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Integrating multiple criteria for the characterization of Psammotettix populations in European cereal fields

Published online by Cambridge University Press:  27 July 2017

I. Abt
Affiliation:
INRA-Cirad-SupAgro Montpellier, UMR 385 BGPI, Cirad TA A-54K, Campus international de Baillarguet, F-34398 Montpellier, France Bayer S.A.S./Bayer CropScience, 16 rue Jean Marie Leclair – CS 90106, 69266 Lyon Cedex 09, France
M. Derlink
Affiliation:
Department of Organisms and Ecosystems Research, National Institute of Biology (NIB), Večna Pot 111, 1000 Ljubljana, Slovenia
R. Mabon
Affiliation:
INRA-Cirad-SupAgro Montpellier, UMR 385 BGPI, Cirad TA A-54K, Campus international de Baillarguet, F-34398 Montpellier, France Bayer S.A.S./Bayer CropScience, 16 rue Jean Marie Leclair – CS 90106, 69266 Lyon Cedex 09, France
M. Virant-Doberlet
Affiliation:
Department of Organisms and Ecosystems Research, National Institute of Biology (NIB), Večna Pot 111, 1000 Ljubljana, Slovenia
E. Jacquot*
Affiliation:
INRA-Cirad-SupAgro Montpellier, UMR 385 BGPI, Cirad TA A-54K, Campus international de Baillarguet, F-34398 Montpellier, France
*
* Author for correspondence Phone: 00(33) 4 99 62 48 36 E-mail: emmanuel.jacquot@inra.fr

Abstract

The wheat dwarf disease is among the most damaging diseases in cereals. Its aetiological agent is the Wheat dwarf virus (WDV), which is exclusively transmitted from plant to plant by leafhoppers from the genus Psammotettix (Hemiptera, Cicadellidae). The parameters linked to the WDV/Psammotettix pathosystem are still poorly understood. We studied Psammotettix individuals collected in wheat and barley fields in France and, as a comparison, from grassland at agroecological interface in West Slovenia. Species identity of males and females has been determined using multiple criteria. In the first step, the characterization of the collected individuals included recordings of vibrational signals used in mating behaviour and morphometric analyses. In addition, a 442 nt sequence of the mitochondrial cytochrome oxydase I (COI) gene was obtained for some individuals and compared to COI sequences of the Psammotettix leafhoppers available in public databases. In the cereal fields in France, P sammotettix alienus was the most numerous species; however, it sometimes occurred together with Psammotettix confinis, while in the grasslands in Slovenia, the third syntopic species in Psammotettix community was Psammotettix helvolus. The temporal parameters of the P. alienus male calling song that were measured in this study were very similar to those measured in a previous study. The local biotic and/or abiotic parameters most likely influence the life history of Psammotettix leafhoppers, and the proportion of viruliferous individuals collected in cereal fields was 14.9%, while leafhoppers collected in Slovenia were virus-free. Taken together, results show that more detailed information on population structure of Psammotettix leafhoppers is crucial for providing an insight into the epidemiology of wheat dwarf disease.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2017 

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Footnotes

These two authors contribute equally to the work.

References

Abt, I. & Jacquot, E. (2015) Wheat dwarf. pp. 2741 in Tennant, P. & Fermin, R. (Eds) Virus Diseases of Tropical and Subtropical Crops. CAB International, Plant protection series doi: 10.1079/9781780644264.0027.CrossRefGoogle Scholar
Alexander, H.M., Mauck, K.E., Whitfield, A.E., Garrett, K.A. & Malmstrom, C.M. (2014) Plant–virus interactions and the agro-ecological interface. European Journal of Plant Pathology 138, 529547.CrossRefGoogle Scholar
Biedermann, R. & Niedringhaus, R. (2009) The Plant- and Leafhoppers of Germany: Identification Key to all Species. Scheeßel, Germany, Wissenschaftlich Akademischer Buchvertrieb–Fründ, 409 pp.Google Scholar
Bisztray, G., Gaborjanyi, R. & Vacke, J. (1989) Isolation and characterization of wheat dwarf virus found for the first time in Hungary. Zeitschrift Fur Pflanzenkrankheiten Und Pflanzenschutz-Journal of Plant Diseases and Protection 96, 449454.Google Scholar
Bluemel, J.K., King, A.R., Virant-Doberet, M. & Symondson, W.O.C. (2011) Primers for identification of type and other archived spevimens of Aphrodes leafhoppers (Hemiptera, Cicadellidae). Molecular Ecology Resources 11, 770774.CrossRefGoogle ScholarPubMed
Bluemel, J.K., Derlink, M., Pavlovčič, P., Russo, I.M., King, R.A., Corbett, E., Sherrard-Smith, E., Wilson, M.R., Stewart, A.J.A., Symondson, W.O.C. & Virant-Doberlet, M. (2014) Integrating vibrational signals, mitochondrial DNA and morphology for species determination in the genus Aphrodes (Hemiptera: Cicadellidae). Systematic Entomology 39, 304324.CrossRefGoogle Scholar
Borchard, F. & Fartmann, T. (2014) Effects of montane heathland restoration on leafhopper assemblages (Insecta: Auchenorrhyncha). Restoration Ecology 22, 749757.CrossRefGoogle Scholar
Bortolus, A. (2008) Error cascades in the biological sciences: the unwanted consequences of bad taxonomy in ecology. Ambio 37, 114118.CrossRefGoogle ScholarPubMed
Brault, V., Uzest, M., Monsion, B., Jacquot, E. & Blanc, S. (2010) Aphids as transport devices for plant viruses. Comptes Rendus Biologies 333, 524538.CrossRefGoogle ScholarPubMed
Broughton, W.B. (1963) Method in bioacoustic terminology. pp. 324 in Busnel, R.G. (Ed.) Acoustic Behaviour in Animals. Amsterdam, The Netherlands, Elsevier.Google Scholar
Clark, M.F. & Adams, A.N. (1977) Characteristics of the microplate method of enzyme-linked immunosorbent assay for the detection of plant viruses. Journal of General Virology 34, 475483.CrossRefGoogle ScholarPubMed
Conti, M. (1994) Leafhopper borne plant viruses in Italy. Memoire della Società Entomologica Italiana 72, 541547.Google Scholar
Della Giustina, W. (1989) Homoptères Cicadellidae, volume 3 compléments. Faune de France. Fédération Française des sociétés de sciences naturelles, INRA éditions, pp. 1350.Google Scholar
Delpuech, J.M., Dupont, C. & Allemand, R. (2010) Decrease in fecundity induced by interspecific mating between two trichogramma parasitoid species. Journal of Economic Entomology 103(2), 308313.CrossRefGoogle ScholarPubMed
Derlink, M., Abt, I., Mabon, M., Julian, C., Virant-Doberlet, M. & Jacquot, E. (2016) Mating behaviour of Psammotettix alienus Dahlbom (Hemiptera: Cicadellidae). Insect Science. doi: 10.1111/1744-7917.12379.Google ScholarPubMed
Ekzayez, A.M., Kumari, S.G. & Ismail, I. (2011) First report of wheat dwarf virus and its vector (Psammotettix provincialis) affecting wheat and barley crops in Syria. Plant Disease 95, 7676.CrossRefGoogle ScholarPubMed
Folmer, O., Black, M., Hoeh, W., Lutz, R.A. & Vrijenhoek, R.C. (1994) DNA primers for amplification of mitochondrial cytochrome C oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294299.Google ScholarPubMed
Foottit, R.G., Maw, E. & Hebert, P.D.N. (2014) DNA barcodes for Nearctic Auchenorrhyncha (Insecta: Hemiptera). PLoS ONE 9, e101385. doi: 10.1271/journal.pone.0101385.CrossRefGoogle ScholarPubMed
Gibson, C.M., Kako, R.H., Blevins, K.K. & Travers, P.D. (2012) Integrative taxonomy for continental-scale terrestrial insect observations. PLoS ONE 7, e37528. doi: 10.1271/journal.pone.0037528.CrossRefGoogle ScholarPubMed
Gillham, M.C. (1992) Variation in acoustic signals within and among leafhoppers species of the genus Alebra (Homoptera, Cicadellidae). Biological Journal of the Linnean Society 45, 115.CrossRefGoogle Scholar
Guglielmino, A. & Virla, E.G. (1997) Postembryonic development and biology of Psammotettix alienus (Dahlbom) (Homoptera, Cicadellidae) under laboratory conditions. Bollettino di Zoologia, Agraria e di Bachicoltura 29, 6580.Google Scholar
Guindon, S., Dufayard, J.F., Lefort, V., Anisimova, M., Hordijk, W. & Gascuel, O. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307321.CrossRefGoogle ScholarPubMed
Gwiazdowski, R.A., Foottit, R.G., Mawn, H.E.L. & Hebert, P.D.N. (2015) The Hemiptera (Insecta) of Canada: constructing a reference library of DNA barcodes. PLoS ONE 10(4), e0125635. doi: 10.1371/journal.pone.0125635.CrossRefGoogle ScholarPubMed
Heady, S.E., Nault, L.R., Shambaugh, G.F. & Fairchild, L. (1986) Acoustic and mating behavior of Dalbulus leafhoppers (Homoptera: Cicadellidae). Annals of the Entomological Society of America 79, 727736.CrossRefGoogle Scholar
Henry, C.S., Brooks, S.J., Duelli, P., Johnson, J.B., Wells, M.M. & Mochizuki, A. (2013) Obligatory duetting behaviour in the Chrysoperla carnea-group of cryptic species (Neuropetra: Chysopidae): its role in shaping evolutionary history. Biological Reviews 88, 787808.CrossRefGoogle ScholarPubMed
Hogenhaut, S.A., Ammar, E.-D., Whitfield, A.E. & Redinbaugh, M.G. (2008) Insect vector interactions with persistently transmitted viruses. Annual Reviews of Phytopathology 46, 327359.CrossRefGoogle Scholar
Huelsenbeck, J.P. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17(8), 754755.CrossRefGoogle ScholarPubMed
ICTV Report (2012) in King, A.M.Q., Adams, M.J., Carstens, E.B. & Lefkowitz, E.J. (Eds) Virus Taxonomy: Classification and Nomenclature of Viruses: Ninth Report of the International Committee on Taxonomy of Viruses. San Diego, USA, Elsevier Academic Press. https://talk.ictvonline.org/ictv-reports/ictv_9th_report/.Google Scholar
Kamitani, S. (2011) DNA barcodes of Japanese leafhoppers. ESAKIA 50, 8188.CrossRefGoogle Scholar
Kvarnheden, A., Lett, J.M. & Peterschmitt, M. (2016) Mastreviruses: tropical and temperate leafhopper-Borne geminiviruses. pp. 231241 in Brown, J.K. (Ed.) Vector-Mediated Transmission of Plant Pathogens. APS Press doi: 10.1094/9780890545355.016.CrossRefGoogle Scholar
Le Roux, J.J. & Rubinoff, D. (2009) Molecular data reveals California as the potential source of an invasive leafhopper species, Macrosteles sp. nr. severini, transmitting the aster yellows phytoplasma in Hawaii. Annals of Applied Biology 154, 419427.CrossRefGoogle Scholar
Li, Y., Chen, W., Wang, Q., Wang, N. & Wu, Y.F. (2014) Assessment of reference genes for quantitative real-time PCR gene expression normalization in periwinkle during wheat blue dwarf phytoplasma infection. Australasian Plant Pathology 43, 477485.CrossRefGoogle Scholar
Lindblad, M. & Areno, P. (2002) Temporal and spatial population dynamics of Psammotettix alienus, a vector of wheat dwarf virus. International Journal of Pest Management 48, 233238.CrossRefGoogle Scholar
Manurung, B., Witsack, W., Mehner, S., Gruntzig, M. & Fuchs, E. (2004) The epidemiology of wheat dwarf virus in relation to occurrence of the leafhopper Psammotettix alienus in Middle-Germany. Virus Research 100(1), 109113.CrossRefGoogle ScholarPubMed
Manurung, B., Witsack, W., Mehner, S., Gruntzig, M. & Fuchs, E. (2005) Studies on biology and population dynamics of the leafhopper Psammotettix alienus Dahlb. (Homoptera: Auchenorrhyncha) as vector of wheat dwarf virus (WDV) in Saxony-Anhalt, Germany. Zeitschrift fur Pflanzenkrankheiten und Pflanzenschutz 112(5), 497507.Google Scholar
Okoth, V.A.O., Dabrowski, Z.T. & Van Emden, H.F. (1987) Comparative biology of some Cicadulina species and populations from various climatic zones in Nigeria (Hemiptera: Cicadellidae). Bulletin of Entomological Research 77, 18.CrossRefGoogle Scholar
Patterson, D.J., Copper, J., Kork, P.M., Pyle, R.L. & Remsen, D.P. (2010) Names are key to the big new biology. Trends in Ecology & Evolution 25, 686691.CrossRefGoogle Scholar
Percy, D.M., Boyd, E.A. & Hoddle, M.S. (2008) Observations on acoustic signalling in three sharpshooters: Homalodisca vitripenis, Homalodisca liturata and Graphocephala atropunctata (Hemiptera: Cicadellidae). Annals of the Entomological Society of America 101, 253259.CrossRefGoogle Scholar
Posadas, G. & Henry, M. (2002) Resistance to BYDV-PAV and CYDV-RPV in a bread wheat x agrotricum cross. 139 pp in Henry, M. & McNab, A. (Eds) Barley Yellow Dwarf Disease: Recent Advances and Future Strategies. Mexico, CIMMYT.Google Scholar
R Development Core Team (2010) R: A Language and Environment for Statistical Computiing. Vienna, Austria, R Foundation for Statistical Computing.Google Scholar
Raatikainen, M. & Vasarainen, A. (1973) Early- and high-summer flight periods of leafhoppers. Annales Agriculturae Fenniae 12, 7794.Google Scholar
Rasband, W. (2006) IMAGEJ. Bethesda, Maryland, USA, National Institute of Health.Google Scholar
Sadeghi, S.E., Dedryver, C.A., Riault, G. & Tanguy, S. (2000) Variation in virus content among individual leaves and roots of barley and wheat infected with a BYDV-PAV isolate. Journal of Agricultural Science Techniques 2, 151160.Google Scholar
Schiemenz, H. (1969) Die Zikadenfauna mitteleurop.aischer Trockenrasen (Homoptera, Auchenorrhyncha). Entomologische Abhandlungen 36, 201280.Google Scholar
Schlick-Steiner, B.C., Steiner, F.M., Seifert, B., Stauffer, C., Christian, E. & Crozier, R.H. (2010) Integrative taxonomy: a multisource approach to exploring biodiversity. Annual Review of Entomology 55, 421438.CrossRefGoogle ScholarPubMed
Schubert, J., Habekuss, A., Wu, B.L., Thieme, T. & Wang, X.F. (2014) Analysis of complete genomes of isolates of the wheat dwarf virus from new geographical locations and descriptions of their defective forms. Virus Genes 48, 133139.CrossRefGoogle ScholarPubMed
Tamura, K. & Nei, M. (1993) Estimation of the number of nucleotide substitutions in the control of mitochondrial-DNA in humans and chimpanzees. Molecular Biology and Evolution 10, 512526.Google ScholarPubMed
Tishechkin, D. Yu. (1999) The variability of acoustic signals and some morphological characters in Psammotettix striatus (Homoptera, Cicadellidae) from Russia and adjacent countries. Zoologichesky Zhurnal 78(11), 12981305.Google Scholar
Tishechkin, D. Yu. (2000) Vibrational communication in Aphrodinae leafhoppers (Deltocephalinae auct., Homoptera: Cicadellidae) and related groups with notes on classification of higher taxa. Russian Entomological Journal 9(1), 166.Google Scholar
Tishechkin, D. Yu. (2014) The use of bioacoustic characters for distinguishing between cryptic species in insects: potentials, restrictions, and prospects. Entomological Review 94(3), 289309.CrossRefGoogle Scholar
Vacke, J. (1961) Wheat dwarf virus disease. Biologia Plantarum 3, 228233.CrossRefGoogle Scholar
Vacke, J. (1972) Host plants range and symptoms of wheat dwarf virus. Vyzkumnych Ustavu Rostlinné Vyroby Praha-Ruzyne 17, 151162.Google Scholar
Van Rensburg, G.D.J. (1982) Laboratory observations on the biology of Cicadulina mbila (Naudé) (Homoptera: Cicadellidae), a vector of maize streak disease. 1. The effect of temperature. Phytophylactica 14, 99107.Google Scholar
Vilbaste, J. (1982) Preliminary key for the identification of the nymphs of North European Homoptera, Cicadinea. II. Cicadelloidea. Annales Zoologici Fennici 19, 120.Google Scholar
Viršček Marn, M. & Mavrič Pleško, I. (2017) First report of the occurrence of wheat dwarf virus infecting wheat in Slovenia. Plant Disease in press. doi: 10.1094/PDIS-11-16-1642-PDN.CrossRefGoogle Scholar
Weintraub, P.G. & Beanland, L.A. (2008) Insect vectors of phytoplasmas. Annual Review of Entomology 51, 91111.CrossRefGoogle Scholar
Wilson, M., Stewart, A., Bidermann, R., Nickel, H. & Niedringhaus, R. (2015) The Planthoppers and Leafhoppers of Britain and Ireland. Scheeßel, Germany, Wissenschaftlich Akademischer Buchvertrieb–Fründ, 138 pp.Google Scholar
Yeates, D.K., Seago, A., Nelson, L., Cameron, S.L., Joseph, L. & Trueman, J.W.H. (2011) Integrative taxonomy or iterative taxonomy? Systematic Entomology 34, 209217.CrossRefGoogle Scholar
Zhang, F., Zhang, C., Dai, W. & Zhang, Y. (2012) Morphology and histology of the digestive system of the vector leafhopper Psammotettix striatus (L.) (Hemiptera: Cicadellidae). Micron 43, 725738.CrossRefGoogle ScholarPubMed
Zhang, X., Zhou, G.H. & Wang, X.F. (2010) Detection of wheat dwarf virus (WDV) in wheat and vector leafhopper (Psammotettix alienus Dahlb.) by real-time PCR. Journal of Virological Methods 169(2), 416419.CrossRefGoogle ScholarPubMed
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