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Asian Citrus Psyllid, Diaphorina Citri, Vector of Citrus Huanglongbing Disease David G

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Asian Citrus Psyllid, Diaphorina Citri, Vector of Citrus Huanglongbing Disease David G DOI: 10.1111/eea.12025 MINI REVIEW Asian citrus psyllid, Diaphorina citri, vector of citrus huanglongbing disease David G. Hall1*, Matthew L. Richardson1, El-Desouky Ammar1 & Susan E. Halbert2 1United States Department of Agriculture, Agricultural Research Service, US Horticultural Research Laboratory, 2001 South Rock Road, Fort Pierce, FL 34945, USA, and 2Florida Department of Agriculture and Consumer Services, Division of Plant Industry, 1911 SW 34th Street, Gainesville, FL 32614, USA Accepted: 29 October 2012 Key words: biological control, host plant resistance, vector interactions, citrus greening, Liberibacter, Hemiptera, Psyllidae, integrated pest management, IPM Abstract The Asian citrus psyllid (ACP), Diaphorina citri Kuwayama (Hemiptera: Psyllidae), is an important pest of citrus because it transmits phloem-limited bacteria [Candidatus Liberibacter spp., notably Ca. L. asiaticus (LAS)] associated with huanglongbing (HLB; citrus greening disease), currently consid- ered the world’s most serious disease of citrus. Asian citrus psyllid transmits LAS in a persistent man- ner and, although the rate of LAS transmission by ACP individuals usually is low, HLB can spread rapidly in a citrus grove and the geographic range of the disease is expanding, threatening citrus industries in new areas. Intensive chemical control of ACP is the primary management strategy cur- rently advocated for HLB, but this strategy is costly, unsustainable, and generally ineffective. The sci- entific community is searching aggressively for solutions to HLB on many fronts, but it could still be years before solutions are found and implemented. Plant resistance to LAS is one area of research being pursued, whereby traits that confer resistance are identified and incorporated into citrus germ- plasm through conventional or transgenic methods. It remains to be seen if a solution to HLB can be found that specifically targets ACP, but research on ACP has been stepped up in a number of areas, notably on ACP–LAS–plant interactions, on host plant resistance to ACP, and on molecular methods of silencing ACP genes to induce mortality or to block its ability to transmit HLB-causing bacteria. Advancements in these and other research areas may depend greatly on a better understanding of basic ACP biology and vector–pathogen–host plant interactions at the molecular, cellular, and community levels. Here, we present an updated review of ACP and HLB with an emphasis on the problem in Florida. distribution, food plants, biology and ecology, behavior, Introduction damage, and control. Asian citrus psyllid and HLB have The Asian citrus psyllid (ACP), Diaphorina citri Kuway- since spread to citrus-growing regions nearly worldwide ama (Hemiptera: Psyllidae), is an important pest of citrus (Halbert & Manjunath, 2004; Halbert & Nunez,~ 2004; because it transmits phloem-limited bacteria (Candidatus Pluke et al., 2008), increasing research efforts on ACP and Liberibacter spp.) strongly implicated in huanglongbing HLB over the past 85 years and expanding our knowledge (HLB; citrus greening disease), which is the world’s most of the insect, the disease, and their interactions. More serious disease of citrus (McClean & Schwartz, 1970; Bove, recent reviews of ACP or HLB were compiled by Halbert 2006). Husain & Nath (1927) presented an early, detailed & Manjunath (2004), Bove (2006), Hall (2008a,b, 2010), review of ACP in India, which touched on systematics, and Gottwald (2010). Asian citrus psyllid invaded many countries in Central and North America starting in the 1990s and HLB subse- quently has been detected in the USA, eastern and western *Correspondence: David G. Hall, United States Department of Agri- culture, Agricultural Research Service, US Horticultural Research Mexico, Belize, Puerto Rico, and Cuba. Following the dis- Laboratory, 2001 South Rock Road, Fort Pierce, FL 34945, USA. covery of HLB in Florida during 2005, a three-component E-mail: [email protected] management program against HLB was advocated initially © 2012 The Authors Entomologia Experimentalis et Applicata 146: 207–223, 2012 Entomologia Experimentalis et Applicata © 2012 The Netherlands Entomological Society 207 208 Hall et al. and implemented by some citrus growers: intensive chem- the pathogen–host plant relationship, research has been ical control of ACP, aggressive removal of HLB-infected expanded that targets ACP–pathogen or ACP–host plant trees, and planting disease-free nursery stock (Su et al., interactions. This review presents an updated summary of 1986; Gottwald, 2007; Hall & Gottwald, 2011). Florida information on ACP with an emphasis on experiences in imposed strict nursery compliance agreements to help Florida citrus. ensure disease-free nursery stock, but this reduced the number of qualified sources for young trees and inflated Geographical distribution and invasion history prices. Hundreds of thousands of trees in Florida that probably were infected before the management program The geographical origin of ACP is thought to be south- was implemented were removed from groves. The extent western Asia (Halbert & Manjunath, 2004; Beattie et al., to which the three-tiered management program negates 2009). According to Beattie et al. (2009), all evidence con- incidence and spread of the disease may depend largely on cerning the origin of ACP supports that it evolved in India. levels of inoculum within and around a grove. Within less Asian citrus psyllid occurs in China (incl. Hong Kong), than 7 years of the discovery of HLB in Florida, most India, Myanmar, Taiwan, Philippine Islands, Malaysia, growers found the three-tiered program too expensive, Indonesia, Sri Lanka, Pakistan, Thailand, Nepal, Ryukyu were reluctant to remove infected trees that were produc- Islands (Japan), Afghanistan, Saudi Arabia, Reunion, and tive, and consequently abandoned efforts to remove trees Mauritius (Mead, 1977; Halbert & Manjunath, 2004). (Spann et al., 2011) unless they were non-productive. Asian citrus psyllid has been in South America since the Regional increases in inoculum loads therefore have 1940s, invading Brazil and subsequently Argentina and occurred across Florida. More recently, a number of grow- Venezuela, and it invaded the West Indies (Guadeloupe), ers have implemented increased tree nutritional programs Abaco Island, Grand Bahama Island, Cayman Islands, and hoping to sustain the productivity of infected trees (Hall & Florida, USA, in the 1990s (Tsai & Liu, 2000; Halbert & Gottwald, 2011; Spann et al., 2011). Empirical observa- Nunez,~ 2004). During 2001, ACP was found in the tions suggest that some nutritional programs in combina- Dominican Republic, Cuba (Halbert & Nunez,~ 2004), tion with insecticide sprays against ACP may help sustain Puerto Rico (Pluke et al., 2008), and Texas, USA (French the productivity of infected trees at least in some situa- et al., 2001). Asian citrus psyllid has been reported more tions, but as of yet there have been no published research recently in many new areas in the Americas, including reports supporting these observations. In fact, the only Mexico, Costa Rico, Belize, Honduras, and the states of published report we are aware of indicates that none of Alabama, Arizona, California, Georgia, Louisiana, Missis- several nutritional programs had any value for sustaining sippi, and South Carolina in the USA [see Halbert et al. the productivity of infected trees (Gottwald et al., 2012). (2010) for a recent summary]. Solutions to HLB are needed desperately and must be Phylogeographic and genetic studies of ACP popula- implemented soon to ensure the sustainability of commer- tions in the Americas indicated that two founding events cial citrus. Novel tactics are needed for areas such as Flor- of ACP probably occurred, one in South America and one ida where the HLB problem is severe, as little or no in North America (De Leon et al., 2011). Phylogenetic progress has been made using more conventional strate- analyses among worldwide collections of ACP suggested gies, such as classical biological control by insect predators that there are two major haplotype groups of ACP with and parasitoids. Plant resistance to the HLB bacterium is preliminary geographic bias between southwestern and one area of research being pursued vigorously by plant southeastern Asia (Boykin et al., 2012). The recent inva- breeders and pathologists, whereby traits that confer resis- sion of ACP into the USA and Mexico originated from tance are being identified and incorporated into citrus only the southwestern group, but both the southwestern germplasm through conventional or transgenic methods. and southeastern groups invaded separate locations in The United States Department of Agriculture – Agricultural Brazil. A haplotype unique to the Caribbean (Puerto Rico Research Service (USDA-ARS) in Fort Pierce, FL, USA, is and Guadeloupe) was found, indicating that a distinction generating thousands of citrus plants transformed to exists between tested populations in the USA and the express different antimicrobial peptides known to have Caribbean. Additional investigations into the phylogenetic activity against plant pathogens in hopes of an HLB solu- relationships among worldwide populations of ACP might tion, and a high throughput screening program is in place be worthwhile, as research by Boykin et al. (2012) did not for faster evaluations. Curative therapies for HLB-infected distinguish mitochondrial DNA from nuclear DNA, poly- trees are being investigated, including infusion of antibiot- merase chain
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