (Hymenoptera: Mymaridae) (Triapitsyn et al. nutrient acquisition, glassy-winged sharpshooter uses the cosym- 2002). The most commonly released natural enemies are the egg bionts, Baummania and Bacteroidetes (Wu et al. 2006). Host plants parasitoids, Gonatocerus ashmeadi Girault, Gonatocerus trigutattus and distributions of insect vectors that have been implicated in the Girault, a few other Gonatocerus spp., and Anagrus epos Girault transmission of X. fastidiosa in the southern United States are sum- (Son et al. 2012). Of those released, G. ashmeadi and G. trigutattus marized in Table 1. were established successfully in California and both have significant Glassy-winged sharpshooter, H. vitripennis (Germar) (formerly potential to reduce numbers of H. vitripennis (Gutierrez et al. 2011, Homalodisca coagulata (Say)), is the most important vector of dis- Son et al. 2012). Pilkington et al. (2005) provide a thorough review eases caused by X. fastidiosa (Fig. 1). This large sharpshooter is na- of biological control of glassy-winged sharpshooter in California. In tive to the southeastern United States and northern Mexico, and has Florida, biological control of glassy-winged sharpshooter has spread to southern California (United States; Sorensen and Gill included evaluating the insect pathogenic fungus, Hirsutella sp. 1996), French Polynesia (Tahiti; Hoddle 2004), and Hawaii (United (Conklin and Mizell 2013). States; Almeida 2007). In California, glassy-winged sharpshooter transmits bacteria that cause Pierce’s disease of grapes and leaf scorch in almonds and oleander. In Texas and Florida, glassy- Diseases Caused by X. fastidiosa in the Southern winged sharpshooter is a major vector of the pathogen that causes United States Pierce’s disease, phony peach disease, and plum leaf scald. The abil- ity of H. vitripennis to transmit X. fastidiosa has been studied exten- Pierce’s Disease of Grape sively owing to its importance as a vector. Glassy-winged The earliest account of disease in grapes caused by X. fastidiosa sharpshooter is an inefficient vector of X. fastidiosa that causes occurred in the late 1800s and was referred to as California vine dis- phony peach disease (15%) compared with two species of compar- ease by N. B. Pierce (Pierce 1892). The cause of the disease was un- able size, Oncometopia orbona (F.) (Fig. 2) and Homalodisca inso- known. Pierce (1892) described symptoms of the disease and lita (Walker) (Turner and Pollard 1959a). Although glassy-winged variations seen in different grape varieties. Most diseased cultivars sharpshooter was not the most efficient vector of phony peach dis- showed characteristic symptoms of marginal leaf necrosis, separated ease, it was the most abundant vector in orchards (Turner and from the healthy leaf tissue by a yellow chlorotic band (Fig. 3). Not Pollard 1959a). In California, glassy-winged sharpshooter is less ef- all cultivars displayed the characteristic yellow banding (e.g., ficient at spreading X. fastidiosa that causes Pierce’s disease com- Riesling). Symptoms in grape canes appeared as distinct green areas pared with the native species, Graphocephala atropunctata (Say) owing to unequal hardening of stems (Fig. 4). Symptoms typically (Purcell and Finlay 1979, Almeida and Purcell 2003a). The success manifested in the fall (Pierce 1892). A third symptom known as at which glassy-winged sharpshooter spreads X. fastidiosa can be “matchsticks” is caused by premature defoliation of leaves, with the high owing to its ability to feed on and inoculate dormant woody petioles remaining attached to the vine (Fig. 5). Although first tissue, an increased ability to disperse, and its large number of plant described by a California specialist, Pierce’s disease was originally hosts (Almeida 2007, Almeida and Purcell 2003a, Blua and Morgan suspected to be native to the southeastern United States based on pres- 2003). Early investigators observed that glassy-winged sharpshooter ence of Pierce’s disease-tolerant wild grape varieties in that region feeds throughout mild winters and does not hibernate. When tem- (Purcell 1977). More recently, Nunney et al. (2010) provide evidence peratures are <9 C, the insects are unable to fly and drop to the that X. fastidiosa subsp. fastidiosa is native to Central America. Their ground. However, they are able to withstand overnight freezing tem- evidence relies mainly on lack of genetic variability of North peratures (Pollard and Kaloostian 1961). American strains of X. fastidiosa subsp. fastidiosa compared with In California, research in control methods for glassy-winged strains in Central America. It is highly probable that the subspecies sharpshooter has been extensive, including biological, chemical, and that causes Pierce’s disease was introduced into southern California mechanical methods. Insecticides that have been targeted include via the importation of coffee plants from Central America in the late those that reduce glassy-winged sharpshooter feeding, thereby mini- to mid-1800s. Alternatively, Pierce’s disease could have been intro- mizing the opportunity for acquisition and transmission (Bethke duced into Texas or Florida and subsequently spread to California et al. 2001). In California, the neonicotinoids imidacloprid and (Nunney et al 2010). dinotefuran are effective for glassy-winged sharpshooter control In Florida, 16th-century Spanish settlers attempted to plant (Byrne and Rosa 2008). Mechanical control methods include use of European grape cultivars (Vitis vinifera L.) based on success of na- a screen barrier to limit dispersal of glassy-winged sharpshooter into tive grape species (Vitis simpsonii Munson). However, all attempts vineyards. Blua et al. (2005) found that a barrier fastened from a to establish the exotic varieties failed owing to what investigators shade cloth 5 m in height deterred up to 70% of glassy-winged sharpshooter from crossing or even approaching the barrier. considered “degeneration” four centuries later. Investigators soon Ramirez et al. (2008) have used symbiotic control to reduce the abil- realized that symptoms described as “degeneration” in Florida were ity of glassy-winged sharpshooter to transmit X. fastidiosa by similar to those described for Pierce’s disease in California (Stoner Downloaded from https://academic.oup.com/jipm/article-abstract/8/1/12/3745634 by Ed 'DeepDyve' Gillespie user on 13 July 2018 4 Journal of Integrated Pest Management, 2017, Vol. 8, No. 1 Table 1. Insect vectors of X. fastidiosa in the southern United States a b Vector Disease(s) transmitted Observed Host and Food Plants Distribution Cicadellidae: Cicadellinae: Proconiini Homalodisca vitripennis Pierce’s disease (Crall and Stover Johnsongrass, sunflower, hollyhock, Southeastern United States, northern (Germar) 1957, Adlerz and Hopkins 1979); okra, lambsquarters, cotton, corn, Mexico, southern California (H. coagulata, H. triquetra ) Leaf scorch in almonds (Almeida cowpeas, oak, ash, silktree, crape- (United States) (Sorensen and Gill and Purcell 2003b), and oleander myrtle, elderberry, and peach 1996); French Polynesia (Tahiti) (Purcell and Saunders 1999); (Turner and Pollard 1959b) (Hoddle 2004); Hawaii (United Phony peach disease (Turner States) (Almeida 2007) 1949); Pecan bacterial leaf scorch (Sanderlin and Melanson 2010) Homalodisca insolita Pierce’s disease (Crall and Stover Texas millet, Johnsongrass and crab- Texas, Arizona, Georgia, Louisiana, (Walker) 1957); Phony peach (Turner and grass (Turner and Pollard 1959b); Missouri, Mississippi, Alabama, Pollard 1955); Pecan bacterial leaf southern sandbur (Tipping et al. Arkansas, Florida, North scorch (Sanderlin and Melanson 2004) Carolina, South Carolina, Mexico 2010) (Neilson 1968); Tennessee (Turner and Pollard 1959b); Virginia (Wallingford and Pfeiffer 2012) Paraulacizes irrorata (F.) Transmission has not been Virginia wildrye, tall thistle, horse- Southeastern and central United (Cicada irrorata, Aulacizes demonstrated weed, thistle, prickly lettuce, States and Mexico (Young 1968). irrorata)(Fig. 12) wholeleaf rosinweed, and culti- vated sorghum (Mason and Yonke 1971). Oncometopia nigricans Pierce’s disease (Adlerz and Hopkins Crapemyrtle (Triapitsyn et al. 2002); Florida and South America (Neilson (Walker) 1979); Phony peach (Turner and Texas millet and Johnsongrass 1968) (Proconia nigricans) Pollard 1959a); Citrus variegated (Tipping et al. 2004); The biology chlorosis (Brlansky et al. 2002) of this species has not been fully studied (Nielson 1968) Oncometopia orbona (F.) Pierce’s disease (Crall and Stover Ash, honeysuckle, Chickasaw plum, It is distributed throughout the east- (Oncometopia undata) 1957, Myers et al. 2007); Phony redbud, silktree, blackberry, sep- ern United States from Florida to peach (Turner 1949) ticweed, Dahlia, Johnsongrasss, Maryland and south from greenbrier, hibiscus, pokeweed, Missouri and Texas to northern sunflower, hollyhock, okra, lambs- Mexico (Neilson 1968, Turner quarters, ragweed, and peach and Pollard 1959b) (Turner and Pollard 1959b). Cicadellidae: Cicadellinae: Cicadellini Cuerna costalis (F.) Pierce’s disease (Kaloostian 1962); Bermudagrass, crabgrass, Southeastern United States with Phony peach (Turner 1949); Pecan Johnsongrass, Texas millet, cot- ranges extending from Texas to bacterial leaf scorch (Sanderlin ton, cowpea, sunflower, ragweed, New York (Nielson 1968). and Melanson 2010) and young peach trees (Turner and Pollard 1959b) Graphocephala versuta Say Pierce’s disease (Myers et al. 2007); Ragweed, sunflower, okra, plum, Southern United States ranging as far (Fig. 13) Phony peach (Turner 1949) and blackberry (Turner and north as Illinois and west to Texas Pollard 1959b) (Neilson 1968) Graphocephala coccinea Transmission has not been Blackberry, forsythia, cheesewood, Ontario, Canada, and in the United (Forster) demonstrated cup plant, wholeleaf rosinweed, States from Maine to Florida and rose, thistle, milkweed, goldenrod, west to California and Mexico and fragrant sumac (Young 1977) (Young 1977) Graphocephala hieroglyphica Pierce’s disease and alfalfa dwarf Willow, poplar, broad-leafed milk- Mississippi, Kansas, Texas, Arizona, (Say) (Frazier and Freitag 1946) weed, and great ragweed New Mexico, Illinois, Missouri, (Hackman 1922) Iowa, Nebraska, and Mexico (Hackman 1922) Xyphon flaviceps Riley Pierce’s disease, alfalfa dwarf (Stoner Bermudagrass (Neilson 1968); cot- Southeastern and midwestern United 1953) ton, cucumber, alfalfa, beebalm, States with ranges as far north as and prickly Russina thistle Wisconsin and west to New (Catanach et al. 2013) Mexico (Neilson 1968) Hemiptera: Cercopidae Clastoptera xanthocephala Transmission has not been Ragweed, sunflower, corn chamo- Eastern United States (Doering 1928) Germar (Fig. 14) demonstrated mile, chrysanthemum, grasses, many shrubs, and many trees (Doering 1942) Clastoptera achatina Germar Pecan bacterial leaf scorch (Sanderlin Maple, hickory, and pecan (Doering Eastern United States (Doering 1928) and Melanson 2010) 1942); basswood and hazelnut (Tedders 1995) (continued) Downloaded from https://academic.oup.com/jipm/article-abstract/8/1/12/3745634 by Ed 'DeepDyve' Gillespie user on 13 July 2018 Journal of Integrated Pest Management, 2017, Vol. 8, No. 1 5 Table 1. continued a b Vector Disease(s) transmitted Observed Host and Food Plants Distribution Lepyronia quadrangularis Pecan bacterial leaf scorch (Sanderlin Ragweed, horseweed, milkweed, Eastern United States (Doering 1922) (Say) and Melanson 2010) dandelion, coneflower, indian- hemp, lambsquarters, red mul- berry, black locust, and black raspberry (Doering 1922); maple (Doering 1942) Scientific names in parenthesis are synonyms, for more information on synonyms, keys, distribution records, plant hosts of leafhoppers refer to Dmitriev, D. A. 2003. 3I Interactive Keys and Taxonomical Databases. http://dmitriev.speciesfile.org/index.asp (accessed 6 April 2017). Johnsongrass, Sorghum halepense (L.) Pers.; sunflower, Helianthus annuus L.; hollyhock, Alcea L.; okra, Abelmoschus Medik.; lambsquarters, Chenopodium album L.; cotton, Gossypium L.; corn, Zea mays L.; cowpea, Vigna unguiculata (L.) Walp.; oak, Quercus L.; ash, Fraxinus L.; silktree, Albizia julibrissin Durazz.; crapemyrtle, Lagerstroemia indica L.; elderberry, Sambucus L.; peach, Prunus persica (L.) Batsch; Texas millet, Brachiaria texana (Buckley) Blake; crab- grass, Digitaria Haller; southern sandbur, Cenchrus echinatus L.; Virginia wildrye, Elymus virginicus L.; tall thistle, Cirsium altissimum (L.) Hill; horseweed, Conyza Less.; thistle, Cirsium sp.,; prickly lettuce, Lactuca serriola L; wholeleaf rosinweed, Silphium integrifolium Michx.; and cultivated sorghum, Sorghum Moench; honeysuckle, Lonicera L.; Chickasaw plum, Prunus angustifolia Marshall; redbud, Cercis L.; blackberry, Rubus L.; septicweed, Senna occidentalis (L.) Link; dahlia, Dahlia Cav.; greenbrier, Smilax L.; hibiscus, Hibiscus lunariifolius Willd.; pokeweed, Phytolacca L.; ragweed, Ambrosia L.; Bermudagrass, Cynodon dactylon (L.) Pers.; crabgrass, Digitaria Haller; plum, Prunus L.; forsythia, Forsythia Vahl; cheesewood, Pittosporum Banks ex Sol.; cup plant, Silphium perfoliatum L.; rose, Rosa L.; milkweed, Asclepias L.; goldenrod, Solidago L.; fragrant sumac, Rhus aromatic Aiton; willow, Salix L.; poplar, Populus alba L.; broad-leafed milkweed, Asclepias latifolia (Torr.) Raf.; and great ragweed, Ambrosia trifida L.; cucumber, Cucumis sativus L.; alfalfa, Medicago sativa L.; bee- balm, Monarda L.; prickly Russian thistle, Salsola tragus L.; corn chamomile, Anthemis arvensis L.; chrysanthemum, Chrysanthemum L.; maple, Acer L.; hickory, Carya Nutt.; hazelnut, Corylus L.; basswood, Tilia L; horseweed, Conyza Less.; dandelion, Taraxacum F. H. Wigg.; coneflower, Echinacea Moench; indianhemp, Apocynum cannabinum L.; black locust, Robinia pseudoacacia L.; black raspberry, Rubus occidentalis L. Incorrect identification by early investigators (Turner and Pollard 1959b). Fig. 1. Glassy-winged sharpshooter, Homalodisca vitripennis (Germar). Photo by Lisa Overall. Fig. 2. Female Oncometopia nigricans (Walker). Photo by Lisa Overall. 1953). At the time, the pathogen responsible for disease symptoms had yet to be identified. In the early 1940s, leafhoppers were identified as vectors of transmission studies, four species of sharpshooters were found to X. fastidiosa that causes Pierce’s disease and alfalfa dwarf in transmit X. fastidiosa subsp. fastidiosa in California— California (Hewitt et al. 1946). Initially, insects were the primary sus- Draeculacephala minerva Ball, Xyphon fulgida (Nott.), Helochara pects based on patterns of disease occurrence in alfalfa fields. From delta Oman, and Neokolla circullata (Baker) (Hewitt et al. 1946). Downloaded from https://academic.oup.com/jipm/article-abstract/8/1/12/3745634 by Ed 'DeepDyve' Gillespie user on 13 July 2018 6 Journal of Integrated Pest Management, 2017, Vol. 8, No. 1 Fig. 5. Symptom of Pierce’s disease known as “matchsticks,” which result Fig. 3. Foliar symptoms of Pierce’s disease. Photo by Lisa Overall. when petioles remain attached to the vine after leaf drop. Photo by Lisa Overall. of the fruit and juice produced (Walker et al. 2011). Another approach to developing Pierce’s disease-resistant grape cultivars involves genetic- ally engineering cultivars that express antimicrobial proteins that target and suppress X. fastidiosa subsp. fastidiosa (Dandekar et al. 2012). In addition to using resistant cultivars, resistant rootstocks have been eval- uated that could lessen symptoms of Pierce’s disease in desirable but more susceptible V. vinifera scion. In Florida, Ren and Lu (2002) found that using muscadine rootstocks with ‘Blanc du Bois’ scions reduced the development of both Pierce’s disease and anthracnose. In Texas, Cousins and Goolsby (2011) evaluated five different rootstocks used with scions of Chardonnay, which is susceptible to Pierce’s disease. These researchers found that Dog Ridge rootstocks grafted to Chardonnay scion exhibited more abundant vine growth and reduced symptoms of Pierce’s disease. Phony Peach Disease and Plum Leaf Scald Fig. 4. Green island (circled in yellow) typical of Pierce’s disease. Photo by Phony peach disease was observed initially in Georgia in the late Lisa Overall. 1800s and was thought to be caused by a virus. Twenty-five years after its first observation, the disease had spread to orchards in six Once the connection was made between Pierce’s disease in California counties in Georgia. Twenty years later the disease had spread to and “degeneration” of grapes in Florida, leafhoppers were identified Texas, Illinois, Kentucky, and North Carolina (Turner and Pollard as vectors of agents causing “degeneration” in Florida, and those 1959a). Xylella fastidiosa subsp. multiplex causes phony peach dis- identified include Oncometopia nigricans (Walker), H. vitripennis ease and plum leaf scald (Schaad et al. 2004). Symptomatic peach (Germar), and Xyphon flaviceps (Riley) (Adlerz and Hopkins 1979, trees tend to foliate and flower prematurely in the spring and defoli- Stoner 1953). In the 1990s, glassy-winged sharpshooter was intro- ate later in the fall than trees void of disease. Diseased trees produce duced into California (Sorensen and Gill 1996) and within 10 yr, less fruit that is usually much smaller than that of healthy trees and populations of glassy-winged sharpshooter had increased in vine- the fruit color from diseased trees is generally more intense (Fig. 6). yards, quickly spreading X. fastidiosa (Hopkins and Purcell 2002). Similar symptoms were observed in other Prunus spp., including Xylella fastidiosa subsp. fastidiosa is restricted to warmer climates wild plum and apricot (Turner and Pollard 1959a). Leaf scorching (Purcell 1997); however, warming trends seem to be contributing to its symptoms do not appear on peach foliage (Mizell et al. 2008). range expansion northward in the southeastern United States (Anas Early investigators noted that the pathogen could be spread et al. 2008). Ongoing programs are in place in all states to develop inte- through root grafts; therefore, it was suspected that a soil-dwelling grated pest management strategies. Efforts include insecticides that tar- arthropod could be responsible for spreading the pathogen and re- get leafhopper vectors (Krewer et al. 2002) and use of less virulent sulting in increased disease (Turner and Pollard 1959a). However, strains of X. fastidiosa (Hopkins 2005). Plant breeding programs have symptoms developed in the upper canopy of peach trees and sam- developed tolerant grape cultivars by incorporating resistance genes pling efforts were expanded to include sap-sucking insects. Fifty from grape cultivars that are native to the southeastern United States, years after first observing phony peach disease, several species of in- such as muscadine (Hopkins and Purcell 2002). Similar cultivars have sects in the family Cicadellidae were identified as vectors in Florida been planted in California, Texas, and Alabama, to evaluate the quality and South Carolina orchards, including H. vitripennis, O. orbona, Downloaded from https://academic.oup.com/jipm/article-abstract/8/1/12/3745634 by Ed 'DeepDyve' Gillespie user on 13 July 2018 Journal of Integrated Pest Management, 2017, Vol. 8, No. 1 7 Fig. 6. Phony peach disease symptoms. Photo courtesy of Chunxian Chen, Fig. 8. Blueberry leaf scorch. Photo courtesy of Phillip Brannen, University of USDA-ARS. Georgia. Fig. 7. Plum leaf scald. Photo courtesy of Chung-Jan Chang, University of Georgia. Cuerna costalis (F.), H. insolita, and Graphocephala versuta Say (Turner and Pollard 1959a, Kalkandelen and Fox 1968). Plum leaf scald is a serious disease of Japanese plums (Prunus salicinia Lindl.) in the southeastern United States and was reported initially in Argentina (Chang and Yonce 1987). Symptoms of plum leaf scald are similar to that seen with phony peach disease, with the addition of scorching symptoms on the foliage (Fig. 7). Furthermore, X. fastidiosa-infected plum trees are more susceptible to other plant pathogens and insect pests (Mizell et al. 2008). Symptoms of leaf scorching can be reduced with oxytetracycline trunk injections in Georgia (Chang et al. 1987). Fig. 9. Defoliated blueberry plant resulting from blueberry leaf scorch. Photo Currently, phony peach disease and plum leaf scald limit the life courtesy of Phillip Brannen, University of Georgia. of orchards in Florida. Controlling leafhopper vectors with insecti- cides is ineffective. However, removal of infected trees and eliminat- Bacterial Leaf Scorch of Blueberry ing reservoir hosts both within and near orchards are effective in Chang et al. (2009) observed disease in blueberry in Georgia and con- minimizing disease occurrence (Mizell et al. 2008). In northern firmed that the causative agent was X. fastidiosa. Symptoms of south- Georgia, rogueing of diseased peach trees and eliminating wild plums (Prunus americana Marshall) adjacent to orchards is an ef- ern highbush blueberries (Vaccinium corymbosum L.) include leaf fective management strategy. However, in southern Georgia, this scorch of older leaves (Fig. 8), thinner young shoots, fewer flower strategy has not been effective owing to higher disease incidence. buds, followed by eventual defoliation of the young twigs and stems Both plum leaf scald of Japanese plums and phony peach disease (Fig. 9). Symptoms were observed in individual twigs or on the whole limit the life of orchards in southern Georgia (Dutcher et al. 2005). plant, and infected plants died after defoliation (Chang et al. 2009). Downloaded from https://academic.oup.com/jipm/article-abstract/8/1/12/3745634 by Ed 'DeepDyve' Gillespie user on 13 July 2018 8 Journal of Integrated Pest Management, 2017, Vol. 8, No. 1 Fig. 10. Elm leaf scorch. Photo courtesy of Jen Olson, Oklahoma State University. In Louisiana, leaf scorch of rabbiteye blueberry (Vaccinium virgatum Aiton) reduced yield and fruit quality (Ferguson et al. 2016). Bacterial Fig. 11. Oak leaf scorch foliar symptoms. Photo by Lisa Overall. leaf scorch of blueberry is caused by X. fastidiosa subsp. multiplex (Nunney et al. 2013). In Georgia, blueberries generate more revenue than any other crop, and bacterial leaf scorch of blueberry poses signifi- cant risk to the blueberry market (Brannen et al. 2016). Currently, re- searchers are identifying blueberry cultivars that are less susceptible to X. fastidiosa (Chang et al. 2009). Bacterial Leaf Scorch of Shade Trees Since 1931, bacterial leaf scorch has been observed in American elm (Ulmus americanus L.) in the southeastern United States, which now occurs from the Gulf and mid-Atlantic states to as far north as Washington, D.C. (Sherald et al. 1994). Elm leaf scorch has been re- ported as far north as Ontario, Canada (Sherald 1999). In Oklahoma, bacterial leaf scorch caused by X. fastidiosa subsp. multiplex has been detected in American elm (Fig. 10), mulberry, red oak (Fig. 11), giant ragweed, and sycamore (Dominiak and Olsen 2006). Bacterial leaf scorch of sugar maple (Acer saccharum Marsh) and sweetgum (Liquidambar styraciflua L.) in Kentucky was caused by X. fastidiosa based on enzyme linked immunosorbent assay (ELISA) tests (Haartman and Jarlfors 1996). Other plants with bac- terial leaf scorch in Kentucky include oak species (burr, pin, red, and shingle) and sycamore (Haartman and Jarlfors 1996). In Washington, D.C., leaf scorch of white mulberry has been detected and found to be caused by X. fastidiosa. Based on serological tests, Kostka et al. (1986) concluded the mulberry strains of X. fastidiosa were more similar to strains that cause Pierce’s disease than those isolated from sycamore, elm, and oak. Most recently, strains that in- fect mulberry have been placed in a separate subspecies, X. fastid- iosa subsp. morus (Nunney et al. 2014). In the 1980s, sycamores (Platanus occidentalis L.) in South Carolina, Washington, D.C., Fig. 12. Paraulacizes irrorata (F.) (Hemiptera: Cicadellidae). Photo by Lisa Texas, and Louisiana were observed to have leaf scorch symptoms Overall. and tests confirmed the causal agent was X. fastidiosa (Haygood and Witcher 1988, Sherald et al. 1983). Symptoms of bacterial leaf scorch of shade trees are similar yet vary Management of bacterial leaf scorch of shade trees is difficult. The in the development of symptoms, depending on the species. pathogen may remain dormant in trees years before symptoms of bac- All symptoms typically manifest in late June to July and increase into terial leaf scorch appear. Tree injections of antibiotics can be costly and the fall (Sherald 2007). Symptoms of bacterial leaf scorch of mulberry can lead to damage. Current recommendations include maintaining include necrotic distal areas of the leaf, with a yellow chlorotic band tree health, rogueing trees with severe symptoms, and planting trees separating dead tissue from green leaf areas (Henneberger et al. 2004). less susceptible to X. fastidiosa (Gould and Lashomb 2007). Downloaded from https://academic.oup.com/jipm/article-abstract/8/1/12/3745634 by Ed 'DeepDyve' Gillespie user on 13 July 2018 Journal of Integrated Pest Management, 2017, Vol. 8, No. 1 9 follows the same pattern of symptom development. It is common to observe bare rachises with terminal leaflets remaining attached (Sanderlin and Heyderich-Alger 2000). Sanderlin and Heyderich- Alger (2003) found that defoliation of leaflets caused by pecan bac- terial leaf scorch decreased nut and kernel weight by 10–13% and 14–19%, respectively, and speculated that yield could decline sig- nificantly over time as bacteria migrate through the pecan tree. Sanderlin and Melanson (2010) verified insect transmission of bacterial leaf scorch from infected to uninfected pecan trees in the laboratory by the sharpshooters, H. vitripennis, H. insolita, and C. costalis, and the spittlebugs, Clastoptera achatina Germar and Lepyronia quadrangularis Say. Insecticide applications targeting spittlebug nymphs have potential to reduce the spread of X. fastid- iosa in pecan (Sanderlin and Melanson 2010). As pecan bacterial leaf scorch is transmissible from grafts of scion wood (Sanderlin 2005), pecan growers can treat scions with hot water to reduce dis- ease occurrence (Sanderlin and Melanson 2008). Sanderlin (2015) recommends using rootstocks that are less susceptible to X. fastid- iosa, and is currently working to identify these cultivars. Future Outlook Extensive research on X. fastidiosa has been completed in California Fig. 13. Graphocephala versuta Say (Hemiptera: Cicadellidae). Photo by Lisa Overall. where Pierce’s disease is now confined to southern grape-growing re- gions (refer to Bruening et al. (2014) for a thorough review of success- ful and current research). Although much has come from research in California, it is difficult to directly adapt and utilize those findings in growing systems in the southern United States. Except for glassy- winged sharpshooter, the primary insect vectors present in California grapevines and almond orchards are different species with different life histories than those found in the southern United States. Much research has been conducted to identify the insect vectors of X. fastidiosa in southern grapevines (Kaloostian et al. 1962, Buzombo et al. 2006, Myers et al. 2007, Lauzie `re et al. 2008, Villanueva et al. 2008, Mitchell et al. 2009, Morano et al. 2010, Wallingford and Pfeiffer 2012, Overall and Rebek 2015), peach orchards (Turner 1955, Turner and Pollard 1959b, Kalkandelen and Fox 1968, Anderson et al. 2008), pecan orchards (Sanderlin and Melanson 2010), citrus groves (Hall and Hunter 2008), and shade trees (Zhang et al. 2011, Overall and Rebek 2015). There is a need to study the spread of the pathogen by screening plant hosts for pathogenic and nonpathogenic infections of X. fastidiosa and cataloguing X. fastidiosa isolates using multilocus se- quence typing to track development of new subspecies and additionally catalogue X. fastidiosa isolates recovered from insect vectors (Almeida and Nunney 2015). Xylella fastidiosa has been detected in citrus in Florida (Hopkins et al. 1991); fortunately to date, X. fastidiosa subsp. pauca that causes citrus variegated chlorosis has not been detected in citrus in the United States. Quarantine protocols are in place in states that would be impacted negatively by this disease. Insect vectors should Fig. 14. Clastoptera xanthocephala Germar (Hemiptera: Cercopidae). Photo be surveyed in preexisting affected commodities and when new diseases by Lisa Overall. arise, such as blueberry leaf scorch. Understanding the presence and biology of vectors and alternate natural hosts of the pathogen will allow researchers to develop effective management strategies for plant Pecan Bacterial Leaf Scorch diseases associated with X. fastidiosa, at least in those commodities Bacterial leaf scorch of pecan (Carya illinoinensis (Wangenh.) K. where management is feasible. Koch) was observed for the first time in Louisiana in 1972, and was thought to be caused by a fungus until Sanderlin and Heyderich- Alger (2000) found that X. fastidiosa was the causative agent. Acknowledgments Symptoms of bacterial leaf scorch of pecan appear in June and pro- We thank Drs. Tom Royer and John Damicone, Department of Entomology and gressively increase into the fall. Marginal necrosis of the leaflets is Plant Pathology, Oklahoma State University, and two anonymous reviewers for typical beginning on the older leaflets at the basal portion of the ra- their careful review of this manuscript. We thank the investigators acknowledged chis and progressing toward younger leaflets. Leaflet abscission in figure captions for granting permission to use their images. This manuscript Downloaded from https://academic.oup.com/jipm/article-abstract/8/1/12/3745634 by Ed 'DeepDyve' Gillespie user on 13 July 2018 10 Journal of Integrated Pest Management, 2017, Vol. 8, No. 1 was prepared with support from the Oklahoma Cooperative Extension Service resistance. California Agriculture 68: 134–141. DOI: 10.3733/ and the Oklahoma Agricultural Experiment Station. ca.v068n04p134. Buzombo, P., J. Jaimes, V. Lam, K. Cantrell, M. Harkness, D. McCullough, and L. Morano. 2006. An American hybrid vineyard in the Texas Gulf References Cited Coast: Analysis within a Pierce’s disease hot zone. American Journal of Enology and Viticulture 57: 347–355. Adlerz, W. C., and D. L. Hopkins. 1979. Natural infectivity of two sharp- Byrne, B. W., and C. Rosa. 2008. 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Insect Vectors and Current Management Strategies for Diseases Caused by Xylella fastidiosa in the Southern United States

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Abstract

Xylella fastidiosa is a bacterial plant pathogen that causes Pierce’s disease of grape, citrus variegated chlorosis, phony peach disease, alfalfa dwarf, and leaf scorch of plum, blueberry, and pecan in the southern United States. Xylella fastidiosa also causes almond leaf scorch and oleander leaf scorch. This bacterial plant pathogen is transmitted by xylem-feeding insects, including sharpshooters (Cicadellidae: Cicadellinae) and spittlebugs (Cercopidae). The following paper is a review of the plant diseases caused by X. fastidiosa, its insect vectors, and management strategies in the southern United States. Key words: Cicadellidae, Cercopidae, horticultural entomology, plant pathology, vector-borne pathogens–plant Xylella fastidiosa Wells et al. (1987) is a bacterial plant pathogen cause disease in white and red mulberry (Morus alba L. and that causes Pierce’s disease of grape, citrus variegated chlorosis, M. rubra L.) should be grouped as a new subspecies; they proposed phony peach disease, plum leaf scald, alfalfa dwarf, almond leaf the name Xylella fastidiosa subsp. morus. Pear leaf scorch caused by scorch, oleander leaf scorch, and leaf scorch of blueberry, pecan, X. fastidiosa occurs in Taiwan and based on sequence variability of and many shade trees. Common symptoms include leaf scorch, char- the 16S rRNA gene and 16S-23S ITS sequences, Su et al. (2012) pro- acterized by cell death beginning at the leaf margins and separated pose that strains causing pear leaf scorch in Taiwan may belong to a from healthy tissue by a chlorotic band. Although X. fastidiosa can new subspecies and should be studied further. Xylella fastidiosa that infect >100 plant species in almost 50 families, it is not pathogenic is genetically similar to the Xylella fastidiosa subsp. fastidiosa in- in all plant hosts (Schaad et al. 2004). Xylella fastidiosa is primarily fects grapevines in Taiwan (Su et al. 2013). Interestingly, Almeida transmitted from plant to plant by an insect vector (Purcell and and Nunney (2015) suggest that the isolates from Taiwan may be a Hopkins 1996). However, the bacterium can be transmitted via in- new species. Randall et al. (2009) proposed a new X. fastidiosa sub- fected scions or rootstock of pecan (Sanderlin and Melanson 2006, species tashke that causes scorching symptoms in chitalpa trees Sanderlin 2015), pruning shears (Krell et al. 2007), or propagation (Chitalpa tashkentensis Ellis and Wisura), which is a hybrid com- of infected grape cuttings (Robacker and Chang 1992). mon in New Mexico, Arizona, and California landscapes. However, Several subspecies of X. fastidiosa are infectious to one or several additional genetic typing is needed to fully support the recognition plant species and in some cases, inhabit the plant without causing of this new subspecies and to further study the isolates in Taiwan symptoms. For instance, the subspecies that causes disease in plum (Nunney et al. 2012, Retchless et al. 2014). Almeida and Nunney will not induce symptoms in grapevines (Schaad et al. 2004). Xylella (2015) provide insight into how diseases of X. fastidiosa have fastidiosa subsp. multiplex is responsible for disease in peach, plum, emerged, with an extensive review of genetics, plant hosts, and almond, elm, pigeon grape, sycamore, and other trees. Xylella fas- worldwide distribution. tidiosa subsp. pauca causes disease in citrus and coffee, whereas Pierce’s disease limits grape production in Texas and North subsp. fastidiosa causes disease in grape, alfalfa, almond, and Carolina (Myers et al. 2007, Mitchell et al. 2009). Pierce’s disease maples (Schaad et al. 2004). Finally, subsp. sandyi is associated with has been detected in vineyards across the state of Virginia and in disease in oleander, daylily, Jacaranda spp., and magnolia vineyards that had previously been considered low risk for the dis- (Schuenzel et al. 2005, Hernandez-Martinez et al. 2007). Nunney ease (Wallingford et al. 2007). Several cases have been reported in et al. (2014) provide evidence based on multilocus sequence typing Oklahoma (Smith et al. 2009), and a recent outbreak has occurred (i.e., sequencing seven different genes) that X. fastidiosa isolates that in New Mexico (Randall et al. 2007). Bacterial leaf scorch caused V C The Authors 2017. Published by Oxford University Press on behalf of Entomological Society of America. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unre- stricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. 1 Downloaded from https://academic.oup.com/jipm/article-abstract/8/1/12/3745634 by Ed 'DeepDyve' Gillespie user on 13 July 2018 2 Journal of Integrated Pest Management, 2017, Vol. 8, No. 1 by X. fastidiosa of southern highbush blueberry (Vaccinium corym- the esophagus and cibarium (Alves et al. 2008), and must be able to bosum L.) has been reported in Georgia (Chang et al. 2009). Xylella withstand the fast flow of xylem fluid being ingested by the insect fastidiosa subspecies are able to recombine genetically, which could (Silva et al. 2011). After attachment to the cuticle of the insect fore- lead to new pathogenic subspecies and pose a threat to agriculturally gut, bacterial titers increase and cells in the center of the colony be- important crops in the southern United States (Almeida and Nunney come attached at the pole of cell, which increases the absorption of 2015). nutrients (Killiny and Almeida 2009). Almeida and Purcell (2006) detected X. fastidiosa cells on the precibarium of the blue-green sharpshooter, Graphocephala atropunctata (Signoret), and found Historical Background of Xylella fastidiosa that colonization of the precibarium was important for successful in- oculation of the plant host with bacterial cells. Jackson et al. (2008) In the late 1800s, scorch-like symptoms on grape leaves and stunted studied the glassy-winged sharpshooter, Homalodisca vitripennis growth of peach and plum were observed in the United States, Mexico, and Argentina, yet a real connection was lacking among (Germar), and found that the size of the bacterial community within these plant maladies (Pierce 1892, Turner and Pollard 1959a, Chang the foregut of this vector does not increase or decrease the inocula- and Yonce 1987). The causal agent of leaf scorch and stunting in the tion rate of the bacteria. Plant variables may affect insect transmis- infected plants was thought to be a virus owing to the difficulty in sion. Daugherty et al. (2011) found that glassy-winged sharpshooter prefers to feed on healthy grapevines, or those that are infected but culturing and graft transmissibility of the pathogen (Turner and asymptomatic versus grapevines that are symptomatic for Pierce’s Pollard 1959a, Hopkins 1977). In the 1970s, a similar rickettsia-like disease. Further, Rashed et al. (2011) found that transmission effi- organism was found to be likely responsible for leaf scorch and ciency of glassy-winged sharpshooter was not affected by differing stunted growth in grape, peach, plum, almond, periwinkle, and al- falfa, based on morphological and serological tests (Goheen et al. grape cultivars or the titers of X. fastidiosa within petioles. 1973, Hopkins et al. 1973, Hopkins 1977, McCoy et al. 1978, Raju et al. 1981). Once suspected to be a virus, a rickettsia-like organism, Insect Inoculation a mycoplasma-like organism, and even a gram-positive bacterium Xylella fastidiosa gains entry into the plant via feeding by xylem- (Schaad et al. 2004), the pathogen was isolated from grape and feeding sharpshooters (Cicadellidae: Cicadellinae) and spittlebugs described as a gram-negative, aerobic, rod-shaped bacterium (Davis (Cercopidae). These insects have piercing–sucking mouthparts charac- et al. 1978). Wells et al. (1987) described the bacterium in great de- terized by mandibular and maxillary stylets that are sheathed by the la- tail and proposed the name, Xylella fastidiosa. Xylella fastidiosa be- bium. Xylem fluid is drawn up through the stylets into the longs to the widespread family Xanthomonadaceae, which contains precibarium, then to the cibarium (i.e., sucking pump) before finally one other plant pathogenic genus of bacteria, Xanthomonas. reaching the esophagus (Backus 1988). The precibarium is a narrow Xanthomonadaceae consists of gram-negative proteobacteria and canal that spans the insect head (Backus 1988), and is the site of bacter- contains 22 genera (Mhedbi-Hajri et al. 2011). ial attachment and colonization (Almeida and Purcell 2006). Purcell and Finlay (1979) studied Draeculacephala minerva Ball and Graphocephala atropunctata (Signoret) and reported a noncirculative Biology and Insect Transmission of X. fastidiosa transmission mechanism (i.e., pathogen is not internalized) that did not Bacterial Colonization of the Host Plant require a latent period (i.e., insects were able to transmit bacteria after a 1-h acquisition period). The noncirculative transmission mechanism Xylella fastidiosa colonizes and multiplies in plant xylem, which transports water throughout the plant and is composed of vessels of was supported further by their observation that insects lost the ability dead, lignified cells that are joined by bordered pits or channels. The to transmit bacteria after molting. Xylella fastidiosa is considered to be bordered pits have a membrane that restricts large objects from propagative, as it is able to reproduce within the insect vector foregut. passing (Newman et al. 2003). Xylella fastidiosa cells will attach to In fact, it is the only known insect-transmitted pathogen that is both the vessel wall and multiply, subsequently forming a biofilm that noncirculative and propagative (Backus et al. 2009). Basedonelectrical can eventually block the passage of water, causing leaf scorch penetration graph studies of H. vitripennis, Backus et al. (2009, 2015) proposed the “ingestion-(salivation and egestion)” hypothesis to ex- (Newman et al. 2003). Xylella fastidiosa has a wide host range. However, most plant plain pathogen transmission and characterized the glassy-winged hosts are not susceptible but support low populations with little in- sharpshooter as a “flying syringe” for X. fastidiosa.In thismodel,in- tervessel movement (Purcell and Saunders 1999). Host plants of sects acquire the bacterium via ingestion of bacteria-contaminated X. fastidiosa can be grouped into three general categories based on plant juices and inoculation of the plant occurs through a combination the fate of the bacteria within that host: propagative or nonpropaga- of both salivation and egestion. Sharpshooter saliva is secreted into the tive, systemic or nonsystemic, and pathological or nonpathological. plant (salivation) and then is quickly sucked back into the anterior fore- Xylella fastidiosa is able to multiply within a propagative host, gut, where the saliva passes forcefully over the bacterial biofilm owing move between xylem vessels in systemic hosts, and cause observable to actions of the precibarial valve and cibarium pump, dislodging the symptoms in a pathological plant host (Purcell and Saunders 1999). bacteria that are subsequently egested into the plant (Backus et al. 2012, 2015). Bacterial Colonization of Insect Foregut Insect Vectors of X. fastidiosa Xylella fastidiosa colonization differs between its plant host and in- sect vectors. In plants, X. fastidiosa attaches to the xylem vessel wall The primary vectors of X. fastidiosa are in the insect family, in any orientation and forms a matrix-enclosed community. In con- Cicadellidae (Order: Hemiptera). Two tribes within this family, trast, in insects, X. fastidiosa attaches in a polar arrangement to the Proconiini and Cicadellini, are known to be xylem feeders. Many cuticle of the foregut, forming a mat-like community species from both tribes are known vectors of X. fastidiosa (Newman et al. 2004). Colonies of X. fastidiosa inhabit the foregut (Redak et al. 2004), and four species of spittlebugs (Cercopidae) and of insect vectors, specifically, the longitudinal groove that leads to cicadas (Cicadidae) are able to transmit X. fastidiosa. In addition, it Downloaded from https://academic.oup.com/jipm/article-abstract/8/1/12/3745634 by Ed 'DeepDyve' Gillespie user on 13 July 2018 Journal of Integrated Pest Management, 2017, Vol. 8, No. 1 3 is speculated that xylem-feeding leafhoppers in other subfamilies introducing the transformed bacterial symbiont, Alcaligenes xylo- can potentially transmit the bacterium (Redak et al. 2004). soxidans var. denitrificans (S1Axd), into insect foreguts by way of All members of Cicadellidae (sharpshooters) have piercing–suck- insect feeding. The bacterial symbionts have been altered genetically ing mouthparts with specialized muscles that enable them to feed on to introduce antibiotics that specifically interfere with the pathogen- xylem fluid, which possesses negative pressure potential. Thus, icity of X. fastidiosa. sharpshooters have evolved larger muscles and, therefore, enlarged Emphasis has been placed on biological control of glassy-winged clypeal regions to house those muscles (Redak et al. 2004). In add- sharpshooter in California, where its economic impact as a disease ition, minimal nutrients are present in sap fluid, adding a nutritional vector is estimated at billions of dollars in damage to almonds, hurdle for sharpshooters. This fluid is limited in organic nutrients grape, and stone fruits (Son et al. 2012). Eggs of glassy-winged including nonessential amino acids. Sharpshooters have symbiotic sharpshooter are known to be parasitized by several species in the gut bacteria that aid in providing necessary nutrients. To enhance genus Gonatocerus (Hymenoptera: Mymaridae) (Triapitsyn et al. nutrient acquisition, glassy-winged sharpshooter uses the cosym- 2002). The most commonly released natural enemies are the egg bionts, Baummania and Bacteroidetes (Wu et al. 2006). Host plants parasitoids, Gonatocerus ashmeadi Girault, Gonatocerus trigutattus and distributions of insect vectors that have been implicated in the Girault, a few other Gonatocerus spp., and Anagrus epos Girault transmission of X. fastidiosa in the southern United States are sum- (Son et al. 2012). Of those released, G. ashmeadi and G. trigutattus marized in Table 1. were established successfully in California and both have significant Glassy-winged sharpshooter, H. vitripennis (Germar) (formerly potential to reduce numbers of H. vitripennis (Gutierrez et al. 2011, Homalodisca coagulata (Say)), is the most important vector of dis- Son et al. 2012). Pilkington et al. (2005) provide a thorough review eases caused by X. fastidiosa (Fig. 1). This large sharpshooter is na- of biological control of glassy-winged sharpshooter in California. In tive to the southeastern United States and northern Mexico, and has Florida, biological control of glassy-winged sharpshooter has spread to southern California (United States; Sorensen and Gill included evaluating the insect pathogenic fungus, Hirsutella sp. 1996), French Polynesia (Tahiti; Hoddle 2004), and Hawaii (United (Conklin and Mizell 2013). States; Almeida 2007). In California, glassy-winged sharpshooter transmits bacteria that cause Pierce’s disease of grapes and leaf scorch in almonds and oleander. In Texas and Florida, glassy- Diseases Caused by X. fastidiosa in the Southern winged sharpshooter is a major vector of the pathogen that causes United States Pierce’s disease, phony peach disease, and plum leaf scald. The abil- ity of H. vitripennis to transmit X. fastidiosa has been studied exten- Pierce’s Disease of Grape sively owing to its importance as a vector. Glassy-winged The earliest account of disease in grapes caused by X. fastidiosa sharpshooter is an inefficient vector of X. fastidiosa that causes occurred in the late 1800s and was referred to as California vine dis- phony peach disease (15%) compared with two species of compar- ease by N. B. Pierce (Pierce 1892). The cause of the disease was un- able size, Oncometopia orbona (F.) (Fig. 2) and Homalodisca inso- known. Pierce (1892) described symptoms of the disease and lita (Walker) (Turner and Pollard 1959a). Although glassy-winged variations seen in different grape varieties. Most diseased cultivars sharpshooter was not the most efficient vector of phony peach dis- showed characteristic symptoms of marginal leaf necrosis, separated ease, it was the most abundant vector in orchards (Turner and from the healthy leaf tissue by a yellow chlorotic band (Fig. 3). Not Pollard 1959a). In California, glassy-winged sharpshooter is less ef- all cultivars displayed the characteristic yellow banding (e.g., ficient at spreading X. fastidiosa that causes Pierce’s disease com- Riesling). Symptoms in grape canes appeared as distinct green areas pared with the native species, Graphocephala atropunctata (Say) owing to unequal hardening of stems (Fig. 4). Symptoms typically (Purcell and Finlay 1979, Almeida and Purcell 2003a). The success manifested in the fall (Pierce 1892). A third symptom known as at which glassy-winged sharpshooter spreads X. fastidiosa can be “matchsticks” is caused by premature defoliation of leaves, with the high owing to its ability to feed on and inoculate dormant woody petioles remaining attached to the vine (Fig. 5). Although first tissue, an increased ability to disperse, and its large number of plant described by a California specialist, Pierce’s disease was originally hosts (Almeida 2007, Almeida and Purcell 2003a, Blua and Morgan suspected to be native to the southeastern United States based on pres- 2003). Early investigators observed that glassy-winged sharpshooter ence of Pierce’s disease-tolerant wild grape varieties in that region feeds throughout mild winters and does not hibernate. When tem- (Purcell 1977). More recently, Nunney et al. (2010) provide evidence peratures are <9 C, the insects are unable to fly and drop to the that X. fastidiosa subsp. fastidiosa is native to Central America. Their ground. However, they are able to withstand overnight freezing tem- evidence relies mainly on lack of genetic variability of North peratures (Pollard and Kaloostian 1961). American strains of X. fastidiosa subsp. fastidiosa compared with In California, research in control methods for glassy-winged strains in Central America. It is highly probable that the subspecies sharpshooter has been extensive, including biological, chemical, and that causes Pierce’s disease was introduced into southern California mechanical methods. Insecticides that have been targeted include via the importation of coffee plants from Central America in the late those that reduce glassy-winged sharpshooter feeding, thereby mini- to mid-1800s. Alternatively, Pierce’s disease could have been intro- mizing the opportunity for acquisition and transmission (Bethke duced into Texas or Florida and subsequently spread to California et al. 2001). In California, the neonicotinoids imidacloprid and (Nunney et al 2010). dinotefuran are effective for glassy-winged sharpshooter control In Florida, 16th-century Spanish settlers attempted to plant (Byrne and Rosa 2008). Mechanical control methods include use of European grape cultivars (Vitis vinifera L.) based on success of na- a screen barrier to limit dispersal of glassy-winged sharpshooter into tive grape species (Vitis simpsonii Munson). However, all attempts vineyards. Blua et al. (2005) found that a barrier fastened from a to establish the exotic varieties failed owing to what investigators shade cloth 5 m in height deterred up to 70% of glassy-winged sharpshooter from crossing or even approaching the barrier. considered “degeneration” four centuries later. Investigators soon Ramirez et al. (2008) have used symbiotic control to reduce the abil- realized that symptoms described as “degeneration” in Florida were ity of glassy-winged sharpshooter to transmit X. fastidiosa by similar to those described for Pierce’s disease in California (Stoner Downloaded from https://academic.oup.com/jipm/article-abstract/8/1/12/3745634 by Ed 'DeepDyve' Gillespie user on 13 July 2018 4 Journal of Integrated Pest Management, 2017, Vol. 8, No. 1 Table 1. Insect vectors of X. fastidiosa in the southern United States a b Vector Disease(s) transmitted Observed Host and Food Plants Distribution Cicadellidae: Cicadellinae: Proconiini Homalodisca vitripennis Pierce’s disease (Crall and Stover Johnsongrass, sunflower, hollyhock, Southeastern United States, northern (Germar) 1957, Adlerz and Hopkins 1979); okra, lambsquarters, cotton, corn, Mexico, southern California (H. coagulata, H. triquetra ) Leaf scorch in almonds (Almeida cowpeas, oak, ash, silktree, crape- (United States) (Sorensen and Gill and Purcell 2003b), and oleander myrtle, elderberry, and peach 1996); French Polynesia (Tahiti) (Purcell and Saunders 1999); (Turner and Pollard 1959b) (Hoddle 2004); Hawaii (United Phony peach disease (Turner States) (Almeida 2007) 1949); Pecan bacterial leaf scorch (Sanderlin and Melanson 2010) Homalodisca insolita Pierce’s disease (Crall and Stover Texas millet, Johnsongrass and crab- Texas, Arizona, Georgia, Louisiana, (Walker) 1957); Phony peach (Turner and grass (Turner and Pollard 1959b); Missouri, Mississippi, Alabama, Pollard 1955); Pecan bacterial leaf southern sandbur (Tipping et al. Arkansas, Florida, North scorch (Sanderlin and Melanson 2004) Carolina, South Carolina, Mexico 2010) (Neilson 1968); Tennessee (Turner and Pollard 1959b); Virginia (Wallingford and Pfeiffer 2012) Paraulacizes irrorata (F.) Transmission has not been Virginia wildrye, tall thistle, horse- Southeastern and central United (Cicada irrorata, Aulacizes demonstrated weed, thistle, prickly lettuce, States and Mexico (Young 1968). irrorata)(Fig. 12) wholeleaf rosinweed, and culti- vated sorghum (Mason and Yonke 1971). Oncometopia nigricans Pierce’s disease (Adlerz and Hopkins Crapemyrtle (Triapitsyn et al. 2002); Florida and South America (Neilson (Walker) 1979); Phony peach (Turner and Texas millet and Johnsongrass 1968) (Proconia nigricans) Pollard 1959a); Citrus variegated (Tipping et al. 2004); The biology chlorosis (Brlansky et al. 2002) of this species has not been fully studied (Nielson 1968) Oncometopia orbona (F.) Pierce’s disease (Crall and Stover Ash, honeysuckle, Chickasaw plum, It is distributed throughout the east- (Oncometopia undata) 1957, Myers et al. 2007); Phony redbud, silktree, blackberry, sep- ern United States from Florida to peach (Turner 1949) ticweed, Dahlia, Johnsongrasss, Maryland and south from greenbrier, hibiscus, pokeweed, Missouri and Texas to northern sunflower, hollyhock, okra, lambs- Mexico (Neilson 1968, Turner quarters, ragweed, and peach and Pollard 1959b) (Turner and Pollard 1959b). Cicadellidae: Cicadellinae: Cicadellini Cuerna costalis (F.) Pierce’s disease (Kaloostian 1962); Bermudagrass, crabgrass, Southeastern United States with Phony peach (Turner 1949); Pecan Johnsongrass, Texas millet, cot- ranges extending from Texas to bacterial leaf scorch (Sanderlin ton, cowpea, sunflower, ragweed, New York (Nielson 1968). and Melanson 2010) and young peach trees (Turner and Pollard 1959b) Graphocephala versuta Say Pierce’s disease (Myers et al. 2007); Ragweed, sunflower, okra, plum, Southern United States ranging as far (Fig. 13) Phony peach (Turner 1949) and blackberry (Turner and north as Illinois and west to Texas Pollard 1959b) (Neilson 1968) Graphocephala coccinea Transmission has not been Blackberry, forsythia, cheesewood, Ontario, Canada, and in the United (Forster) demonstrated cup plant, wholeleaf rosinweed, States from Maine to Florida and rose, thistle, milkweed, goldenrod, west to California and Mexico and fragrant sumac (Young 1977) (Young 1977) Graphocephala hieroglyphica Pierce’s disease and alfalfa dwarf Willow, poplar, broad-leafed milk- Mississippi, Kansas, Texas, Arizona, (Say) (Frazier and Freitag 1946) weed, and great ragweed New Mexico, Illinois, Missouri, (Hackman 1922) Iowa, Nebraska, and Mexico (Hackman 1922) Xyphon flaviceps Riley Pierce’s disease, alfalfa dwarf (Stoner Bermudagrass (Neilson 1968); cot- Southeastern and midwestern United 1953) ton, cucumber, alfalfa, beebalm, States with ranges as far north as and prickly Russina thistle Wisconsin and west to New (Catanach et al. 2013) Mexico (Neilson 1968) Hemiptera: Cercopidae Clastoptera xanthocephala Transmission has not been Ragweed, sunflower, corn chamo- Eastern United States (Doering 1928) Germar (Fig. 14) demonstrated mile, chrysanthemum, grasses, many shrubs, and many trees (Doering 1942) Clastoptera achatina Germar Pecan bacterial leaf scorch (Sanderlin Maple, hickory, and pecan (Doering Eastern United States (Doering 1928) and Melanson 2010) 1942); basswood and hazelnut (Tedders 1995) (continued) Downloaded from https://academic.oup.com/jipm/article-abstract/8/1/12/3745634 by Ed 'DeepDyve' Gillespie user on 13 July 2018 Journal of Integrated Pest Management, 2017, Vol. 8, No. 1 5 Table 1. continued a b Vector Disease(s) transmitted Observed Host and Food Plants Distribution Lepyronia quadrangularis Pecan bacterial leaf scorch (Sanderlin Ragweed, horseweed, milkweed, Eastern United States (Doering 1922) (Say) and Melanson 2010) dandelion, coneflower, indian- hemp, lambsquarters, red mul- berry, black locust, and black raspberry (Doering 1922); maple (Doering 1942) Scientific names in parenthesis are synonyms, for more information on synonyms, keys, distribution records, plant hosts of leafhoppers refer to Dmitriev, D. A. 2003. 3I Interactive Keys and Taxonomical Databases. http://dmitriev.speciesfile.org/index.asp (accessed 6 April 2017). Johnsongrass, Sorghum halepense (L.) Pers.; sunflower, Helianthus annuus L.; hollyhock, Alcea L.; okra, Abelmoschus Medik.; lambsquarters, Chenopodium album L.; cotton, Gossypium L.; corn, Zea mays L.; cowpea, Vigna unguiculata (L.) Walp.; oak, Quercus L.; ash, Fraxinus L.; silktree, Albizia julibrissin Durazz.; crapemyrtle, Lagerstroemia indica L.; elderberry, Sambucus L.; peach, Prunus persica (L.) Batsch; Texas millet, Brachiaria texana (Buckley) Blake; crab- grass, Digitaria Haller; southern sandbur, Cenchrus echinatus L.; Virginia wildrye, Elymus virginicus L.; tall thistle, Cirsium altissimum (L.) Hill; horseweed, Conyza Less.; thistle, Cirsium sp.,; prickly lettuce, Lactuca serriola L; wholeleaf rosinweed, Silphium integrifolium Michx.; and cultivated sorghum, Sorghum Moench; honeysuckle, Lonicera L.; Chickasaw plum, Prunus angustifolia Marshall; redbud, Cercis L.; blackberry, Rubus L.; septicweed, Senna occidentalis (L.) Link; dahlia, Dahlia Cav.; greenbrier, Smilax L.; hibiscus, Hibiscus lunariifolius Willd.; pokeweed, Phytolacca L.; ragweed, Ambrosia L.; Bermudagrass, Cynodon dactylon (L.) Pers.; crabgrass, Digitaria Haller; plum, Prunus L.; forsythia, Forsythia Vahl; cheesewood, Pittosporum Banks ex Sol.; cup plant, Silphium perfoliatum L.; rose, Rosa L.; milkweed, Asclepias L.; goldenrod, Solidago L.; fragrant sumac, Rhus aromatic Aiton; willow, Salix L.; poplar, Populus alba L.; broad-leafed milkweed, Asclepias latifolia (Torr.) Raf.; and great ragweed, Ambrosia trifida L.; cucumber, Cucumis sativus L.; alfalfa, Medicago sativa L.; bee- balm, Monarda L.; prickly Russian thistle, Salsola tragus L.; corn chamomile, Anthemis arvensis L.; chrysanthemum, Chrysanthemum L.; maple, Acer L.; hickory, Carya Nutt.; hazelnut, Corylus L.; basswood, Tilia L; horseweed, Conyza Less.; dandelion, Taraxacum F. H. Wigg.; coneflower, Echinacea Moench; indianhemp, Apocynum cannabinum L.; black locust, Robinia pseudoacacia L.; black raspberry, Rubus occidentalis L. Incorrect identification by early investigators (Turner and Pollard 1959b). Fig. 1. Glassy-winged sharpshooter, Homalodisca vitripennis (Germar). Photo by Lisa Overall. Fig. 2. Female Oncometopia nigricans (Walker). Photo by Lisa Overall. 1953). At the time, the pathogen responsible for disease symptoms had yet to be identified. In the early 1940s, leafhoppers were identified as vectors of transmission studies, four species of sharpshooters were found to X. fastidiosa that causes Pierce’s disease and alfalfa dwarf in transmit X. fastidiosa subsp. fastidiosa in California— California (Hewitt et al. 1946). Initially, insects were the primary sus- Draeculacephala minerva Ball, Xyphon fulgida (Nott.), Helochara pects based on patterns of disease occurrence in alfalfa fields. From delta Oman, and Neokolla circullata (Baker) (Hewitt et al. 1946). Downloaded from https://academic.oup.com/jipm/article-abstract/8/1/12/3745634 by Ed 'DeepDyve' Gillespie user on 13 July 2018 6 Journal of Integrated Pest Management, 2017, Vol. 8, No. 1 Fig. 5. Symptom of Pierce’s disease known as “matchsticks,” which result Fig. 3. Foliar symptoms of Pierce’s disease. Photo by Lisa Overall. when petioles remain attached to the vine after leaf drop. Photo by Lisa Overall. of the fruit and juice produced (Walker et al. 2011). Another approach to developing Pierce’s disease-resistant grape cultivars involves genetic- ally engineering cultivars that express antimicrobial proteins that target and suppress X. fastidiosa subsp. fastidiosa (Dandekar et al. 2012). In addition to using resistant cultivars, resistant rootstocks have been eval- uated that could lessen symptoms of Pierce’s disease in desirable but more susceptible V. vinifera scion. In Florida, Ren and Lu (2002) found that using muscadine rootstocks with ‘Blanc du Bois’ scions reduced the development of both Pierce’s disease and anthracnose. In Texas, Cousins and Goolsby (2011) evaluated five different rootstocks used with scions of Chardonnay, which is susceptible to Pierce’s disease. These researchers found that Dog Ridge rootstocks grafted to Chardonnay scion exhibited more abundant vine growth and reduced symptoms of Pierce’s disease. Phony Peach Disease and Plum Leaf Scald Fig. 4. Green island (circled in yellow) typical of Pierce’s disease. Photo by Phony peach disease was observed initially in Georgia in the late Lisa Overall. 1800s and was thought to be caused by a virus. Twenty-five years after its first observation, the disease had spread to orchards in six Once the connection was made between Pierce’s disease in California counties in Georgia. Twenty years later the disease had spread to and “degeneration” of grapes in Florida, leafhoppers were identified Texas, Illinois, Kentucky, and North Carolina (Turner and Pollard as vectors of agents causing “degeneration” in Florida, and those 1959a). Xylella fastidiosa subsp. multiplex causes phony peach dis- identified include Oncometopia nigricans (Walker), H. vitripennis ease and plum leaf scald (Schaad et al. 2004). Symptomatic peach (Germar), and Xyphon flaviceps (Riley) (Adlerz and Hopkins 1979, trees tend to foliate and flower prematurely in the spring and defoli- Stoner 1953). In the 1990s, glassy-winged sharpshooter was intro- ate later in the fall than trees void of disease. Diseased trees produce duced into California (Sorensen and Gill 1996) and within 10 yr, less fruit that is usually much smaller than that of healthy trees and populations of glassy-winged sharpshooter had increased in vine- the fruit color from diseased trees is generally more intense (Fig. 6). yards, quickly spreading X. fastidiosa (Hopkins and Purcell 2002). Similar symptoms were observed in other Prunus spp., including Xylella fastidiosa subsp. fastidiosa is restricted to warmer climates wild plum and apricot (Turner and Pollard 1959a). Leaf scorching (Purcell 1997); however, warming trends seem to be contributing to its symptoms do not appear on peach foliage (Mizell et al. 2008). range expansion northward in the southeastern United States (Anas Early investigators noted that the pathogen could be spread et al. 2008). Ongoing programs are in place in all states to develop inte- through root grafts; therefore, it was suspected that a soil-dwelling grated pest management strategies. Efforts include insecticides that tar- arthropod could be responsible for spreading the pathogen and re- get leafhopper vectors (Krewer et al. 2002) and use of less virulent sulting in increased disease (Turner and Pollard 1959a). However, strains of X. fastidiosa (Hopkins 2005). Plant breeding programs have symptoms developed in the upper canopy of peach trees and sam- developed tolerant grape cultivars by incorporating resistance genes pling efforts were expanded to include sap-sucking insects. Fifty from grape cultivars that are native to the southeastern United States, years after first observing phony peach disease, several species of in- such as muscadine (Hopkins and Purcell 2002). Similar cultivars have sects in the family Cicadellidae were identified as vectors in Florida been planted in California, Texas, and Alabama, to evaluate the quality and South Carolina orchards, including H. vitripennis, O. orbona, Downloaded from https://academic.oup.com/jipm/article-abstract/8/1/12/3745634 by Ed 'DeepDyve' Gillespie user on 13 July 2018 Journal of Integrated Pest Management, 2017, Vol. 8, No. 1 7 Fig. 6. Phony peach disease symptoms. Photo courtesy of Chunxian Chen, Fig. 8. Blueberry leaf scorch. Photo courtesy of Phillip Brannen, University of USDA-ARS. Georgia. Fig. 7. Plum leaf scald. Photo courtesy of Chung-Jan Chang, University of Georgia. Cuerna costalis (F.), H. insolita, and Graphocephala versuta Say (Turner and Pollard 1959a, Kalkandelen and Fox 1968). Plum leaf scald is a serious disease of Japanese plums (Prunus salicinia Lindl.) in the southeastern United States and was reported initially in Argentina (Chang and Yonce 1987). Symptoms of plum leaf scald are similar to that seen with phony peach disease, with the addition of scorching symptoms on the foliage (Fig. 7). Furthermore, X. fastidiosa-infected plum trees are more susceptible to other plant pathogens and insect pests (Mizell et al. 2008). Symptoms of leaf scorching can be reduced with oxytetracycline trunk injections in Georgia (Chang et al. 1987). Fig. 9. Defoliated blueberry plant resulting from blueberry leaf scorch. Photo Currently, phony peach disease and plum leaf scald limit the life courtesy of Phillip Brannen, University of Georgia. of orchards in Florida. Controlling leafhopper vectors with insecti- cides is ineffective. However, removal of infected trees and eliminat- Bacterial Leaf Scorch of Blueberry ing reservoir hosts both within and near orchards are effective in Chang et al. (2009) observed disease in blueberry in Georgia and con- minimizing disease occurrence (Mizell et al. 2008). In northern firmed that the causative agent was X. fastidiosa. Symptoms of south- Georgia, rogueing of diseased peach trees and eliminating wild plums (Prunus americana Marshall) adjacent to orchards is an ef- ern highbush blueberries (Vaccinium corymbosum L.) include leaf fective management strategy. However, in southern Georgia, this scorch of older leaves (Fig. 8), thinner young shoots, fewer flower strategy has not been effective owing to higher disease incidence. buds, followed by eventual defoliation of the young twigs and stems Both plum leaf scald of Japanese plums and phony peach disease (Fig. 9). Symptoms were observed in individual twigs or on the whole limit the life of orchards in southern Georgia (Dutcher et al. 2005). plant, and infected plants died after defoliation (Chang et al. 2009). Downloaded from https://academic.oup.com/jipm/article-abstract/8/1/12/3745634 by Ed 'DeepDyve' Gillespie user on 13 July 2018 8 Journal of Integrated Pest Management, 2017, Vol. 8, No. 1 Fig. 10. Elm leaf scorch. Photo courtesy of Jen Olson, Oklahoma State University. In Louisiana, leaf scorch of rabbiteye blueberry (Vaccinium virgatum Aiton) reduced yield and fruit quality (Ferguson et al. 2016). Bacterial Fig. 11. Oak leaf scorch foliar symptoms. Photo by Lisa Overall. leaf scorch of blueberry is caused by X. fastidiosa subsp. multiplex (Nunney et al. 2013). In Georgia, blueberries generate more revenue than any other crop, and bacterial leaf scorch of blueberry poses signifi- cant risk to the blueberry market (Brannen et al. 2016). Currently, re- searchers are identifying blueberry cultivars that are less susceptible to X. fastidiosa (Chang et al. 2009). Bacterial Leaf Scorch of Shade Trees Since 1931, bacterial leaf scorch has been observed in American elm (Ulmus americanus L.) in the southeastern United States, which now occurs from the Gulf and mid-Atlantic states to as far north as Washington, D.C. (Sherald et al. 1994). Elm leaf scorch has been re- ported as far north as Ontario, Canada (Sherald 1999). In Oklahoma, bacterial leaf scorch caused by X. fastidiosa subsp. multiplex has been detected in American elm (Fig. 10), mulberry, red oak (Fig. 11), giant ragweed, and sycamore (Dominiak and Olsen 2006). Bacterial leaf scorch of sugar maple (Acer saccharum Marsh) and sweetgum (Liquidambar styraciflua L.) in Kentucky was caused by X. fastidiosa based on enzyme linked immunosorbent assay (ELISA) tests (Haartman and Jarlfors 1996). Other plants with bac- terial leaf scorch in Kentucky include oak species (burr, pin, red, and shingle) and sycamore (Haartman and Jarlfors 1996). In Washington, D.C., leaf scorch of white mulberry has been detected and found to be caused by X. fastidiosa. Based on serological tests, Kostka et al. (1986) concluded the mulberry strains of X. fastidiosa were more similar to strains that cause Pierce’s disease than those isolated from sycamore, elm, and oak. Most recently, strains that in- fect mulberry have been placed in a separate subspecies, X. fastid- iosa subsp. morus (Nunney et al. 2014). In the 1980s, sycamores (Platanus occidentalis L.) in South Carolina, Washington, D.C., Fig. 12. Paraulacizes irrorata (F.) (Hemiptera: Cicadellidae). Photo by Lisa Texas, and Louisiana were observed to have leaf scorch symptoms Overall. and tests confirmed the causal agent was X. fastidiosa (Haygood and Witcher 1988, Sherald et al. 1983). Symptoms of bacterial leaf scorch of shade trees are similar yet vary Management of bacterial leaf scorch of shade trees is difficult. The in the development of symptoms, depending on the species. pathogen may remain dormant in trees years before symptoms of bac- All symptoms typically manifest in late June to July and increase into terial leaf scorch appear. Tree injections of antibiotics can be costly and the fall (Sherald 2007). Symptoms of bacterial leaf scorch of mulberry can lead to damage. Current recommendations include maintaining include necrotic distal areas of the leaf, with a yellow chlorotic band tree health, rogueing trees with severe symptoms, and planting trees separating dead tissue from green leaf areas (Henneberger et al. 2004). less susceptible to X. fastidiosa (Gould and Lashomb 2007). Downloaded from https://academic.oup.com/jipm/article-abstract/8/1/12/3745634 by Ed 'DeepDyve' Gillespie user on 13 July 2018 Journal of Integrated Pest Management, 2017, Vol. 8, No. 1 9 follows the same pattern of symptom development. It is common to observe bare rachises with terminal leaflets remaining attached (Sanderlin and Heyderich-Alger 2000). Sanderlin and Heyderich- Alger (2003) found that defoliation of leaflets caused by pecan bac- terial leaf scorch decreased nut and kernel weight by 10–13% and 14–19%, respectively, and speculated that yield could decline sig- nificantly over time as bacteria migrate through the pecan tree. Sanderlin and Melanson (2010) verified insect transmission of bacterial leaf scorch from infected to uninfected pecan trees in the laboratory by the sharpshooters, H. vitripennis, H. insolita, and C. costalis, and the spittlebugs, Clastoptera achatina Germar and Lepyronia quadrangularis Say. Insecticide applications targeting spittlebug nymphs have potential to reduce the spread of X. fastid- iosa in pecan (Sanderlin and Melanson 2010). As pecan bacterial leaf scorch is transmissible from grafts of scion wood (Sanderlin 2005), pecan growers can treat scions with hot water to reduce dis- ease occurrence (Sanderlin and Melanson 2008). Sanderlin (2015) recommends using rootstocks that are less susceptible to X. fastid- iosa, and is currently working to identify these cultivars. Future Outlook Extensive research on X. fastidiosa has been completed in California Fig. 13. Graphocephala versuta Say (Hemiptera: Cicadellidae). Photo by Lisa Overall. where Pierce’s disease is now confined to southern grape-growing re- gions (refer to Bruening et al. (2014) for a thorough review of success- ful and current research). Although much has come from research in California, it is difficult to directly adapt and utilize those findings in growing systems in the southern United States. Except for glassy- winged sharpshooter, the primary insect vectors present in California grapevines and almond orchards are different species with different life histories than those found in the southern United States. Much research has been conducted to identify the insect vectors of X. fastidiosa in southern grapevines (Kaloostian et al. 1962, Buzombo et al. 2006, Myers et al. 2007, Lauzie `re et al. 2008, Villanueva et al. 2008, Mitchell et al. 2009, Morano et al. 2010, Wallingford and Pfeiffer 2012, Overall and Rebek 2015), peach orchards (Turner 1955, Turner and Pollard 1959b, Kalkandelen and Fox 1968, Anderson et al. 2008), pecan orchards (Sanderlin and Melanson 2010), citrus groves (Hall and Hunter 2008), and shade trees (Zhang et al. 2011, Overall and Rebek 2015). There is a need to study the spread of the pathogen by screening plant hosts for pathogenic and nonpathogenic infections of X. fastidiosa and cataloguing X. fastidiosa isolates using multilocus se- quence typing to track development of new subspecies and additionally catalogue X. fastidiosa isolates recovered from insect vectors (Almeida and Nunney 2015). Xylella fastidiosa has been detected in citrus in Florida (Hopkins et al. 1991); fortunately to date, X. fastidiosa subsp. pauca that causes citrus variegated chlorosis has not been detected in citrus in the United States. Quarantine protocols are in place in states that would be impacted negatively by this disease. Insect vectors should Fig. 14. Clastoptera xanthocephala Germar (Hemiptera: Cercopidae). Photo be surveyed in preexisting affected commodities and when new diseases by Lisa Overall. arise, such as blueberry leaf scorch. Understanding the presence and biology of vectors and alternate natural hosts of the pathogen will allow researchers to develop effective management strategies for plant Pecan Bacterial Leaf Scorch diseases associated with X. fastidiosa, at least in those commodities Bacterial leaf scorch of pecan (Carya illinoinensis (Wangenh.) K. where management is feasible. Koch) was observed for the first time in Louisiana in 1972, and was thought to be caused by a fungus until Sanderlin and Heyderich- Alger (2000) found that X. fastidiosa was the causative agent. Acknowledgments Symptoms of bacterial leaf scorch of pecan appear in June and pro- We thank Drs. Tom Royer and John Damicone, Department of Entomology and gressively increase into the fall. Marginal necrosis of the leaflets is Plant Pathology, Oklahoma State University, and two anonymous reviewers for typical beginning on the older leaflets at the basal portion of the ra- their careful review of this manuscript. We thank the investigators acknowledged chis and progressing toward younger leaflets. Leaflet abscission in figure captions for granting permission to use their images. This manuscript Downloaded from https://academic.oup.com/jipm/article-abstract/8/1/12/3745634 by Ed 'DeepDyve' Gillespie user on 13 July 2018 10 Journal of Integrated Pest Management, 2017, Vol. 8, No. 1 was prepared with support from the Oklahoma Cooperative Extension Service resistance. California Agriculture 68: 134–141. DOI: 10.3733/ and the Oklahoma Agricultural Experiment Station. ca.v068n04p134. Buzombo, P., J. Jaimes, V. Lam, K. Cantrell, M. Harkness, D. McCullough, and L. Morano. 2006. An American hybrid vineyard in the Texas Gulf References Cited Coast: Analysis within a Pierce’s disease hot zone. American Journal of Enology and Viticulture 57: 347–355. Adlerz, W. C., and D. L. Hopkins. 1979. Natural infectivity of two sharp- Byrne, B. W., and C. Rosa. 2008. 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