Pests and Diseases of Plants Are Cosmopolitan, and Have Been

InternationalInternational EntomologyEntomology

Kostas Bourtzis, Steven Crook, Daniele Daffonchio, Ravi Durvasula, Yupa Hanboonsong, Francisco Infante, Paulo T. Lacava, Thomas A. Miller, and Fernando E. Vega

ests and diseases of plants are cosmopolitan, and have been the percentage is lowest near the equator and higher farther away. from the beginning of agriculture. Domestication of plants and breeding for increased yields allowed civilizations to nights in diapause only at non-freezing temperatures underground. develop, but often created new problems associated with DiapauseAs a tropical is triggered moth, the by pink low temperature,bollworm can short survive days, freezing and food winter qual- P ity. Older literature claimed that diapause could last two years or era, inorganic fertilizer in some cases has eliminated crop rotation andmonocultures led to pollution and displacedof rivers and native aquifers. flora Theand following fauna. In descriptionsthe modern of several international collaborators’ attempts to manage pests more (see F. C. Willcocks 1916, in Naranjo et al. 2002; Anonymous and diseases represent the beginnings of a practical international 1984). Diapausing pink bollworm larvae tend to associate with cotton entomology, and are a form of science diplomacy. A common theme regionsseeds, spinning in this condition. a modified cocoon and often knitting seeds together. in each of the examples is the urgent need for new tools in pest and It can survive shipment from infested areas to other cotton-growing disease management. program starting a few years after introduction to California from Pink bollworm was the object of a Sterile Insect Technique (SIT) Pink Bollworm - plow-downArizona around and 1965.other Whilesanitation suppression measures, of ainfestations court decision in eastern to lift worm, Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechi- Arizona starting in 1927 were considered successful using early First recorded as a cotton pest in India about 1843, the pink boll through Arizona to California (Naranjo et al. 2002). This incident on the richness of parasites and predators found there (Naranjo et al. these restrictions lead quickly to a population explosion that spread idae) is thought to have originated in the Indo-Pakistan region, based exacerbate pest problems. clearly shows how human intervention and lack of vigilance can 2002). The larval stage infests fruit and flower buds of the Malvaceae- pendingfamily of onplants, prevailing including weather okra, conditions; mallow, hibiscus, earlier and generations cotton. feed deltaThe endotoxin advent of genes Bollgard® from acotton strain developed of Bacillus by thuringiensis Monsanto provided, an ento- The pink bollworm has from three to six generations a year de a powerful new tool to control pink bollworm. Insertion of one of the most chewing Lepidoptera, including larvae of the budworm and on cotton squares or flowers in the spring, while later ones infest mopathogenic bacterium, into cotton offered 100% protection against bolls. A certain number of larvae in field populations enter diapause; 234 American Entomologist 2012

• Winter bollworm complex (Lepidoptera: Noctuidae) and pink bollworm itself. theseResistance published was studies readily and demonstrated anecdotal infestation by feeding reports, pink bollworms resistance on a Bollgard® diet for several generations (Bartlett 1995). Despite- of pink bollworm to the Bollgard® plants was not reported from in troduction around 1994 until 2011, when resistance was confirmed thein India United by StatesTim Dennehy, was due then to the with resistance Monsanto management (Dhurua and strategy Gujar followed2011). Perhaps by the U.S. this Environmental outstanding record Protection of holding Agency, off which resistance insisted in that a non-Bollgard® harborage be included in every Bollgard® maintain a large enough supply of susceptible genes to prevent the cotton field. Because resistance is a recessive trait, the intent was to rigidoccurrence resistance of homozygous management resistant strategy. strains (Tabashnik et al. 2000). The Indian resistance incidentAnthonomous may have grandis been grandiscaused by Boheman), relaxing this the

Like the boll weevil ( ofpink the bollworm program isare the a specialobject ofwaiver eradication of the EPAattempts, rule requiring the latest non- one Bollgard®starting in 2005harborage (http://tinyurl.com/cjhh5bk). plants, early-season pheromone The main treatment, elements

- toring.SIT releases The waiver when wasthe field granted populations by EPA because are reduced sterile to insect small releases enough werenumbers said to to make satisfy SIT the practical, harborage and requirement.extensive pheromone trap moni

No pink bollworms have been found in California, Arizona, New Mexico, or most of Chihuahua, Mexico for the past few years. The eradication program is now focusing on west Texas and Mexico in the Colorado River drainage areas of San Luis, Sonora and Mexicali, Baja California Norte. During the 2011 cotton season, 83,202 acres of cotton were grown in the Mexicali area just over the California tensborder of thousands from El Centro. of cotton Of this bolls acreage, that were 137 randomly fields out sampled. of 2,310 Forty- were Fig. 1. Coffee berry borer, Hypothenemus hampei Ferrari. Left photo by Eric non-Bollgard® cotton, and fewer than 12 larvae were found in the Erbe, colorized by Chris Pooley, USDA; right photo by Peggy Greb, USDA. five million SIT moths were released each week in this area and San Luis during the 2011 growing season. Twenty-five larvae were found arein the expensive, San Luis-Mexicali requiring intensivearea at the labor end and of the unprecedented 2012 season. coopera - tion.Eradication Therefore, programs they are only like feasiblethose for when boll weevil the costs and are pink outweighed bollworm

Coffeeby overwhelming Berry Borer financial incentives. The most devastating insect pest of Coffea arabica L. and C. canephora Pierre ex A. Froehner worldwide is the coffee berry borer, Hypothenemus hampei Ferrari (Coleoptera: Curculionidae: Scolyti- coffee-producing countries, causing severe damage to the coffee seed, nae) (Fig. 1). This bark beetle has disseminated from Africa to most whichThe is insect the marketable poses a formidable product. Yearly control losses challenge due to due the to coffee its cryptic berry Fig. 2. Coffee berries ready for picking. Photo by Fernando E. Vega. borer have been estimated at over $500 million (Vega et al. 2002a). sibling mating inside the berry means that females are inseminated nature inside the coffee berry (Fig. 2). Infestation begins when a and ready to oviposit as soon as they exit the berry. theyfemale start bores consuming a hole in the the seed, coffee reducing berry and both deposits quality upand to yield. 300 eggsTwo Research aimed at developing pest management strategies (Jaramillo 2008) in galleries within the seed. Once the larvae hatch, against the coffee berry borer have focused on the use of biological control agents, such as parasitoids and fungal entomopathogens. offactors the maternallymake the insect inherited even moreintracellular problematic: alphaproteobacterium the sex ratio of the Unfortunately, even though some mortality might ensue, use of these Wolbachiaspecies is skewed, favoring females 10:1 (likely due to the presence

biocontrol agents is not sufficient to control the insect. Furthermore, American Entomologist or another male-killingVolume 58, Number agent [Vega4 et al. 2002b]); and 235

• long-term studies after introduction of both parasitoids and fungal fee berry, and due to sibling mating in this cryptic environment, opportunities for mating disruption appear limited. Some success the use of fungal entomopathogens against the coffee berry borer has been reported in recruiting local entomopathogenic fungi as a wasentomopathogens the development are of lacking a technique (Vega that et al. was 2009). effective A novel in introducing aspect of Beauveria bassiana deliverybiological paradigm control method is needed. that is applied like an insecticide. However, (Balsamo) Vuillemin (Ascomycota: Hypocreales) as inTools the forcase pest of the control pink fall bollworm, into one deliveryof the four is categoriesthe problem. shown A new in as a fungal endophyte in coffee plants (Posada and Vega 2006; Posada Of these, neurotoxic chemicals are the most frequently used et al. 2007), although establishment was short-lived, probably due to the presence of other fungal endophytes in the plant (Vega et al. ofTable broad-spectrum 1. neurotoxic insecticides, well-established agro- 2008a, 2010). Further research aimed at permanent and systemic and the only ones on the list that give results immediately. In the case strategyestablishment against of thefungal coffee entomopathogens berry borer. as endophytes (Vega 2008; VegaOne et ofal. the 2008b) interesting might aspectsresult in in anthe effective biology ofpest the management coffee berry chemical companies enjoy a $30 billion global market that maintains borer is the insect’s ability to survive on a food source that contains attractivethe industry. selectivity The current that trendthis approach to find local offers. fungi While or other biopesticides microbial arecontrol more agents sustainable is hampered and environmentally by a narrow market friendly dictated than byneurotoxic the very insecticides, they still suffer from development of resistance and the weightthe alkaloid basis) caffeine in C. arabica (1,3,7-trimethylxanthine;C. canephora Vega et al. 2003).- delivery problem faced by neurotoxins. Caffeine levels in the coffee seed are on average 1.1-1.7% (on a dry - the role of caffeine in plants and might 2-3% be in as a defense against (Mösli herbiWald- vores.hauser Therefore, and Baumann the ability 1996). of Nathanson the coffee berry (1984) borer hypothesized to successfully that The California Cotton Pest Control Board spent significant fund - ing on a ten-year effort to find natural enemies for pink bollworm,- tion mechanisms that are absent in species that cannot survive on hopper,but did notCirculifer succeed. tenellus The Curly Top Virus Control Program funded caffeine-containingexploit a food source food containing sources. caffeine Research is aimedlikely dueat elucidating to detoxifica the withouta similar success. effort to The find current natural emphasis enemies foron thebiodiversity key vector, and beet natural leaf resource protection has had (Baker) a negative (Hemiptera: side effect Cicadellidae), on attempts also at part of an ongoing project between scientists at the U.S. Department biocontrol: countries of origin are increasingly reluctant to approve ofrole Agriculture–Agricultural of the coffee berry borer Research microbiome Service in caffeine and the U.S.detoxification Department is of the biology of the insect is better understood, it might be possible Table One. Pest control categories with examples. of Energy–Lawrence Berkeley National Laboratory. When this aspect to develop new pest management strategies by interfering with Cultural (Agronomic): Crop rotation; intercropping to avoid monoculture (Resistant crop varieties) microorganisms that might be contributing to caffeine breakdown. Physical: Improving attractants used in traps might provide another ethanol:methanol mixture currently used in different trap designs Barriers; Farming in remote areas; Quarantines possible mechanism to manage the insect (Vega et al. 2009). The results in capture of high numbers of insects, but this capture has not Greenhouse crops

The development of a repellent that could be used when the berry Chemical: been shown to significantly reduce infestation levels or yield losses. NeurotoxicHeat; cold insecticides; growth regulators - Systemic insecticides becomes suitable for infestation, i.e., when dry weight becomes 20% ment strategy. Finally, determining whether the insect produces and Pheromones; biopesticides respondsor higher (Bustillo to a pheromone et al. 1998), could could also be result a revolutionary in a novel pestand manageeffective pest management strategy against the insect. Biological: NaturalInorganics enemies (arsenates; Paris Green; boric acid) Tools to Control Pests and Diseases in Agriculture Entomopathogens (viruses, bacteria, fungi) As shown by the two examples above, some insects can be inac- (Biopesticides) cessible to surface insecticide treatments. The adult pink bollworm night, it feeds on nectar or searches for a mate. The egg, pupal, and NaturalSterile Insect product Technique fumigants (cassava leaf extract) spends the day in cracks in the ground in arid growing areas, and at larval stages are respectively spent hidden under boll calyxes, in the SymbioticGenetically control: modified insects soil, or inside the cotton boll, where they consume the seed. Thus, the Wolbachia-based population replacement - Wolbachia-based population suppression tion of a toxin into a transgenic plant so that all tissues contain lethal Paratransgenesis most efficient method of delivering an insecticide is via incorpora doses. The alternative of leaving an insecticide residue on the cotton Transgenic crop plants (with weed or insect resistance) in the face of continuous emergence of moths from diapause over Biopesticides appear in two places on this list. Entomo- plant for the adult to encounter does work, but is much less efficient pathogens are also biopesticides, but some biopesticides are spring and early summer. The other successful control method for broad-spectrum neurotoxic natural product chemicals, such as avermectin (from Streptomyces avermitilis) and the spinosyns in the season to disrupt attraction for mating. One such treatment (from Saccharopolyspora spinosa). Thus their exact categoriza- canpink last bollworm a month is when to saturate applied the in cotton slow-release field with formulations. pheromone early tion is not entirely clear. The coffee berry borer spends considerable time inside the cof-

236 American Entomologist 2012

• Winter are less inclined to approve releases locally without evidence that nativeshipment fauna of willnatural be unaffected. enemies for testing abroad, and local officials the host fitness. Dysbiosis (i.e., an imbalance of the gut microbiome) is one of the first factors that allow pathogens to invade the host Sterile Insect Technique (SIT) body and trigger diseases or decrease general host fitness (Hamdi BIODESERTet al. 2011). out reproduction of pest populations has been conducted in different Symbiotic control is a general strategy that aims at exploiting countriesDaily field and releasecontinents of mass-reared by international and sterilizedconsortia insectsof entomologists. to swamp Wolbachia) - for various aspects of insect management, including population sup- ization” of entomology, while stressing environmentally friendly and specific members of the insect host microbiome (e.g., sustainableThese efforts methods guide scientific of pest control. societies towards true “international pression of agricultural pests (Zabalou et al. 2004, 2009, Apostolaki et al. 2011) and disease vectors (Atyame et al. 2011; Brelsfoard and Invented by Edward F. Knipling (USDA) and collaborators, SIT has currentlyDobson 2009, developing 2011) approachor interference is the applicationwith pathogen of symbiotic transmission control by become a key tool of several area-wide control programs (Tan 2000; forinsect the vectorsprotection (Hoffmann of useful et insects al. 2011, such Walker as pollinators et al. 2011). or parasitoids A novel, lowVreysen enough et al. to 2007).allow the Some survival insects of boll(famously, weevils the for aforementionedat least ten days boll weevil) are not suitable for SIT protocols. Doses of radiation One recent case study is the exploitation of honeybee symbionts - for(Hamdi protection et al. 2011, from Crottia widespread et al. 2012). and dangerous honeybee disease, did not induce sterility (Abdul Matin et al. 1980). The successful American Foulbrood Disease (AFB). AFB is caused by a pathogenic U.S. national boll weevil eradication program (http://www.txboll bacterium, Paenibacillus larvae pheromoneweevil.org/) or (http://tinyurl.com/8czdnbx) lures and spot treatments with did notmalathion rely on orclassical other neurotoxicSIT. Instead, insecticides. the program relied on monitoring using aggregation , that fatally infects bee larvae (Hamdi potentialet al. 2011). of bacterial In a European symbionts Union-funded in protecting project the honeybee(GA-245746), from three AFB. of mass-reared and irradiated insects must be released in order to teams from Tunisia, Italy, and Greece are cooperating to assess the To inflict the desired fitness costs on a target pest, large numbers- evaluating microbial resources in the arid ecosystems of the Saharan andThe pre-Saharanproject, BIODESERT, lands in southernis generally Tunisia. framed Using under approaches the concept from of compete with wild types. New variations on the SIT method, Auto molecular ecology and metagenomics coupled with biochemical employcidal Biological a single Controllethal gene (ABC; in aFryxell strain andthat Milleris capable 1995) of andbeing Release mass- and physiological characterization of honeybee symbionts, the of Insects carrying a Dominant Lethal (RIDL; Thomas et al. 2000), This new strategy allows the strain to be reared under permissive for improving honeybee health. In vivo tests showed the feasibility reared, but passes on lethal genes to field populations when released. BIODESERT project selected a set of natural microbial probiotics lethalconditions, gene must out-crossed be dominant to wild so types,that the and lethal then condition back-crossed is expressed to the of the approach for protecting the major pollinator from AFB (Hamdi withhomozygous only one condition copy as heterozygote. for the lethal geneAlthough with increasedthis strategy fitness. is one The of Sugarcaneand Daffonchio White 2011). Leaf Disease the most sustainable and environmentally friendly ever invented Sugarcane white leaf disease (SCWL) is one of the most harmful

States by regulatory strangulation. (Miller 2012), it has been delayed or even prohibited in the United diseases of sugarcane, making it a threat to sugarcane industry in the Asia region, especially in Thailand, Taiwan, Lao PDR, Vietnam, The efficiency of SIT can be sustained by proper management isand caused Sri Lanka by plant-pathogenic (Nakashima and phytoplasma, Murata 1993, a bacterium Kumarasinghe without and a of the insect gut microbiome (Crotti et al. 2012) that is essentialCeratitis cellJones wall 2001; belonging Nakashima to the et classal. 2001, Mollicutes Thein etthat al. lives2012). in Thethe phloemdisease capitatafor maintaining (Diptera: host Tephritidae) fitness following have been irradiation. shown Forto beinstance, extremely the microbial gut symbionts of Mediterranean fruit fly (medfly) C. capi- of host plants and is vectored by insects (Chen 1974; Wongkaew et tataimportant males inare maintaining less competent the reproductive in mating than fitness wild of males, irradiated decreasing males symptomsal. 1997). The of stunt, SCWL leaf phytoplasma chlorosis, and belongs profuse to tilleringthe 16Sr (formation XI-B genetic of (Ben Ami et al. 2010). In a standard SIT application, the sterile abovegroundgroup of the rice shoots yellow from dwarf a node category at the base (Lee of et the al. principal1998) and shoot shows in that the decreased mating competence was associated to a profound the efficiency of the field treatment. Ben Ami et al. (2010) showed The infected sugarcane plants show disease symptoms at an early The irradiation treatment, besides sterilizing the males, decreased grasses and some other plants) on infected sugarcane plants (Fig. 3). thechange levels in ofthe certain structure probiotic of the members microbiome of the associated symbiotic to microbiome the medfly. Klebsiella species) while favoring the growth shortenedgrowth stage internodes (1-6 months and cannotold), and prolong in the growthcase of severeuntil the infection, second of Pseudomonas ratoonplants die(multiple at a young seasons age. Infectedof yield) plantscrop as with the no disease symptoms symptoms show feedingof the medfly the males (namely after irradiation with cells of a Klebsiella oxytoca will appear and the plant dies, with high yield loss. The SWCL phy- sp. that have no beneficial effects on the host. By Matsumu- ratettix hiroglyphicus Yamatotettix flavovittatus colonizationstrain isolated of fromK. oxytoca the medfly and decreased prior to presenceirradiation, of theBen potentially Ami et al. toplasma is transmitted to the plant by the leafhoppers pathogenic(2010) demonstrated pseudomonads. higher mating fitness associated with a stable (Matsumura) and Matsumura (Hemiptera: Cicadellidae) (Matsumoto et al. 1968, Chen other animals, maintaining a stable gut microbiome is essential for planting1974, Hanboonsong material and et by al. insect 2002, vectors. 2006). The SCWL phytoplasma still The study of Ben Ami et al. (2010) indicates that in insects, as in The disease is spread through the use of infected cane stalks for American Entomologist Volume 58, Number 4 237

• with a low phytoplasma load and allow them to reach maturity. The threshold of phytoplasma inoculum that leads to symptoms has yet to be determined. SCWL disease remains a major challenge to the sugarcane in-

described here offer the hope, if not of eradicating the disease, at leastdustry of of diminishing Southeast Asia. its impact. However, the multiple control approaches

Xylella fastidiosa and Pierce’s Disease

Pierce’s disease (PD) of grapevines (Fig. 4) was first detected in Southern California in 1884, where it destroyed approximately experience,40,000 acres which of grapes was restrictedin Anaheim, to OrangeCA, during County, a five-year PD became outbreak only an(Pierce occasional 1892, Goodwin concern andto West Purcell Coast 1992). viticulture Following for this many devastating decades

habitats. This all changed when the glassy-winged sharpshooter (GWSS),because ofHomalodisca the preference vitripennis of native vector leafhoppers for riparian

Germar (Hemiptera: Cicadellidae; Fig. 3. A field of sugarcane in northeast Thailand heavily affected with Takiya et al. 2006) invaded California at some point during the white leaf disease. Photo by Yupa Hanboonsong. Temecula, where about one-third of the vineyards were lost. The 1980s. By the late 1990s, it had caused new epidemics centered in cannot be cultured, and so far there is no resistant sugarcane variety of X. fastidiosa in the United States. The insect is a major concern or effective method to control SCWL disease, except elimination of forGWSS horticultural (Fig. 5) is industriesthe most widespread beyond viticulture sharpshooter due to insect its ability vector to infected plants to decrease the amount of phytoplasma inoculums. transmit X. fastidiosa strains that cause scorch diseases in a number Approaches such as tissue culture technique or hot water treatment of host plants, including X. fastidiosa subsp. fastidiosa, which causes - gies have not been able to effectively control or prevent the disease. have been applied to ensure disease-free cane stalks, but these strate PD in grapevines (Purcell, 2005). vectors and sugarcane host plants. Currently, no alternative host Integrated pest management practices are aimed at both insect plants are known as reservoirs of SCWL phytoplasma (Wongkaew et vectoral. 1997). is therefore Insect vectors one ofcan the transmit most important the pathogen factors from contributing generation to generation through eggs (Hanboonsong et al. 2006); the insectM. hiroglyphicus Y. flavovittatus to the spread of SCWL disease. The transmission efficiency of for these insect (55%) vectors is higher(M. hiroglyphicus than that of and Y. flavovittatus (45%)) are (Hanboonsong et al. 2006). The estimated natural dispersal distances approximately 8 and 20 meters per day, respectively (Thein et al. not2011, only 2012). in disease epidemiology, but also in developing vector mod- els Insectand strategies vector transmission to prevent the efficiency spread ofand the dispersal pathogens are by relevant vector - tion of disease transmission in insect vectors is under investigation. insects. In addition, using a symbiotic controlM. hiroglyphicus approach for harbors interrup the M. hiroglyphicus” Fig. 4. Pierce’s disease symptoms in Chardonnay grapevines, Temecula, California, 2004. Leaf scorch characteristic is clearly evident and the It was revealed that the insect vector - grapes themselves slightly shriveled. Photo by José M. Ramírez. perbacterial and is symbiont found in all “Bacterium developmental Associated stages including with eggs, nymphs, (BAMH). BAMH is present in the midgut and ovaries of the leafhop As with other sharpshooter insects, GWSS is a xylophagous insect aand candidate adults. Moreover,for symbiotic it appears control toof sugarcanebe specific whiteto the leaf vector disease. of the pathogen causing SCWL (Wangkeree et al. 2012). This symbiont isthat feeds on hundreds of plant species (Purcell and Hopkins 1996,- trolling this disease. Crop rotation between sugarcane and upland shipPurcell between and Saunders PD incidence 1999), in withgrapes citrus and thebeing proximity one of its of vineyardspreferred Implementing good farming practice is also important for con hosts (Blua et al. 2001). Perring et al. (2001) demonstrated a relation the growth cycle of the insect vector population and consequently rice is likely to reduce the prevalence of SCWL, and may cut down- to citrus orchards. The leafhopper has X. fastidiosathe capacity-carrying to survive insects winter as- ing plant health by providing essential and appropriate nutrients to temperatures as low as -6°C (Park et al. 2006). infectedreduce the plants presence could preventof the disease the appearance pathogen. of In symptoms addition, inimprov plants Moreover, compared with other sociated with PD and native to California, GWSS has a longer flight 238 range (up to 1/4 mile). These traitsAmerican make Entomologist the GWSS a veryWinter serious 2012

• to cause scorch diseases in many fruit trees and ornamental species,

of the GWSS-transmitted pathogens causing diseases of horticultural cropsespecially in California in North andby a South symbiotic America control (Hopkins (SC) or 1989). paratransgenic Control of anyap- proach would be of immediate interest to other industries as well. The technique of paratransgenesis was developed as a novel method to create conditions that render insect vectors incompetent. The strategy of SC employs both paratransgenic and non-recombinant

solutions may result in competitive displacement of the pathogen withmethods a more to control benign disease microbe. or health problems. In some cases, these The strategy, paratransgenesis, was intended to prevent the transmission of pathogens by insect vectors to humans (Beard et

anyal. 1998, pathogen, 2001, including 2002, Rio a et plant al. 2004) pathogen. using This symbiotic overall microbes strategy asof diseasedelivery preventionvehicles. However, is an example in principle of SC it canand beis applieda variation to displace on the

theme of symbiotic therapy (Ahmed 2003). Genetic manipulation has fitness costs that must be factored into the application (Durvasula candidateet al. 1997, microbe Miller 2007). that has an existing association with the patho- systemThe keythat to includes SC, and the therefore problem paratransgenesis, or condition at ishand. to find The a local candidate microbe should occupy the same niche as, or have access

Fig. 5. One week of glassy-winged sharpshooters, Homalodisca vitripennis, on yellow sticky cards in research vineyard at UC Riverside, 7 July 2009. origin of the biocontrol microbe in SC differs from classical biological to, the target pathogen or condition (Durvasula et al. 1997). The local The lines are one inch apart (2.54 cm). Photo by Candice Sanscartier. control, in which microbes, herbivores, parasites, or predators are threat to the wine industry in Southern to Central California (Castle - co-evolvedsought from with outside and established of the local in ecosystem the pathosystem; to control foreign a pest explora (Miller- fornia vineyards, programs aimed at controlling the dissemination of 2007). In SC, all elements originate at the local site and are already et al. 2005). Indeed, since the first identification of GWSS in the Cali Because of these strict requirements, a suitable symbiotic candidate maytion isnot not always only unnecessary, be found or but may also not most be amenable likely counter-productive. to practical ma- this insect as a strategy to prevent PD outbreaks have involved more Californiathan $160 because million of andirect aggressive investments quarantine (http://www.cdfa.ca.gov/ program. - phpps/pdcp/).Xylella fastidiosa So far, is GWSS a complex has not of fastidious become established Gram-negative in Northern xylem- nipulation (Miller 2007). limited bacteria, rod-shaped with distinctively rippled cell walls. The Microbes chosen for symbiotic control must be able to pass subse quent regulatory scrutiny (Miller 2007). Once a candidate symbiont is identified as a control agent for paratransgenesis, all genetic or strains are non-flagellate, do not form spores, and measure 0.1-0.5 × beother suitable manipulations for another can site be or local.condition Indeed, elsewhere a symbiotic (Durvasula control et oral. 1-5 micrometers (Nyland et al. 1973, Bradbury 1991). These Gram- paratransgenic solution developed for a specific location may not negative bacteria were formally named only in 1987 (Wells et al. obscurity.1987), and Natural are extremely transmission slow-growing occurs via in insects culture. feeding These suctoriallytraits have for1999, the 2003, generation Miller of 2007). panels of recombinant single-chain antibodies made the pathogen difficult to study, contributing to its previous againstAzizi the et al.surface-exposed (2012) recently elements presented of X.a simple,fastidiosa robust that mayapproach have species. The bacterium overwinters in the xylem of the host plant ason wellxylem as sap.in weeds. Transmission efficiency varies widely among vector combinatorial antibody ribosome display libraries The main control method for PD in the quarantine zone of werepotential assembled use in diagnosisfrom immunoglobulin and/or disease transcripts transmission rescued blocking from Southern California is one early season treatment with imidacloprid studies. In vitro X. fastidiosa. The systemic insecticide applied via drip irrigation. This was extremely libraries were used in a single round of selection against an outer effective in most vineyards but was not used in organic vineyards, the spleens of mice immunized with heat-killed which continue to sustain losses. Citrus that provides overwinter harborage for GWSS is also treated where possible. These measures antibodiesmembrane wasprotein, demonstrated MopB, resulting by the insuccessful the isolation application of a panel of the of stimulated a rebound in new plantings and vineyards as the Temecula recombinant antibodies. The potential use of selected anti-MopB area recovered, and allowed researchers and the industry to buy time to search for other remedies. One new method is a transgenic 4XfMopB3 antibody in an enzyme-linked recombinant immunosorbent single-chain antibody assay grapevine with factors preventing PD symptoms from developing (ELISA), a Western blot assay, and an immunofluorescenceX. fastidiosa are a resource assay (IFA).for the These Pierce’s immortalized disease research in vitro community, and may be readily growers either. librariesaccessed generatedfor the isolation against of heat-killed antibodies against a plethora of X. fas- (Dandekar 2012), but of course, this cannotXylella fastidiosabe used by organic tidiosa surface-exposed antigenic molecules. These authors (Azizi et

AmericanBesides Entomologist PD, other specificVolume strains 58, Number of 4 are known 239

• other abundant surface-exposed molecules on X. fastidiosa could also beal. 2012)engineered concluded in a similar that recombinant way to agglutinate antibodies the bacteria against andMopB evalu and- dieback, necrotic leaf lesions, and undersized, hard fruit (Derrick ated in the GWSS via paratransgenic organisms such as engineered and Timmer 2000; Hopkins and Purcell 2002). The causal agent commensals or symbionts, providing novel alternative platforms to of CVC has been found to be transmitted in Brazil by sharpshooter investigate in the control of PD. leafhoppers (Cicadellidae) (Lopes et al. 1996; Almeida and Purcell 2003). CVC has been experimentally transmitted by 11 different Citrus Variegated Chlorosis (CVC). sharpshooterAlthough X. species fastidiosa (Fig. subsp. 7) tested pauca in Brazil (Fundecitrus 2005). toThe have pathogen its genome can be sequenced also transmitted (Simpson through et al. seeds 2000), (Li there et al. 2003).is still Citrus sinensis Xylella fastidiosa was the first plant pathogen- subsp.Citrus pauca variegated chlorosis (CVC) (Fig. 6) is a disease of the sweet nary host range among higher plants in New World ecosystems orange [ (L.)], which is caused by no effective control. The pathogen is known to have an extraordi (Chang et al. 1993, Hartung et al. 1994, Schaad et al. plants, X. fastidiosa does not damage the host plant and behaves 2004), a phytopathogenic bacterium that has been shown to infect (Freitag 1951). Interestingly, within the majority of native host importantall sweet orange diseases cultivars affecting (Li sweet et al. 1997a). orange production CVC was first in Brazilreported (Ros in- horticultural crops that suffer from diseases caused by X. fastidiosa Brazil in 1987 and has rapidly become one of the most economically areas an those endophyte that have (Purcell been introduced and Saunders into New1999). World In contrast, ecosystems the most major citrus-growing areas through unregulated movement of (Chen et al. 2000). The observation that a few asymptomatic trees setti et al. 1990, Lee et al. 1991). CVC rapidly became widespread in persist in some infected orchards may lead to new approaches to infected nursery stock due to a previous lack of certification programs have the same genotype as diseased plants and are located in the and high CVC infection rates in Brazil. CVC can be found in at least samethe investigation grove under of similarthe control climatic of CVC. and These edaphic asymptomatic conditions, plants sug- 90% of the orchards in Brazil (Lambais et al. 2000), where it causes inlosses Brazil: of $100C. limonia million, C. perreshni year, and (Della-Coletta C. volkameriana et al. 2001). TheCVC disease occurs has on not trees been propagated observed on on limes all commonly (C. latifolia) used or mandarinsrootstocks endophyticgesting that microbialsome other community factor is responsible colonizing forindividual resistance C. sinensis to CVC. (C. reticulata), even when the trees were planted in severely(Li et al. affected1997c). plantsOne factor (Araújo that etmay al. influence2002). resistance to CVC is the nature of the

having an existing association with the ecosystem that includes the orange groves (Li et al. 1997 b). problemThe key or conditionto symbiotic at hand, control and isthat finding occupies a candidate the same microbeniche as Citrus plants with symptoms of CVC show a brilliant leaf chlorosis, similar to zinc deficiency, as the initial symptom (Laranjeira et al. genus Methylobacterium X. 1998, Anonymous 2000). Later symptoms include wilting, canopy fastidiosaor has access subsp. to paucathe target inside pathogen citrus plants (Miller, (Araújo 2007). et al.Bacteria 2002, Lacava of the are known to occupy the same niche as

localizationet al. 2004). ofDuring the endophytic feeding, insects bacterium, acquire M. not mesophilicum only the pathogen,, in a C. roseusbut also model endophytes plant system from host and plants. the transmission Gai et al. (2009) of this reported endophyte the by Bucephalogonia xanthophis, a sharpshooter insect vector of X. fastidiosa subsp. pauca. Methylobacterium mesophilicum, originally isolated as an endophytic bacterium from citrus plants (Araújo et al. 2002), was geneti-

M. mesophilicum was inoculated intocally C. transformed roseus (model to plant)express seedlings green fluorescent and was observed protein colonizing (GFP; Gai itset xylemal. 2007). vessels. The GFP-labeled The transmission strain of of M. mesophilicum by B. xanthophis

- dophyticwas verified colonization with insects by feedingM. mesophilicum on fluids containing the GFP-labeled asbacterium. a nonpathogenic, Forty-five xylem-associated days after inoculation, endophyte the plants (Gai exhibitedet al. en These data demonstrate that M. mesophilicum, confirming not this only bacterium occupies the same niche as X. fastidiosa subsp. pauca inside plants, but also 2009). that it may be transmitted by B. xanthophis. The transmission, colonization, and genetic manipulation of M. mesophilicum is a prerequisite to examining the potential use of paratransgenic SC to interrupt transmission of X. fastidiosa subsp. pauca, the bacterial pathogen M. mesophilicum as a candidate for a paratransgenic SC strategy to reduce the spread of causingX. fastidiosa CVC, subsp. by insect pauca vectors. We proposeX. fastidiosa subsp. pauca Fig. 6. Citrus Variegated Chlorosis symptoms. A. Advanced symptoms - with small, yellowed fruits. B and C. Leaf symptoms showing chlorotic . It is known that spots on the upper leaf surface corresponding to gummy brown spots on sible for the obstruction of xylem in affected plants (Lambais et al. produces a fastidian gum (da Silva et al. 2006), which may be respon the underside. Photo by H.D. Coletta-Filho.

240 2000), so the production of endoglucanaseAmerican Entomologist by genetically modified2012

• Winter Fig 7. Brazilian leafhopper vectors of Citrus Variegated Chlorosis. Photos by Pedro T. Yamamoto. Authorized by FUNDECITRUS (http:// www.fundecitrus. com.br/Home/Default.aspx). endophytic bacteria may transform the endophytes into symbiotic

One of the more successful examplesInsect occurred Symbiosis when (BourtzisNancy Moran and control agents for CVC. Methylobacterium expressing antibi- started working with Paul Baumann. Moran’s beautiful dedication Azevedo and Araújo (2003) used the replicative vector pEGLA160 to Professor Baumann in Volume 3 of otic resistance and endoglucanase genes. Furthermore, other strate- - to produce genetically modified Moran 2009) is pertinent: - Methylobacterium to secrete soluble anti-Xylella protein effectors in ing“I still on remember a study on verythe bacterial clearly my endosymbionts first conversation of aphids; with Paul the Bauyear gies can be evaluated, such as a production of geneticallyEscherichia modified coli mann. He had phoned to ask if I might be interested in collaborat to secrete soluble anti-Xylella citrus, such as Lampe et al. (2006) suggested in the was 1990. His excitement was infectious. I had read much of Paul α-hemolysin system for use in Axd Buchner’s book as a graduate student but had never considered suggested the evaluation of proteins secreted from the grapevine workingThis introduction on symbionts covers and knewseveral almost issues nothing germane of microbiology.” to the present bacterialprotein effectors symbiont in Pantoeagrapevine agglomerans and GWSS. forAlso, use Lampe as secretion et al. (2007) part- ners of anti-Xylella protein effectors. One strategy that can serve at the time, that a major source of conceptual information may be context. It illustrates the degree of isolation between disciplines Methylobacterium, to secrete anti-Xylella proteinas the next effectors. step for SC of CVC is producing a genetically modified Universityfound in a book, of California, and that Davis:collaboration two different starts by states, reaching but theyout. Nancy could endophytic bacterium, like - justMoran as wellwas athave the been University in different of Arizona, countries. Tucson and Paul was at the ated with vector insects and plants differ in abundance through According to Gai et al. (2011) the bacterial communities associ journal for the publications. There are myriad outlets, including entomology,Once microbiology, interdisciplinary and collaborationplant pathology starts, journals, it is difficult but publications to pick a competitionthe yearly season. with pathogens Endophytic in host bacteria plants andcould also influence in insect foreguts. disease that combine all three disciplines include the International Journal development by reducing the insect transmission efficiency due toof Pest Management and Symbiosis tors of X. fastidiosa subsp. pauca changed with time, environmental In addition, the bacterial communities in the foregut of insect vec that symbiosis, besides being interdisciplinary,, the journal ofwas the global. International the genus Curtobacterium were consistently detected in the sharp- Symbiosis Society (ISS). The founders of ISS understood instinctively shooters’conditions, foreguts and in anddifferent are commonly insect species. isolated However, from themembers xylem of international connection is when international congresses are held. citrus plants (Araújo et al. 2002), and may therefore be candidates Most agriculture-related societies are national, and their only for biological control. - These are typically held every four years. Thus, while it is difficult to Barriers to Interdisciplinary Collaboration aknow plant where disease to publishcaused interdisciplinaryby a microbial pathogen work, it is transmitted equally challeng by an The nature of symbiotic control is interdisciplinary, though it insect,ing to know do you which attend society an entomology, meetings to plant attend. pathology, If you are or working microbiol on- is not easy to initiate collaborations across interdisciplinary lines. ogy meeting? Do you attend the Congress of Plant Protection, the

American Entomologist Volume 58, Number 4 241

• - ment, or all of them? InternationalDespite the Congress national characterof Entomology, of agriculture-based ISS, Integrated sciences, Pest Manage there enrolledtion is in English,as undergraduates the students and are graduates.from around The the placement world and rateKorea, of is an urgent need to become international. The Entomological Society and the faculty is international. In 2009, about 8,000 students were being expanded adjacent to the campus and the major science and KAIST graduates is nearly 100%. A Science and Technology Belt is of America (ESA) took the first step in this direction by establishing an Similar Science and Technology education and research centers were International Branch to join the regional national branches. Everyone startedtechnology in China companies over ten in years Korea ago, eagerly all teaching recruit thein English, KAIST graduates. and a new entomologyin ESA should organization. belong to the International Branch, but, oddly, they don’t. When they do, ESA will become the first truly international- oping, to ensure that colleagues are adequately trained and actively Globalone opened Knowledge in North Initiative Korea two (GKI) years ago. It is in the vested interest of every country, developed or devel - and invade others. working in all countries that have pests or diseases likely to travel EducationThe Global Summit Knowledge for Global Initiative Development (GKI) is convened a non-profit by theorgani U.S. International Connections Secretarieszation based of in State Washington, and Education DC. It andarose the from administrator the 2008 Higher of the Several advances serve to support the feasibility of international - population to become mobile. The second is the revolution in com- U.S. Agency for International Development. Attended by more than municationcollaborations. that The has first brought is air us travel, e-mail which and cellularhas enabled telephones. the world’s The 200 university presidents, heads of technology firms, and philan thropists, the summit identified the need for a “clearinghouse for to place results into print than ever before. resources and information to help build knowledge partnerships thirdThere is open-access are also more publication. of us. Each It is professor now less expensivein a major and research faster that can tackle development challenges.” With a leadership team institution has produced more than enough potential replacement that includes the Prime Minister of India’s Advisor on Innovation and TechnologyPublic Information Advisor Infrastructure, to the U.S. Secretary Sam Pitroda, of State, the Nina Director Fedoroff, of the Library of Alexandria, Ismail Serageldin, and the former Science faculty over the past 50 years. Every major research program now hasThe a Web American site. Most Association of these things for werethe Advancement not possible 20 of years Science ago. aGKI bridge responds between to this the call.needs and resources of scientists and agrono- Today, we take them for granted. mists,The so Global that theyKnowledge can access Initiative the assets has the and unique expertise ability needed to create to understand and address the biology of a pest or disease. Although out(AAAS) to colleagues. has just opened a new venture, Science Diplomacy (http:// - diplomacy.aaas.org/). This will greatly increase our ability to reach mate change, their mandate stretches across all areas of science, International Education technology,much of GKI’s and work innovation has been that in the support areas ofeconomic food security development and cli

building collaborations between researchers in the United States In 2011, Brazil initiated the Science Without Borders program and Europepoverty and reduction. individuals Much in East of GKI’s and Southernwork thus Africa far has and been Central in to(http://www.cienciasemfronteiras.gov.br/web/csf-eng/), study abroad in top research laboratories. The intent is to in solve which a Asia, and they are rapidly expanding their geographic reach. By forg- eventually 100,000 of the top students in the country will be sent Recognizing a shortage of science and technology talent, Thailand to solve development challenges pertinent to science, technology, skilled labor shortage and empower the country’s growing economy. ing, enabling, and sustaining knowledge partnerships, GKI hopes studentslaunched in the science Golden and Jubilee technology Program and in ensure 1996 that(http://rgj.trf.or.th/ they receive the and innovation worldwide. For more information on GKI, see: www. latesteng/rgje11.asp). training in advancedThis was intended research tolaboratories increase the around number the of world. Ph.D. Internationalglobalknowledgeinitiative.org. Invasive Species Surveillance - The United States Department of Agriculture (USDA) Animal and

Their intent was to produce 5,000 new Ph.D.s in science and technol (PPQ) mission is to safeguard U.S. agriculture and natural resources ogy in the first 15 years of the program. Plant Health Service (APHIS), Plant Protection and Quarantine’s The Kingdom of Saudi Arabia (KSA) launched a very similar of exotic plant pests. For a proactive and effective safeguarding ap- initiative by founding the King Abdullah University of Science and proach,from the PPQ risks needs associated early warning with the systems entry, regardingestablishment, plant orpests spread that Technology (KAUST) just outside of Jeddah, KSA. The new campus, are not yet established in the U.S. faculty.opened All in teachingSeptember is in 2009, English. is a The graduate four core research areas of university emphasis and are To address this need, PPQ established various systems to monitor presently has some 800 graduate students and an international-

Resources and Energy; Bioscience and Bioengineering; Materials Sci conductsand report plant occurrences pest surveillance of significant by continuously pest events incollecting, other countries. analyz- ences and Applied Mathematics and Computation. The standards set ing,The Exoticdistributing, Pest Information and archiving Collection relevant and open-source Analysis (EPICA) information system beare a equivalent catalyst for to economic Massachusetts development Institute in of the Technology region and or around California the world.Institute Foreign of Technology. graduate Thestudents state-of-the-art are encouraged campus to apply.is intended to for PPQ programs. EPICA monitors mostly English-language sources worldwide for relevant pest information. EPICA searches more The Korean Advanced Institute of Science and Technology (KAIST)- than 90 scientific journals and uses nearly 250 queries to search in Daejeon, Korea was founded in 1971 to achieve the same goals of the Internet for relevant pest news. The information is then filtered KAUST242 in KSA. (http://www.kaist.edu/edu.html) Again, all instruc and analyzed, and the articles areAmerican supplemented Entomologist with background2012

• Winter Araújo W., J. Marcon, W. Maccheroni Jr., J. D. Van Elsas, and J. L. Azevedo. research and information. The EPICA notification is e-mailed to PPQ 2002.J. Appl. Diversity Entomol. of135: endophytic 546-553. bacterial populations and their interac- programs and other plant safeguarding officials throughout the U.S. tion with Xylella fastidiosa once a week. Future Pest Populations Atyame, C. M., N. Pasteur, E. Dumas, in citrus P. plants. Tortosa, Appl. M. andL. Tantely, Environ. N. Microbiol. Pocquet, The state entomologist of California, Robert Dowell, surveyed S.68: Licciardi, 4906-4914. A. Bheecarry, B. Zumbo, M. Weill, and O. Duron. 2011. records of new pests and diseases in California from historic times Cytoplasmic incompatibility as a means of controlling Culex pipiens quinquefasciatus

mosquito in the islands of the south-western Indian until 2000 and found a new occurrence on average of one every 60 Aukema, J. E., D. G. McCullough, B. V. Holle, A. M. Liebhold. K. Britton, andOcean. S. J. PLoS Frankel. Negl. 2010. Trop. Dis. 5: e1440. Dowelldays, or also 6 times reports a year. that His the more rate ofrecent arrival data of newindicates pests that and betweendiseases 2000 and 2010, the rate of arrival has increased to one every 41 days. Azevedo, J. L., and W. L. Araújo. Historical 2003. accumulation of nonindigenous forest- pests in the continental United States. BioScience 60: 886–897. is on the increase elsewhere (Aukema et al. 2010, Kirkendall and Azizi A., A. Arora, A. Markiv, D. J. Lampe, Genetically T. A. Miller, modified and A. crops:S. Kang. environ 2012. - mental and human health concerns. Mut. Res. 544: 223-233. Faccol 2010, Roy et al. 2011). Ribosome display of combinatorial antibody libraries derived from mice Xylella fastidiosa Attributing this increase to a specific cause is difficult, but predic degree of temperature rise in climate change (Fedoroff and Cohen tions of a 10% decrease in crop yield have already been tied to every Bartlett,immunized A. C. 1995. with heat-killed and the selection of MopB-In specificD. A. Richter single-chain and J. Aramour, antibodies. eds., Appl. Proceedings, Environ. Microbiol. Beltwide 78:Cotton2638-2647. Confer- Resistance of pink bollworm to Bt transgenic cotton. news1999, organization,Fedoroff 2010, concluded Fedoroff that and Brown 2004). There is debate about climate change, but Climate Central, a non-profit research and Beard, C. B., R. V. Durvasula, and F. F. Richards. 1998. Bacterial symbiosis ences, pp. 766-768. Memphis TN: National Cotton Council. a result of greenhouse gas emissions. The science is equally “The science clearly shows that climate is changing largely as Beardin arthropods C. B., E. M. Dotson, and the P. control M. Pennington, of disease S. transmission. Eichler, C. Cordon-Rosales, Emerg. Infect. andDis. 4:R. 581-591. V. Durvasula. 2001. Bacterial symbiosis and paratransgenic Earth’sclear that biosphere without inrapid all sortsand drastic of ways cutbacks ... some in of greenhouse these changes gas emissions, the changes are likely to threaten life, property and Beard C., C. Cordon-Rosales, and R. Durvasula. 2002. Bacterial symbionts ofcontrol the triatominae of vector-borne and their Chagas potential disease. use Int. in J. controlParasitol. of 31:Chagas 621-627. Disease are already happening.” (M. D. Lemonick 2012) (http://www climatecentral.org/)Given this prognosis, and the increase in pest occurrence coupled Ben-Ami E., B. Yuval, and E. Jurkevitch. 2010. - transmission. Annu. Rev. Entomol. 47: 123-141.Ceratitis capitata (Diptera: Manipulation of the micro as one of the new technologies, the apparent decrease in investment Blua,biota M. J., of R. mass-reared A. Redak, D. Mediterranean J. W. Morgan, fruitH. S. Costa.flies 2001. - inwith agricultural few new tools research and seemslack of toenthusiasm be happening for genetic at exactly modification the wrong tivityTephritidae) of two Homalodisca improves sterile male sexual performance. ISME J. 4:28–37. time—all the more reason to develop international entomology and Xylella fastidiosa Seasonal flight ac coordinate efforts globally. Bradbury, J. F. 1991. species (Homoptera: Cicadellidae) that spread in southern California. J. Econ. Entomol. 94: 1506-1510. CMI Descriptions of Pathogenic Fungi and Bacteria. Acknowledgements Brelsfoard, C. L., and S. L. Dobson. 2009. Wolbachia-based strategies to No. 105, CAB International, Wallingford, UK.

control insect pests and disease vectors. Asia Pac. J. Mol. Biol. Biotechnol. This opinion article was based on a presentation by TAM of the Brelsfoard, C. L., and S. L. Dobson. 2011. An update on the utility of Wol- bachia17: 55-63. for controlling insect vectors and disease transmission. Asia Pac. same title at the Second International Symposium on Insect Bio- ofIndustry, this report 16-19 and August added 2012, more Yecheon, recent informationKorea. on eradication. Bustillo P., A. E., R. Cárdenas M., D. A. Villalba G., P. Benavides M., J. Robert Staten offered amendments on the pink bollworm section OrozcoJ. Mol. Biol. H., andBiotechnol. F. Posada. 19: 1998.85-92. Hypothenemus hampei - Manejo integrado de la broca del café Sara Farley approved the descriptions of Global Knowledge Initiative. the Secretary in the U.S. Department of State suggested amendments Castle, S. J., F. J. Byrne, J. L. Bi,(Ferrari) and N. en C. Toscano.Colombia. 2005. Centro Spatial Nacional and temporalde Inves Andrew Reynolds and Eric Bone in the office of Science Advisor to distributiontigaciones de of Café imidacloprid (Cenicafé). and Chinchiná, thiamethoxam Colombia. in citrus and impact on Homalodisca coagulata to the GKI and abstract sections. Chang, C. J., M. Garnier, L. Zreik, V. Rossetti, and J. M. Bove. 1993. Culture References Cited and serological detectionWells of the populations. xylem-limited Pest bacterium Manag. Sci. causing 61: 75-84. citrus Abdul Matin, A. S. M., J. E. Wright, and T. B. Davich. 1980. Effect of low Xylella fastidiosa. levels of gamma irradiation on longevity and sterility of the boll weevil. Chen,variegated C.T. 1974. chlorosis Sugarcane and its white identification leaf disease as a strainin Thailand of and Taiwan. Ahmed, F. E. 2003. Curr. Microbiol. 27: 137-142. Southwestern Entomol. 5: 112-117. Chen, J., R. L. Jarret, X. Qin, J. S. Hartung, C. J. Chang, and D. L. Hopkins. Almeida, R. P. P. and A.Genetically H. Purcell. modified 2003. Transmission probiotics in of foods. Xylella Trends fastidiosa in 2000.Sugarcane Pathologists’ NewsletterXylella fastidiosa 11/12: 23. toBiotechnol. grapevines 21: by 491-497. Homalodisca coagulata Crotti, E, A.16SrDNA Balloi, C.analysis Hamdi, of L. Sansonno, M. .Marzorati, Syst. Appl. E.Microbiol. Gonella, 23: G. Anonymous. 1984. (Hemiptera: Cicadellidae). J. Favia,349-354. A. Cherif, C. Bandi, A. Alma, and D. Daffonchio. 2012. RegionEcon. Entomol. of the United 96: 264-271. States. University of California, Division of Agricul- symbionts: a resource for the management of insect-related problems. Integrated Pest Management for Cotton in the Western Microbial Anonymous. 2000. da Silva, F. R., A. L. Vettore, E. L. Kemper, A. Leite, and P. Arruda. 2006. ture and Natural Resources, Publication 3305, 144 pp. FastidianMicrob. Biotechnol. gum: the Xylella 5: 307-317. fastidiosa exopolysaccharide possibly involved Apostolaki, Α., Livadaras, CVC: Sintomas I., Saridaki, estao A., mais Chrysargyris, graves. Revista A., FundecitrusSavakis, C., Bourtzis,99: 8-9. K. 2011 Bactrocera oleae Dandekar, A. M., H. Gouran, A. M Ibanez, S. L. Uratsu, C. B. Aguero, S. with Wolbachia: towards a symbiont-based population control strategy. McFarland,in bacterial pathogenicity. Y. Borhani, A. FEMS Feldstein, Microbiol. G. Bruening, Lett. 203: R. 165-171. Nascimento, L. . Transinfection of the olive fruit fly

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• R. Goulart, P E. Pardington, A. Chadhary, M. Norvell, E. Civerolo, and Hoffmann, A. A., B. L.Montgomery, J. Popovici, I. Iturbe-Ormaetxe, P. H. G. Gupta. 2012. An engineered innate immune defense protects grape- Johnson, F. Muzzi, M. Greenfield, M. Durkan, Y. S. Leong, Y. Dong, H. Cook, J. Axford, A. G. Callahan, N. Kenny, C. Omodei, E. A. McGraw, Della-Coletta, F. H., M. A. Takita, A. A. Souza, C. I. Aguilar-Vildoso, and P. A. Ryan, S. A. Ritchie, M. Turelli, and S. L. O’Neill. 2011. Successful M.vines A. Machado.from Pierce’s 2001. disease. Differentiation Proc. Natl. Acad.of strains Sci. USAof Xylella 109: 3721-3725.fastidiosa by establishment of Wolbachia in Aedes populations to suppress dengue

Hopkins, D. L. 1989. Xylella fastidiosa: xylem-limited bacterial pathogen of Derricka variable K. S., numberand L. W. of Timmer. tandem repeat2000. analysis.Citrus blight Appl. and Environ. other diseases Microbiol. of plants.transmission. Ann. Rev. Nature Phytopathol. 476: 454-457. recalcitrant67: 4091-4095. etiology. Ann. Rev. Phytopathol. Hopkins, D. L., and A. H. Purcell. 2002. Xylella fastidiosa: Cause of Pierce’s Dhurua, S., and G. T. Gujar. 2011. disease of grapevine and other27: emergent 271-290. diseases. Plant Disease Pectinophora gossypiella38: (Saunders) 181-205. (Lepidoptera: Field-evolved resistance to Bt toxin Cry1Ac Jaramillo, J. 2008. Biology, ecology and biological control of the coffee berry86: Durvasula,in the pink R. bollworm,V., A. Gumbs, A. Panackal, O. Kruglov, S. Aksoy, R. B. Mer- borer,1056-1066. Hypothenemus hampei (Ferrari) (Coleoptera: Curculionidae: Sco- rifield,Gelechiidae), F. F. Richards, from India. and Pest C. B. Manag. Beard. 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Sugar Tech 3(1&2): 55-58. a model for paratransgenic control of disease transmission. In the phytopathogenic bacterium Xylella fastidiosa, causal agent of citrus st Ed.), CRC, Boca Raton, Florida. Interaction between endophytic bacteria from citrus plants and Fedoroff, N. V. 2010. Bourtzis K,- Lambais, M. R., M. H. S. Goldman, L. E. A. Camargo, and G. H. Goldman. Miller TA (Eds.) Insect Symbiosis (Vol I, 1 2000.variegated A genomic chlorosis. approach Lett. Appl. to theMicrobiol. understanding 39: 55-59. of Xylella fastidiosa Fedoroff, N. V., and J. TheE. Cohen. past, present 1999. Plants and future and population: of crop genetic is there modifica time? tion. New Biotechnol. 27: 462-465. Lampe, D., C. Lauzon, and T. A. Miller. 2006. Use of the E. coli Fedoroff, N. V., and N. M. Brown. 2004. secretionpathogenicity. system Curr. in Opin.bacteria Microbiol. designed 3: for459-462. symbiotic control of Pierce’s Proc. Natl. Acad. Sci. USA 96: 5903-5907. disease in grapevines and sharpshooters. Pierce’s Diseaseα-hemolysin Research Freitag, J. H. 1951. Mendel in the Kitchen: a scientist’s determinedview of genetically by insect modified transmission. foods. Joseph Phytopathol. Henry Press, Washington, DC. Lampe, D., A. Kang, and T. A. Miller. 2007. Native secretion systems for Fryxell, K. J., T. A. Miller. Host range 1995. of Autocidal the Pierce’s biological disease control:virus of Agrapes general as theSymposium, grapevine 27-29 endophyte Nov 2006, Pantoea San Diego,agglomerans CA, Proceedings, useful for pp.the 240-241. delivery strategy for insect control based on genetic transformation41: 920-934. with a highly of anti-Xylella effector proteins. Pierce’s Disease Research Symposium, conserved gene. J. Fundecitrus. 2005. Laranjeira, F. F., J. Pompeu Jr., R. Harakava, J. O. Figueiredo, S. A. Car- Econ. Entomol. 88: 1221-1232. valho,12-14 Dec and 2007, H. D. San Coletta-Filho. 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C hagas,Int. J. Syst. and Bacteriol. V. Rossetti. 48: 1991.1153-1169. Citrus variegated chlorosis: a new destructive disease of citrus Gai, C. S., F. Dini-Andreote, F. D. Andreote, J. R. S. Lopes, A W. L. Raújo, in Brazil. T.control A. Miller, strategy J. L. ofAzevedo, citrus variegated and P. T. Lacava.chlorosis. 2011. J. Microbiol. Endophytic 47: 448-454. bacteria Lemonick, M. D. 2012. Science over hype. Los Angeles Times Op-Ed, 2 Citrus Industry 72: 12-13. of Xylella fastidiosa subsp. pauca Li, W. B., L. C. Donadio, M. J. G. Beretta, V. Rosetti, and O. R. Sempionato. associated to sharpshooters (Hemiptera: Cicadellidae), insect vectors 1997a.August 2012,Practical p. A13. methods of resistance evaluation of citrus varieties to Goodwin, P., and A. H. Purcell. 1992.. J. Plant Pathol. and Microbiol. 2: 109.- mentdoi:10.4172/2157-7471.1000109. (2nd Ed.), University of California, Division of Agriculture and Natural Pierce’s Disease. Grape Pest Manage Li W.citrus B., L. variegated C. 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D. chlorosis Pria Jr., (CVC) P. M. of Lacava, sweet orangeX. Qin, ‘Pera’ and (J. S. Hartung. L. Osbeck). 2003. transmission of sugarcane white leaf phytoplasma in the insect vector PresenceProc. Intern. of XylellaSoc. Citricul. fastidiosa 1: 286-289. in sweet orange fruit and seeds and its Matsumuratettix hiroglyphicus transmission to seedlings. Phytopathol. Hanboonsong, Y., W.Ritthison, C. Choosai, and P. Sirithorn. 2006. Lopes, J. R. S., M. J. G. Beretta, R. Harakava, R. P. P. Almeida, R. Krügner, Transmission of sugarcane white (Matsumura). leaf phytoplasma Insect Mol. by Biol. Yamatotettix 11: 97-103. and A. Garcia Júnior. 1996. 93: 953-958. - flavovittatus rinhas do agente causal da clorose variegada dos citros, Xylella fastidiosa. Hartung, J. S., J. Beretta, R. H. Brlansky, J. Spisso, and R. F. Lee. 1994. Confirmação da transmissão por cigar Citrus variegated, a new chlorosis leafhopper bacterium: vector. J. Econ.axenic Entomol. culture, 99: pathogenicity, 1531-1537. Matsumoto T., C. S. Lee, and W. S. Teng. 1968. Studies on sugarcane white leaf and serological relationships with other strains of Xylella fastidiosa. Fitopatologia Brasileira 21: 343. Phytopathol. Epitettix hiroglyphicus disease of Taiwan with special reference to transmission by a leafhopper, 84: 591-597. . Mats. Pro. Soc. Sugarcane Technol. 13: 1090-1099. 244 American Entomologist Winter 2012

• Miller, T. A. 2007. Symbiotic control in agriculture and medicine. Symbiosis Homalodisca and of H. vitripennis as the name for glassy-winged sharp-

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Rossetti, V., M. Garnier, J. M. Bove, M. J. G. Beretta, A. R. R. Teixeira, J. A. Wells,symbiotic J. M., B. control C. aju, H.-Y..Hung,of Sugarcane W. White G. Weisburg, Leaf Disease. L. Mandelco-Paul, Appl. Environ. and Mi Quaggio,12: 325-336. and J. D. deNegri. 1990. Presence de bacteries dans le xyleme D.crobiol. J. Brenner. 78: 6804-6811. 1987. Xylella fastidiosa gen. nov., sp. nov: Gram-negative, d’orangers atteints de chlorose variegee, unenovelle maladie des agrumes xylem limited, fastidious plant bacteria related to Xanthomonas

Roy, H. E., D. B. Roy, and A. Roques. 2011. Wongkaew, P., Y. Hanboonsong, P. Sirithorn, C. Choosai, S. Boonkrong,spp. Int. arthropodau Brasil. C. predators R. Acad. Sci. and Paris parasites Ser. III. established 310: 345-349. in Europe. BioControl T.J. Syst. Tinnangwattana, Bacteriol. 37: 136-143. R. Kitchareanpanya, and S. Damark. 1997. Dif- Inventory of terrestrial alien ferentiation of phytoplasma associated with sugarcane and gramineous Schaad, N. W., E. Postnikova, G. Lacy, M. Fatmi, C.-J. Chang. 2004. Xylella weed white leaf disease and sugarcane grassy shoot disease by RFLP and fastidiosa56: 477–504. subspecies: X. fastidiosa subsp. piercei, subsp. nov., X. fastidiosa subsp. multiplex, subsp. nov., X. fastidiosa subsp. pauca, subsp. nov. Syst. Zabalou, S., A. Apostolaki, I. Livadaras, G. Franz, A. S. Robinson, C. Sa- vakis,sequencing. and K. Theor. Bourtzis. Appl. 2009. Genet. 95: 660-663. - Simpson, A. J. G. , F. C. Reinach, P. Arruda, F. A. Abreu, M. Acencio, R. ible males from a Ceratitis capitata genetic sexing strain. Entomologia Alvarenga,Appl. Microbiol. L. M. 27: C. 290-300.Alves, J. E. Araya, G. S. Baia, and C. S. Baptista. Incompatible insect technique: incompat 2000. The genome sequence of the plant pathogen Xylella fastidiosa. Zabalou, S., M. Riegler, M. Theodorakopoulou, C. Stauffer, C. Savakis, andExperimentalis K. Bourtzis. et 2004. Applicata. Wolbachia 132: 232-240.-induced cytoplasmic incompatibility Tabashnik, B. E., A. L. Patin, T. J. Dennehy, Y. B. Liu, Y. Carrière, M. A. Sims, : andNature L. Antilla.406: 151-159. 2000. Frequency of resistance to Bacillus thuringiensis as a means for insect pest population control. Proc. Natl. Acad. Sci. 101 Kostas15042-15045. Bourtzis is at the University of Western Greece, Agrinio, Greece but in Takiya,in field D. M.,populations S. H. McKamey, of pink bollworm.and R. R. Cavichioli.Proc. Natl. Acad. 2006. Sci. USA 97: 12980-12984. Validity of September 2012 will be attached to the Insect Pest Control Laboratory, Joint American Entomologist Volume 58, Number 4 245

• Steven Crook operates the FAO/IAEA Division of Nuclear Techniques in Food and Agriculture, Vienna, Austria. He can be reached at [email protected]. Daniele Daffonchio Exotic Pest Information Collection and Analysis (EPICA) program at USDA- APHIS. He can be reached at [email protected]. Ravi Durvasulais at University of Milan, DeFENS, Department of Food, Environmental and Nutritional Sciences. He can be reached at [email protected] Hanboonsong is on the faculty of the University of New Mexico Medical School in Albuquerque, NM. He can be reached at [email protected]. Fran- cisco Infante is is at in the the Department Department ofof Entomology,Entomology atEl KhonColegio Kaen, de la University, Frontera Khon Kaen, Thailand. She can be reached at [email protected]. mx. Paulo T. Lacava Sur, 30700 Tapachula, Chiapas, Mexico. He can be reached at finfante@ecosur. edu.br. Thomas A. Miller is at isInstitute at the Entomologyof Natural Sciences, Department, Federal UC UniversityRiverside, of Alfenas, Alfenas, MG, Brazil. He can be reached at [email protected] E. Vega is at the Sustainable Perennial Crops Laboratory, United States Department of

California. He can be reached at [email protected].

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comprehensive review of the North American short-range physical and/or chemical in involved presumably is cicada fauna that provides information on behavior The photographed. been before never has it but MAS,

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The images are of an Old World epipaschiine moth (Pyralidae: (Pyralidae: moth epipaschiine World Old an of are images The Hardcover, 227 pages, 2012. answer. it? is What ISBN: 978-0-9776209-6-8 ESA Members: $79.95 Nonmembers: $99.95 Order online at the ESA Bookstore at: http:// www.entsoc.org/pubs/esa-bookstore CALL FOR ARTICLES American Entomologist invites all members to submit manuscripts for upcoming issues. Contact the editor with questions and interests at: [email protected].

246 American Entomologist Winter 2012

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