Insect Vectors of Phytoplasmas and Their Control

Home , Fieberiella, Orosius (leafhopper), Phytoplasma

Bulletin of Insectology 60 (2): 169-173, 2007 ISSN 1721-8861

Insect vectors of phytoplasmas and their control – an update

Phyllis G. WEINTRAUB Agricultural Research Organization, Gilat Research Center, D.N. Negev, Israel

Abstract

Phytoplasmas are phloem-limited, insect-transmitted, plant pathogenic bacteria that are responsible for hundreds of diseases world-wide. Because transmission occurs quickly, plants become infected before insecticides can act on the vector. The single most effective means of controlling the vector is to cover plants with insect exclusion netting; however, this is not practical for most commercial crops. Because of these limitations, researchers are turning to genetic manipulation of plants to affect vector populations and pathogen transmission. These novel control schemes include symbiont control (SyBaP), plant lectins, and systemic acquired resistance (SAR).

Key words: Taxonomy, symbiont control, plant lectins, systemic acquired resistance

Introduction fected plants. The feeding duration necessary to acquire a sufficient titre of phytoplasma is the acquisition access Phytoplasmas are important phloem-limited, insect- period (AAP), which can be as short as a few minutes, transmitted pathogenic agents causing close to a thou- but is generally measured in hours; the longer the AAP, sand diseases, many of which are lethal, in hundreds of the greater the chance of transmission (Purcell, 1982). plant species. They are non-cultivable degenerate gram- However, it is unknown how phytoplasma titre in plants positive prokaryotes in the class Mollicutes. A large affects the AAP. The period of time that elapses from body of research has accumulated in the past 20 years initial acquisition to the ability to transmit the phyto- that addresses the biology, ecology, vector relationships plasma is known as the latent period (LP) and is some- and epidemiology of crop diseases caused by phyto- times referred to as the incubation period. During the plasmas, which has been recently reviewed by Christen- LP, the phytoplasmas move through, and replicate in, sen et al. (2005), Weintraub and Beanland (2006), and the competent vector’s body. There are some specific Bertaccini (2007). In this review, an update of recent leafhopper-phytoplasma relationships; for example: developments, focusing primarily on insect vectors and Macrosteles striifrons Anufriev can transmit onion yel- on their control is provided. lows, but not rice yellow dwarf phytoplasmas, while Nephotettix cincticeps Uhler can transmit rice yellow dwarf but not onion yellows phytoplasmas. Taxonomy The molecular factors related to the movement of phytoplasmas through the various insect tissues are still un- The single most successful order of insect phytoplasma clear; however progress is being made. Oshima et al. vectors is the Auchenorrhyncha. They are efficient vec- (2002) constructed phage libraries of onion yellows tors of phytoplasmas because: nymphs and adults feed phytoplasma and determined the sequence of 153 inde- similarly and are in the same physical location, often, pendent clones and eventually Oshima et al. (2004) es- both immatures and adults can transmit phytoplasmas, timated the total phytoplasma genome size to be 860 kb, they feed specifically in phloem cells, and phytoplasmas and determined the function of some genes based on are propagative and persistent in them. Within the comparisons with other known bacterial gene functions. groups of phloem-feeding insects only a small number, Among the genes elucidated was an immunodominant primarily in three taxonomic groups, have been con- membrane protein (Amp) that Suzuki et al. (2006) de- firmed as vectors of phytoplasmas; Cicadellidae, Ful- termined interacts with microfilament complexes in goromorpha (in which four families of vector species muscle cells surrounding the intestinal tract of the insect are found), and two genera in the Psyllidae. In Wein- and seems to be responsible for vector-phytoplasma traub and Beanland (2006), 92 confirmed vector species specificity. were listed; table 1 contains an additional five con- Although grapevines are subject to phytoplasma infec- firmed vector species, and some previously known vec- tion on almost every continent, it has been notoriously tors with new phytoplasma associations. difficult to confirm vector status. Using an old method – injection of pathogen directly into the hemocoel of potential vectors – Bressan et al. (2006) were able to select Phytoplasma specificity/acquisition potential new vector candidates and eliminate others from consideration. Scaphoideus titanus Ball, a leaf- Insect vectors feed specifically in phloem cells, obtain- hopper imported from North America, is the natural ing nutrition from free amino acids and sugars. Phyto- vector of “flavescence dorée” (FD) in Europe. By inject- plasmas are acquired passively during feeding in in- ing FD phytoplasma into a number of potential vector

Table 1. Confirmed phytoplasma vectors, taxonomy, pathogen association, host plant and distribution.

Disease Association/ Vector Species Reference Host Plants Distribution Phytoplasma group DELTOCEPHALINAE Oregon, Munyaneza et al., Columbia basin potato Circulifer tenellus (Baker) Beets, potatoes, weeds Washington 2007 purple top USA Tedeschi and Apple proliferation/ Fieberiella florii Stål Apple Italy Alma, 2006 16SrX-A Watercress, plantain, Macrosteles sp. Borth et al., 2006 16SrI-B group Hawaii, USA lettuce Neoaliturus fenestratus Lettuce phyllody, wild Lettuce, wild lettuce, Salehi et al., 2006 Iran (Herrich-Schäffer) lettuce phyllody (16SrIX) periwinkle, sowthistle Laboucheix et al., Orosius cellulosus Lindberg Cotton phyllody/16SrII-F Cotton Africa 1972 Orosius lotophagorum Behncken, 1984 Little leaf disease Bellvine Australia (Kirkaldy) Witches’ broom of sweet " Shinkai, 1964 Sweet potato Japan potato Orosius orientalis Mirzaie et al., Garden beet witches’ Beets Iran (Matsumura) 2007 broom Yamatotettix flavovittatus Hanboonson et Sugarcane white leaf Sugarcane Thailand (Matsumura) al., 2006 disease FULGORIDEA CIXIIDAE Reptalus panzeri (Löw) Jovic et al., 2006 Maize redness Maize Serbia

species, a membracid and a cercopid, they were able to back (causing 10-100% tree death per season in Austra- demonstrate that three cicadellid species have the poten- lia), yellow crinkle (causing 2-27% tree death/season) tial to transmit FD. Additionally, the three newly identi- and mosaic (causing 5-8% tree death/season). Manage- fied species were able to acquire FD from infected bro- ment practices consisted of rouging yellow crinkle- and ad beans and transmit them to healthy plants in the labo- mosaic-infected trees and ratooning (pruning by remov- ratory, further strengthening the supposition that they ing symptomatic shoots and allowing lateral shoot de- could transmit the phytoplasma under field conditions. velopment) dieback-infected trees to reduce the inocu- Since 13 species were not able to transmit FD even by lum load (Guthrie et al., 1998). More recently, Walsh et circumventing the midgut barrier, there is little chance al., (2006) demonstrated that the pathogen vectors could that they could transmit phytoplasmas in a natural set- be 100% controlled by covering the trees with insect ting. This technique narrows the potential list of vectors exclusion netting. Screening was compared to systemic and may lead to greater success in determining vector insecticide (imidacloprid) treatments and non-treated status. control – there was no difference in disease incidence Vector-host plant interactions play an important role between the insecticide and control trees. However, in limiting or expanding phytoplasma spreading. these authors concluded that due to the cost of erecting a Broadly polyphagous vectors have the potential to in- screen support structure and the reduced pollination oculate a wider range of plant species, depending on the within the screening, only cash-crops could justify the susceptibility of each host plant. Several studies have expense. shown that insects that normally do not feed on certain Screening is the only method to attain excellent vector plant species can acquire and transmit phytoplasma to control; however, its applicability is so severely limited those plants under laboratory conditions. Hence, in due to the logistics of large scale agriculture in major many cases, the plant host range of a vector, rather than crops – sugar cane, corn, rice, fruit trees, and grapes – lack of phytoplasma-specific cell membrane receptors, that its use can not even be contemplated. On the other will limit the spread of phytoplasma by that species. hand, conventional insecticides, even when frequently used (e.g. Wally et al., 2004), will not control the ap- pearance of disease because pathogen transmission oc- Traditional control curs faster than insecticides can act, and there is often a constant influx of new vectors from surrounding habi- Traditional vector control methods are insufficient to tats. At best, use of insecticides might help control vec- control the disease (Weintraub and Beanland, 2006). tor populations, and thus reduce intra-crop transmission. The most reliable means of controlling vectors is by Kaolin, a nonabrasive fine-grained aluminosilicate min- covering the crop with insect-proof screening. Papaya is eral, applied as a particle film, is a new version of a very subject to three different phytoplasma diseases (Guthrie old type of inorganic chemical control which may et al., 1998), the latter two being chronic diseases: die- prove to be useful. The glassy-winged sharpshooter,

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Homalodisca coagulata (Say), is a vector of the bacte- Plant lectins rium, Xylella fastidiosa Wells et al. which causes Pier- ce’s disease in grape, and a host of other diseases in o- As stated above, phytoplasma vectors feed specifically ther crops. Initial work by Puterka et al. (2003) demon- in phloem cells, obtaining nutrition from free amino ac- strated that kaolin protected grape plants from feeding ids and sugars. As such, the activity of carbohydrate- and oviposition by the leafhopper, by physically coating binding plant lectins, which would directly affect vector the plant with a mineral film. Tubajika et al. (2007) nutrition and/or be toxic, has been examined as a means showed that grapevines treated with kaolin were less of controlling vectors. These lectins are usually inserted likely to become infected with the bacteria and fewer into the target plant by Agrobacterium rolC (from A. leafhoppers were found in treated fields. While chemi- rhizogenes), specific for expression of the lectins and cal control of vectors likely will continue for the fore- stability in the phloem (Saha et al., 2006). There are two seeable future, vector management will slowly shift to plant lectins that have shown efficacy in vectors: snow- genetic manipulation of crops. drop lectin (Galanthus nivalis agglutinin, GNA) (Na- gadhara et al., 2004) and a 25-kDa homodimeric lectin, Allium sativum leaf lectin (ASAL) (Dutta et al., 2005). Symbiont control The mechanism of GNA is complex and not fully un- derstood: it is not degraded by midgut proteases; it A new and potentially very powerful tool for controlling binds to D-mannose in the midgut of insects and is pathogen transmission is through the manipulation of transported across the epithelial barrier to the circula- symbiotic bacteria. Many arthropods carry a diverse as- tory system (Fitches et al., 2001). In bioassay, feeding sembly of symbiotic microorganisms that are maternally on GNA rice caused 90% mortality in Sogatella furcif- inherited and which have major effects on their hosts. era (Nagadhara et al., 2004) and 29% and 53% mortal- These bacteria can be genetically modified to prevent ity in Nephotettix virescens Distant and Nilaparvata the transmission of pathogens; arthropods containing lugens Stål, repsectively (Foissac et al., 2000). ASAL these transformed bacteria are called paratransgenic. To has a high degree of sequence similarity to GNA (Ma- develop such symbiotic-control methods it is necessary jumder et al., 2004); however, it may decrease the per- to first identify microorganisms in the target vector meability of the gut membrane and seems to be effec- whose characteristics appear promising: 1) the symbiont tive at much lower levels than GNA (Biandyopadhyay is present in the same organs as the pathogen, and 2) the et al., 2001). A major receptor of GNA in the phyto- symbiont exhibits a potential to spread rapidly into the plasma vector N. lugens is 26 kDa ferritin, thus ASAL host populations. Once identified, cultured and modi- may also be involved in iron homeostatasis (Du et al., fied, these bacteria can compromise transmission: by 2000). reducing vector competence, by expressing a gene One of the primary functions of spider venom is to pa- product that could kill the pathogen, by inducing cyto- ralyze prey; often these toxins are polypeptides that tar- plasmic incompatibility, and causing a high offspring- get the nervous system of the host. Some of these poly- mortality rate, or by creating physical competition for peptides bind to specific receptors and can affect the space that the pathogenic bacteria would normally oc- neuronal ion channels, neuronal receptors or presynaptic cupy. membrane proteins. Since GNA is able to cross the in- This symbiont-based strategy is already being applied testinal epithelium, it has the potential to transmit pep- against several insect-borne human-disease pathogens, tides fused to it into the hemolymph. In a novel applica- including the Chagas’ disease agent. Research with lea- tion of this idea, Down et al. (2006) demonstrated the fhoppers transmitting the xylem-limited bacterium X. insecticidal effects of spider venom (SFI1) on the fastidiosa, which replicates in the foregut of the sharp- planthopper, N. lugens. Although the SFI1/GNA fusion shooter, H. coagulata, is also progressing apace. A product and smaller levels of GNA was found in the symbiont, Alcaligenes xylosoxidans subsp. denitrificans, hemolymph, the mechanism of toxicity is not known. has been identified, cultured, modified and successfully Possibly the fusion protein was cleaved, allowing the reintroduced into leafhoppers via several plants (citrus, SFI1 toxin to act. chrysanthemum, grape, periwinkle and crepe myrtle) and is expected to be competing with the pathogen for space and resources, thus reducing the vectoring capaci- Systemic acquired resistance ties of the host (Bextine et al., 2005). Similarly, another bacterium, Cardinium hertigii, has been identified and Plants can activate defence mechanisms when chal- localized in the fat bodies and salivary glands of the lenged by either an arthropod or pathogen. This re- leafhopper S. titanus. Because this insect is the vector of sponse – termed systemic acquired resistance (SAR) – the phytoplasma that causes FD its presence in the same can also be elicited by a number of chemicals (Sticher et locations as the FD phytoplasma may eventually be in- al., 1997). Colladonus montanus (Van Duzee) is an ef- strumental in symbiotic control efforts (Bigliardi et al., ficient vector of X-disease in fruit trees, and can also 2006; Marzorati et al., 2006). One of the major chal- efficiently transmit the phytoplasma to Arabidopsis lenges in this field is the delivery of the transgenic bac- thaliana Columbia under laboratory conditions. Infected teria to the target vectors without adversely affecting the A. thaliana is stunted and produces fewer or no siliques. environment or other insect populations. Treatment with benzothiadiazole (BTH) protected plants from phytoplasma; ~ 74% of non-treated control

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plants became infected, as compared to only 35% of the DOWN R. E., FITCHES E. C., WILES D. P., CORTI P., BELL H. A., plants protected with 4.8 mM BTH a week prior to leaf- GATEHOUSE G. A., EDWARDS J. P., 2006.- Insecticidal spider hopper feeding (Bressan and Purcell, 2005). The mecha- venom toxin fused to snowdrop lectin is toxic to the peach- nism for this effect is not clear: the plant phloem could potato aphid, Myzus persicae (Hemiptera: Aphididae) and the rice brown planthopper, Nilaparvata lugens (Hemiptera: have been morphologically modified to prevented phy- Delphacidae).- Pest Management Science, 62 (1): 77-85. toplasma from establishing or replicating, but the BTH DU J. P., FOISSAC X., CARSS A., GATEHOUSE A. M. R., GATE- could also have elicited production of a substance inhib- HOUSE J. A., 2000. -Ferritin acts as the most abundant bind- iting vector feeding, hence inhibiting transmission. ing protein for snowdrop lectin in the midgut of rice brown Fewer leafhoppers survived on BTH-treated A. thaliana planthoppers (Nilaparvata lugens).- Insect Biochemistry and than on non-treated plants. Molecular Biology, 30 (4): 297-305. DUTTA I., SAHA P., MAJUMER P., SARKAR A., CHAKRABORTI D., BANERJEE S., DAS S., 2005.- The efficacy of a novel in- Conclusions secticidal protein, Allium sativum leaf lectin (ASAL), a- gainst homopteran insects monitored in transgenic tobacco.-

Plant Biotechnology Journal, 3 (6): 601-611. The number of new confirmed phytoplasma vectors has FITCHES E., WOODHOUSE S. D., EDWARDS J. P., GATEHOUSE J. not kept pace with the number of new phytoplasmas de- A., 2001.- In vitro and in vivo binding of snowdrop (Galan- scribed. This is partially due to the ease of describing thus nivalis agglutinin; GNA) and jackbean (Canavalia ensi- new phytoplasmas in lieu of the current molecular me- formis, Con A) lectins within tomato moth (Lacanobia ol- thods available to researchers. eracea) larvae; mechanisms of insecticidal action.- Journal The most effective means of insect vector control is of Insect Physiology, 47 (7): 777-787. through physical prevention – either by use of screening FOISSAC X., LOC N., CHRISTOU P., GAEHOUSE A. M. R., GATE- or by use of a mineral coating on the plant itself. New HOUSE J. A., 2000.- Resistance to green leafhopper (Nepho- tettix virescens) and brown planthopper (Nilaparvata methods will, by necessity, most likely revolve around lugens) in transgenic rice expressing snowdrop lectin (Gal- genetic modification of the plant to either prevent phy- anthus nivalis agglutinin; GNA).- Journal of Insect Physiol- toplasma replication within the plant or to pre- ogy, 46 (4): 573-583. vent/reduce vectors feeding on the plant. GUTHRIE J. N., WHITE D. T., WALSH K. B., SCOTT P. T. 1998.- Epidemiology of phytoplasma-associated papaya diseases in Queensland, Australia.- Plant Disease, 82 (10): 1107-1111. 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