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Development and validation of a real-time PCR assay for the glassy-winged sharpshooter Homalodisca vitripennis (Hemiptera: Cicadellidae)

Published online by Cambridge University Press:  07 November 2016

D.W. Waite ,
D. Li ,
M. D'Souza  and
D. Gunawardana
D.W. Waite*
Affiliation:
Plant Health and Environment Laboratory, Ministry for Primary Industries, PO Box 2095, Auckland 1140, New Zealand
D. Li
Affiliation:
Plant Health and Environment Laboratory, Ministry for Primary Industries, PO Box 2095, Auckland 1140, New Zealand
M. D'Souza
Affiliation:
Plant Health and Environment Laboratory, Ministry for Primary Industries, PO Box 2095, Auckland 1140, New Zealand Department of Surgery, University of Chicago, Chicago, IL, USA The Marine Biological Laboratory, Woods Hole, MA, USA
D. Gunawardana
Affiliation:
Plant Health and Environment Laboratory, Ministry for Primary Industries, PO Box 2095, Auckland 1140, New Zealand
*
*Author for correspondence Phone: +61 (7) 336 54957 Fax: +61 (7) 336 54699 E-mail: [email protected]
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Abstract

The glassy-winged sharpshooter (Homalodisca vitripennis) is an invasive pest organism, which is found throughout Central America and has recently invaded a few countries in the Pacific Islands. As a carrier of the highly virulent plant pathogenic bacterium Xylella fastidiosa, it is of great economic significance to horticulture and is estimated to cost Californian vineyards over US$100 million per year in control and losses. New Zealand is currently free from this pest, but its recent spread through the Pacific has raised concerns of it establishing in New Zealand, potentially as a result of introduction through human travel. We report here a real-time polymerase chain reaction assay for the rapid identification of H. vitripennis. The assay was extensively validated in silico then optimized and tested against a range of Cicadellidae species, both internationally collected and local to New Zealand. This assay was able to correctly identify H. vitripennis samples, and distinguish between H. vitripennis and close relatives, such as the smoke-tree sharpshooter (Homalodisca liturata) and will be of great benefit to New Zealand biosecurity.

Keywords

Homalodisca vitripennisidentificationqPCRCOIbiosecurity
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 107 , Issue 3 , June 2017 , pp. 332 - 339
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Copyright
Copyright © Cambridge University Press 2016 

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References

Almeida, R. & Purcell, A. (2003) Transmission of Xylella fastidiosa to grapevines by Homalodisca coagulata (Hemiptera: Cicadellidae). Journal of Economic Entomology 96, 264–271.CrossRefGoogle ScholarPubMed
Alston, J., Fuller, K., Kaplan, J. & Tumber, K. (2013) Economic consequences of Pierce's Disease and related policy in the California winegrape industry. Journal of Agricultural and Resource Economics 38, 269–297.Google Scholar
Anderson, P., Brodbeck, B. & Mizell, R. III (1989) Metabolism of amino acids, organics acids and sugars extracted from the xylem fluid of four host plants by adult Homalodisca coagulata . Entomologia Experimentalis et Applicata 50, 149–159.CrossRefGoogle Scholar
Bethke, J., Blua, M. & Redak, R. (2001) Effect of selected insecticides on Homalodisca coagulata (Homoptera: Cicadellidae) and transmission of Oleander Leaf Scorch in a greenhouse study. Journal of Economic Entomology 94, 1031–1036.Google Scholar
Blua, M. & Morgan, D. (2003) Dispersion of Homalodisca coagulata (Hemiptera: Cicadellidae), a vector of Xylella fastidiosa, into vineyards in Southern California. Journal of Economic Entomology 96, 1369–1374.Google Scholar
Blua, M., Phillips, P. & Redak, R. (1999) A new sharpshooter threatens both crops and ornamentals. California Agriculture 53, 22–25.Google Scholar
Boykin, L., Shatters, R. Jr., Rosell, R., McKenzie, C., Bagnall, R., De Barro, P. & Frohlich, D. (2007) Global relationships of Bemisia tabaci (Hemiptera: Aleyrodidae) revealed using Bayesian analysis of mitochondrial COI DNA sequences. Molecular Phylogenetics and Evolution 44, 1306–1319.Google Scholar
Brodbeck, B., Mizell, R. III & Andersen, P. (1993) Physiological and behavioral adaptations of three species of leafhoppers in response to the dilute nutrient content of xylem fluid. Journal of Insect Physiology 39, 73–81.Google Scholar
Bustin, S.A., Benes, V., Garson, J.A., Hellemans, J., Huggett, J., Kubista, M., Mueller, R., Nolan, T., Pfaffl, M.W., Shipley, G.L., Vandesompele, J. & Wittwer, C.T. (2009) The MIQE Guidelines: minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry 55, 611–622.CrossRefGoogle ScholarPubMed
Cranston, P. (2010) Insect biodiversity and conservation in Australia. Annual Review of Entomology 55, 55–75.Google Scholar
Dandekar, A., Ibáñez, A., Gouran, H., Phu, M., Rao, B. & Chakraborty, S. (2012) Building a next generation chimeric antimicrobial protein to provide rootstock-mediated resistance to Pierce's disease in grapevines. pp. 89–192 in Esser, T. and Randhawa, R. (Eds) Pierce's Disease Research Progress Reports. Sacramento, CA, California Department of Food and Agriculture.Google Scholar
de León, J., Fournier, V., Hagler, J. & Daane, K. (2006) Development of molecular diagnostic markers for sharpshooters Homalodisca coagulata and Homalodisca liturata for use in predator gut content examinations. Entomologia Experimentalis et Applicata 119, 109–119.CrossRefGoogle Scholar
Dhami, M. & Kumarasinghe, L. (2014) A HRM real-time PCR assay for rapid and specific identification of the emerging pest spotted-wing drosophila (Drosophila suzukii). PLoS ONE 9, e98934.Google Scholar
Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.Google Scholar
Foottit, R., Maw, E. & Hebert, P. (2014) DNA barcodes for Nearctic Auchenorrhyncha (Insecta: Hemiptera). PLoS ONE 9, e101385.Google Scholar
Fournier, V., Hagler, J., Daane, K., de León, J., Groves, R., Costa, H. & Henneberry, T. (2006) Development and application of a glassy-winged and smoke-tree sharpshooter egg-specific predator gut content ELISA. Biological Control 37, 108–118.Google Scholar
Fournier, V., Hagler, J., Daane, K., de León, J. & Groves, R. (2008) Identifying the predator complex of Homalodisca vitripennis (Hemiptera: Cicadellidae): a comparative study of the efficacy of an ELISA and PCR gut content assay. Oecologia 157, 629–640.Google Scholar
Grandgirard, J., Hoddle, M., Roderick, G., Petit, J., Percy, D., Putoa, R., Garnier, C. & Davies, N. (2006) Invasion of French Polynesia by the glassy-winged sharpshooter, Homalodisca coagulata (Hemiptera: Cicadellidae): a new threat to the South Pacific. Pacific Science 60, 429–438.CrossRefGoogle Scholar
Grandgirard, J., Hoddle, M., Petit, J., Roderick, G. & Davies, N. (2008) Engineering an invasion: classical biological control of the glassy-winged sharpshooter, Homalodisca vitripennis, by the egg parasitoid Gonatocerus ashmeadi in Tahiti and Moorea, French Polynesia. Biological Invasions 10, 135–148.Google Scholar
Guan, W., Shao, J., Singh, R., Davis, R., Zhao, T. & Huang, Q. (2013) A TaqMan-based real time PCR assay for specific detection and quantification of Xylella fastidiosa strains causing bacterial leaf scorch in oleander. Journal of Microbiological Methods 92, 108–112.CrossRefGoogle ScholarPubMed
Guiterrez, A., Ponti, L., Hoddle, M., Almeida, R. & Irvin, N. (2011) Geographic distribution and relative abundance of the invasive glassy-winged sharpshooter: effects of temperature and egg parasitoids. Environmental Entomology 40, 755–769.Google Scholar
Gunawardana, D., Ashcroft, T., Braithwaite, M. & Poeschko, M. (2008) Bio-control for glassy-winged sharpshooter in Cook Islands. Biosecurity Magazine 85, 12–13.Google Scholar
Hagler, J., Blackmer, F., Krugner, R., Groves, R., Morse, J. & Johnson, M. (2013) Gut content examination of the citrus predator assemblage for the presence of Homalodisca vitripennis remains. BioControl 58, 341–349.Google Scholar
Hoddle, M. (2004) The potential adventive geographic range of glassy-winged sharpshooter, Homalodisca coagulata and the grape pathogen Xylella fastidiosa: implications for California and other grape growing regions of the world. Crop Protection 23, 691–699.Google Scholar
Hopkins, D. (2005) Biological control of Pierce's Disease in the vineyard with strains of Xylella fastidiosa benign to grapevine. Plant Disease 89, 1348–1352.CrossRefGoogle ScholarPubMed
Hopkins, D. & Purcell, A. (2002) Xylella fastidiosa: cause of Pierce's disease in grapevine and other emergent diseases. Plant Disease 86, 1056–1066.Google Scholar
Huang, K., Lee, S., Yeh, Y., Shen, G., Mei, E. & Chang, C. (2010) Taqman real-time quantitative PCR for identification of western flower thrip (Frankliniella occidentalis) for plant quarantine. Biology Letters 6, 555–557.Google Scholar
Johnson, M., Daane, K., Groves, R. & Backus, E. (2006) Spatial population dynamics and overwintering biology of the glassy-winged sharpshooter in California's San Joaquin Valley. pp. 12–15 in Pierce's Disease Research Symposium Proceedings. Sacramento CA, California Department of Food and Agriculture.Google Scholar
Jones, C., Gorman, K., Denholm, I. & Williamson, M. (2008) High-throughput allelic discrimination of B and Q biotypes of the whitefly, Bemisia tabaci, using TaqMan allele-selective PCR. Pest Management Science 64, 12–15.Google Scholar
Larivière, M.-C. (Ed.) (2005 and updates) Checklist of New Zealand Hemiptera (excluding Sternorrhyncha). Available online at http://hemiptera.landcareresearch.co.nz/ (accessed 2 April 2016).Google Scholar
Li, M., Tian, Y., Zhao, Y. & Bu, W. (2012) Higher level phylogeny and the first divergence time estimation of Heteroptera (Insecta: Hemiptera) based on multiple genes. PLoS ONE 7, e32152.Google Scholar
Malausa, T., Fenis, A., Warot, S., Garmain, J., Ris, N., Prado, E., Botton, M., Vanlerberghe-Masutti, F., Sforza, R., Cruaud, C., Couloux, A. & Kreiter, P. (2011) DNA markers to disentangle complexes of cryptic taxa in mealybugs (Hemiptera: Pseudococcidae). Journal of Applied Entomology 135, 142–155.Google Scholar
Minsavage, G., Thompson, C., Hopkins, D., Leite, R. & Stall, R. (1994) Development of a polymerase chain reaction protocol for detection of Xylella fastidiosa in plant tissue. Phytopathy 84, 456–461.Google Scholar
Northfield, T., Mizel, R. III, Paini, D., Andersen, P., Brodbeck, B., Riddle, T. & Hunter, W. (2009) Dispersal, patch leaving, and distribution of Homalodisca vitripennis (Hemiptera: Cicadellidae). Environmental Entomology 38, 183–191.Google Scholar
Park, D.-S., Foottit, R., Hebert, P. (2011) Barcoding bugs: DNA-based identification of the true bugs (Insecta: Hemiptera: Heteroptera). PLoS ONE 6, e18749.CrossRefGoogle ScholarPubMed
Pérez-Donoso, A., Sun, Q., Roper, M., Greve, L., Kirkpatrick, B. & Labavitch, J. (2010) Cell wall-degrading enzymes enlarge the pore size of intervessel pit membranes in healthy and Xylella fastidiosa-infected grapevines. Plant Physiology 152, 1748–1759.Google Scholar
Petit, J., Hoddle, M., Grandgirard, J., Roderick, G. & Davies, N. (2008) Invasion dynamics of the glassy-winged sharpshooter Homalodisca vitripennis (Germar) (Hemiptera: Cicadellidae) in French Polynesia. Biological Invasions 10, 955–967.Google Scholar
Purcell, A. & Feil, H. (2001) Glassy-winged sharpshooter. Pesticide Outlook 12, 199–203.Google Scholar
Purcell, A., Saunders, S., Hendson, M., Grebus, M. & Henry, M. (1999) Causal role of Xylella fastidiosa in Oleander Leaf Scorch disease. Phytopathology 89, 53–58.Google Scholar
Rakauskas, R., Turčinavičeine, J. & Bašilova, J. (2011) How many species are there in the subgenus Bursaphis (Hemiptera: Sternorrhyncha: Aphididae)? CO-I evidence. European Journal of Entomology 108, 469–479.Google Scholar
Rathé, A., Pilkington, L., Gurr, G., Hoddle, M., Daugherty, M., Constable, F., Luck, J., Powell, K., Fletcher, M. & Edwards, O. (2012) Incursion preparedness: anticipating the arrival of an economically important plant pathogen Xylella fastidiosa Wells (Proteobacteria: Xanthomonadaceae) and the insect vector Homalodisca vitripennis (Germar) (Hemiptera: Cicadellidae) in Australia. Australian Journal of Entomology 51, 209–220.Google Scholar
Ratnasingham, S. & Hebert, P. (2007) BOLD: the barcode of life data system (www.barcodinglife.org). Molecular Ecology Notes 7, 355–364.Google Scholar
R Core Team (2013) R: a language and environment for statistical computing.Google Scholar
Roper, M., Creve, L., Warren, J., Labavitch, J. & Kirkpatrick, B. (2007) Xylella fastidiosa requires polygalacturonase for colonization and pathogenicity in Vitis vinifera grapevines. Molecular Plant-Microbe Interactions 20, 411–419.Google Scholar
Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H. & Flook, P. (1994) Evolution, weighting and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America 87, 651–701.Google Scholar
Smith, P. (2005) Mitochondrial DNA variation among populations of the glassy-winged sharpshooter, Homalodisca coagulata . Journal of Insect Science 5, 41–49.Google Scholar
Song, N., Liang, A.-P. & Bu, C.-P. (2012) A molecular phylogeny of Hemiptera inferred from mitochondrial genome sequences. PLoS ONE 7, e48778.Google Scholar
Sorensen, J. & Gill, R. (1996) A range extension of Homalodisca coagulata (Say) (Hemiptera: Clypeorrhyncha: Cicadellidae) to southern California. Pan-Pacific Entomologist 72, 160–161.Google Scholar
Stamatakis, A. (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313.Google Scholar
Sun, Q., Greve, L. & Labavitch, J. (2011) Polysaccharide compositions of intervessel pit membranes contribute to Pierce's Disease resistance of grapevines. Plant Physiology 155, 1676–1687.Google Scholar
Takiya, D., McKamey, S. & Cavichioli, R. (2006) Validity of Homalodisca and of H. vitripennis as the name for glassy-winged sharpshooter (Hemiptera: Cicadellidae: Cicadellinae). Annals of the Entomological Society of America 99, 648–655.Google Scholar
Triapitsyn, S. & Phillips, P. (2000) First record of Gonatocerus triguttatus (Hymenoptera: Mymaridae) from eggs of Homalodisca coagulata (Homoptera: Cicadellidae) with notes on the distribution of the host. Florida Entomologist 83, 200–203.CrossRefGoogle Scholar
Triapitsyn, S., Mizell, R. III, Bossart, J. & Carlton, C. (1998) Egg parasitoids of Homalodisca coagulata (Homoptera: Cicadellidae). Florida Entomologist 81, 241–243.CrossRefGoogle Scholar
Tumber, K., Alston, J. & Fuller, K. (2014) Pierce's disease costs California $104 million per year. California Agriculture 68, 20–29.CrossRefGoogle Scholar
Turner, W. & Pollard, H. (1959) Life histories and behavior of five insect vectors of phony peach disease. US Department of Agriculture Technical Bulletin 1188, 1–27.Google Scholar
ven de Vossenberg, B. & van der Straten, M. (2014) Development and validation of real-time PCR tests for the identification of four Spodoptera species: Spodoptera eridania, Spodoptera frugiperda, Spodoptera littoralis, and Spodoptera litura (Lepidoptera: Noctuidae). Journal of Economic Entomology 107, 1643–1654.CrossRefGoogle Scholar
Wistrom, C., Sisterson, M., Pryor, M., Hashim-Buckey, J. & Daane, K. (2010) Distribution of glassy-winged sharpshooter and three cornered alfalfa hopper on plant hosts in the San Joaquin Valley, California. Journal of Economic Entomology 103, 1051–1059.Google Scholar
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