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Biological and molecular characterization of Hessian fly (Diptera: Cecidomyiidae) from Israel

Published online by Cambridge University Press:  08 May 2012

A.J. Johnson
Affiliation:
USDA-ARS†, Crop Production and Pest Control Unit, 170South University Street, West Lafayette, IN 47907, USA Purdue University, Department of Entomology, 901 West State Street, West Lafayette, IN 47907, USA
P.G. Weintraub
Affiliation:
Agricultural Research Organization, Gilat Research Center, D.N. Negev, 85280, Israel
R. Katoch
Affiliation:
CSKHPKV, Palampur, HP, 176062, India
B.J. Schemerhorn
Affiliation:
USDA-ARS†, Crop Production and Pest Control Unit, 170South University Street, West Lafayette, IN 47907, USA Purdue University, Department of Entomology, 901 West State Street, West Lafayette, IN 47907, USA
R.H. Shukle*
Affiliation:
USDA-ARS†, Crop Production and Pest Control Unit, 170South University Street, West Lafayette, IN 47907, USA Purdue University, Department of Entomology, 901 West State Street, West Lafayette, IN 47907, USA
*
*Author for correspondence Fax:+1 765 494 5105 E-mail: shukle@purdue.edu; rich.shukle@ars.usda.gov

Abstract

Samples of a dipteran pest of wheat were tested to confirm identity, describe local populations and suggest the use of deploying resistance (R) genes in wheat cultivars for control of Mayetiola destructor, Hessian fly (HF). Morphological evaluation of adults and a free-choice oviposition preference test documenting that females overwhelmingly preferred to oviposit on wheat instead of barley supported they were HF. Using the cytochrome c oxidase subunit I (coxI), the Barcoding Region, nine haplotypes were revealed. Two were found only in the Israeli collections and averaged 3% sequence divergence compared to the other seven haplotypes found in the United States, Israel and Syria. In evaluations of virulence, the Israeli HF in culture was virulent to 11 of the 19 (R) genes tested, and complementation analysis documented that, for four of the R genes tested, the Israeli HF shared loci for virulence with HF from the United States. Levels of HF infestation at seven Israeli fields were at least at the 5–8% level, which historically has indicated a significant yield loss. Microsatellite genotyping of the five HF collections from Israel revealed mixed populations in Israel that are distinctly separate from the single population in Syria.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2012

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References

Aaronsohn, A. (1910) Agricultural and botanical exploration of Palestine. US Department of Agriculture Bureau of Plant Industry, Bulletin No. 180.CrossRefGoogle Scholar
Agrawal, A.A. (2001) Phenotypic plasticity in the interactions and evolution of species. Science 294, 321326.Google Scholar
Ahern, R., Hawthorne, D.J. & Raupp, M.J. (2009) Phylogeography of a specialist insect, Adelges cooleyi: historical and contemporary processes shape the distribution of population genetic variation. Molecular Ecology 18, 343356.CrossRefGoogle ScholarPubMed
Atzmon, S.Y. & Schwarzbach, E. (2004) Wheat production and breeding in Israel 1948–2002. Czech Journal of Genetics and Plant Breeding 40, 1724.Google Scholar
Avidov, Z. & Harpaz, I. (1969) Diptera: Mayetiola destructor. pp. 423425 in Plant Pests of Israel. Jerusalem, Israel, Israel Universities Press.Google Scholar
Black, W.C., Hatchett, J.H. & Kirchma, L.J. (1990) Allozyme variation among population of the Hessian fly (Mayetiola destructor) in the United States. Journal of Heredity 81, 331337.Google Scholar
Blum, A., Golan, G., Mayer, J., Sinmena, B., Shpiler, L. & Burra, J. (1989) The drought response of landraces of wheat from the northern Negev Desert in Israel. Euphytica 43, 8796.Google Scholar
Buntin, G.D. (1999) Hessian fly (Diptera: Cecidomyiidae) injury and loss of winter wheat grain yield and quality. Journal of Economic Entomology 92, 11901197.Google Scholar
Buntin, G.D. & Chapin, J.W. (1990) Biology of Hessian fly (Diptera: Cecidomyiidae) in the southeastern United States: Geographic variation and temperature-dependent phonology. Journal of Economic Entomology 83, 10151024.CrossRefGoogle Scholar
Byers, R.A. & Gallun, R.L. (1972) Ability of Hessian fly to stunt winter wheat. Journal of Economic Entomology 65, 955958.Google Scholar
Cambron, S.E., Buntin, G.D., Weisz, R., Holland, J.D., Flanders, K.L., Schemerhorn, B.J. & Shukle, R.H. (2010) Virulence in Hessian fly (Diptera: Cecidomyiidae) field collections from the southeastern United States to 21 resistance genes in wheat. Journal of Economic Entomology 103, 22292235.Google Scholar
Chen, M.S., Echegaray, E., Whitworth, R.J., Wang, H., Sloderbeck, P.E., Knutson, A., Giles, K.L. & Royer, T.A. (2009) Virulence analysis of Hessian fly population from Texas, Oklahoma, and Kansas. Journal of Economic Entolomolgy 102, 774780.Google Scholar
Chenna, R., Sugawana, H., Koike, T., Lopez, R., Gibson, T.J., Higgins, D.G. & Thompson, J.D. (2003) Multiple sequence alignment with the clustal series of programs. Nucleic Acids Research 31, 34973500.Google Scholar
Clement, M., Posada, D. & Crandall, K. (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology 9(10), 16571660.Google Scholar
Cook, O.F. (1913) Wild wheat in Palestine. US Department of Agriculture Bureau of Plant Industry, Bulletin No. 274.Google Scholar
Cornuet, J.M. & Luikart, G. (1997) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144, 20012014.Google Scholar
Dubcovsky, J. & Dvorak, J. (2007) Genome plasticity a key factor in the success of polyploidy wheat under domestication. Science 316, 18621866.Google Scholar
Duvdevany, S. (1939) Grain gnat: a serious pest of wheat and barley. Hassadeh 19, 609612.Google Scholar
El Bouhssinni, M., Chen, M., Lhaloui, S., Zharmukhamedova, G. & Rihawai, F. (2009) Virulence of Hessian fly (Diptera: Cecidomyiidae) in the Fertile Crescent. Journal of Applied Entomology 133, 381385.CrossRefGoogle Scholar
Evanno, G., Regnaut, S. & Goudet, J. (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14, 26112620.CrossRefGoogle ScholarPubMed
Excoffier, L., Laval, G. & Scheider, S. (2005) Arlequin version 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics 1, 4750.Google Scholar
Falush, D., Stephens, M. & Pritchard, J.K. (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164, 15671587.Google Scholar
Falush, D., Stephens, M. & Pritchard, J.K. (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Molecular Ecology Notes 7, 574578.Google Scholar
Felsenstein, J. (1984) Distance methods for inferring phylogenies: A justification. Evolution 38, 1624.Google Scholar
Foster, J.E., Araya, J.E., Safanski, G.G., Cambron, S.E. & Taylor, P.L. (1988) Rearing Hessian fly for use in the development of resistant wheat. Purdue AES Bulletin #536.Google Scholar
Gagné, R.J., Hatchett, J.H., Lhaloui, S. & Bouhssini, M.E. (1991) Hessian fly and barley stem gall midge, two different species of Mayetiola (Diptera: Cecidoymyiidae) in Morocco. Annals of the Entomological Society of America 84, 436443.Google Scholar
Gepts, P. (2002) A comparison between crop domestication, classical plant breeding, and genetic engineering. Crop Science 42, 17801790.CrossRefGoogle Scholar
Harlan, J.R. & Zohary, D. (1966) Distribution of wild wheats and barley. Science 153, 10741080.Google Scholar
Harris, M.O., Stuart, J.J., Mohan, M., Nair, S., Lamb, R.J. & Rohfritsch, O. (2003) Grasses and gall midges: Plant defense and insect adaptation. Annual Review of Entomology 48, 549577.CrossRefGoogle ScholarPubMed
Harris, M.O., Freeman, T.P., Rohfritsch, O., Anderson, K.G., Payne, S.A. & Moore, J.A. (2006) Virulent Hessian fly (Diptera: Cecidomyiidae) larvae induce a nutritive tissue during compatible interactions with wheat. Annals of the Entomological Society of America 99, 305316.Google Scholar
Hatchett, J.H., Starks, K.J. & Webster, J.A. (1987) Insect and mite pests of wheat. pp. 625675in Heyne, E.G. (Ed.) Wheat and Wheat Improvement. Agronomy Monograph No. 13. Madison, WI, USA, ASA, CSSA and SSSA.Google Scholar
Hebert, P.D.N., Cywinska, A., Ball, S.L. & deWaard, J.R. (2003) Biological identification through DNA barcodes. Proceedings of the Royal Society of London, Series B 270, 313321.CrossRefGoogle ScholarPubMed
Hebert, P.D.N., Penton, E.H., Burns, J., Janzen, D.H. & Hallwachs, W. (2004) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly, Astraptes fulgerator. Proceedings of the National Academy of Science USA 101, 1481214817.Google Scholar
Hornik, K. (2011) The {R} FAQ. ISBN: 3-900051-08-9. Available online at http://www.cran.r-project.org/doc/FAQ/R-FAQ.html (accessed 31 March 2012).Google Scholar
Hubisz, M.J., Falush, D., Stephens, M. & Pritchard, J.K. (2009) Inferring weak population structure with the assistance of sample group information. Molecular Ecology Resources 9, 13221332.Google Scholar
Johnson, A.J., Schemerhorn, B.J. & Shukle, R.H. (2004) A first assessment of mitochondrial DNA variation and geographic distribution of haplotypes in the Hessian fly (Diptera: Cecidomyiidae). Annals of the Entomological Society of America 97, 940948.Google Scholar
Johnson, A.J., Morton, P.O., Schemerhorn, B.J. & Shukle, R.H. (2011) Use of a nuclear marker to assess population structure in Hessian fly (Diptera: Cecidomyiidae). Annals of the Entomological Society of America 104, 666674.Google Scholar
Lev-Yadun, S., Gopher, A. & Abbos, S. (2000) The cradle of agriculture. Science 288, 16021603.Google Scholar
Lidell, M.C. & Schuster, M.F. (1990) Distribution of the Hessian fly and its control in Texas. Southwestern Entomologist 15, 133145.Google Scholar
Liu, X.M., Brown-Guerdira, G.L., Hatchett, J.H., Owuoche, J.O. & Chen, M.S. (2005) Genetic characterization and molecular mapping of a Hessian fly-resistance gene transferred from Triticum turgidum spp. dicoccum to common wheat. Theoretical and Applied Genetics 111, 243249.Google Scholar
Martin-Sanchez, J.A., Gomez-Colmenarejo, M., Del Moral, J., Sin, E., Montes, M.J., Gonzalez-Belinchon, C., Lopez-Brana, I. & Delibes, A. (2003) A new Hessian fly resistance gene (H30) transferred from the wild grass Aegilops triuncialis to hexaploid wheat. Theoretical and Applied Genetics 106, 12481255.Google Scholar
Masel, J. (2011) Genetic drift. Current Biology 21(20), R837R838.CrossRefGoogle ScholarPubMed
McKeon, S.N., Lehr, M.A., Wilkerson, R.C., Ruiz, J.F., Sallum, M.A., Lima, J.B.P., Povoa, M.M. & Conn, J.E. (2010) Lineage divergence detected in the malaria vector Anopheles marajoara (Diptera: Culicidae) in Amazonian Brazil. Malaria Journal 9, 271283.Google Scholar
Morton, P.K., Foley, C.J. & Schemerhorn, B.J. (2011) Population structure and human influence on Hessian fly populations in the southeastern United States. Environmental Entomology 40(5), 13031316.Google Scholar
Naber, N., El Bouhssini, M., Labhilili, M., Udupa, S.M., Nachit, M.M., Baum, M., Lhaloui, S., Benslimane, A. & El Abbouyi, H. (2000) Genetic variation among population of the Hessian fly Mayetiola destructor (Diptera: Cecidomyiidae) in Morocco and Syria. Bulletin of Entomological Research 90, 245252.Google Scholar
Nevo, E. & Beiles, A. (1989) Genetic diversity of wild emmer wheat in Israel and Turkey: Structure, evolution and application in breeding. Theoretical and Applied Genetics 77, 421455.Google Scholar
Ozbeck, O., Millet, E., Anikster, Y., Arslan, O. & Feldman, M. (2007) Spatio-temporal genetic variation in populations of wild emmer wheat, Triticum turgidum ssp. dicoccoides, as revealed by AFLP analysis. Theoretical Applied Genetics 115, 1926.Google Scholar
Ozkan, H., Willcox, G., Graner, A., Salamini, F. & Killian, B. (2011) Geographic distribution and domestication of wild emmer wheat (Triticum dicoccoides). Genetic Resources and Crop Evolution 58, 1153.Google Scholar
Page, R.D.M. (1996) TREEVIEW: An application to display phylogenetic trees on person computers. Computer Application in the Biosciences 12, 357358.Google Scholar
Peng, J., Korol, A.B., Fahima, T., Roder, M.S., Ronin, Y.I., Li., Y.C. & Nevo, E. (2000) Molecular genetic maps in wild emmer wheat, Triticum dicoccoides: Genome-wide coverage, massive negative interference, and putative quasi-linkage. Genome Research 10, 15091531.Google Scholar
Poiarkova, H. & Blum, A. (1983) Landraces of wheat from the northern Negev in Israel. Euphytica 32, 257271.Google Scholar
Pritchard, J.K., Stephens, M. & Donnelly, P. (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945959.Google Scholar
Ratcliffe, R.H. & Hatchett, J.H. (1997) Biology and genetics of the Hessian fly and resistance in wheat. pp. 4756in Bondari, K. (Ed.) New Developments in Entomology. Trivandurm, India, Research Signpost, Scientific Information Guild.Google Scholar
Ratcliffe, R.H., Cambron, S.E., Flanders, K.L., Bosque-Perez, N.A., Clement, S.L. & Ohm, H.W. (2000) Biotype composition of Hessian fly (Diptera: Cecidomyiidae) populations from the southeastern, midwestern, and northwestern United States and virulence to resistance genes in wheat. Journal of Economic Entomology 93, 13191328.Google Scholar
Ratnasingham, S. & Hebert, P.D.N. (2007) Barcoding BOLD: The Barcoding of Life Data System (www.barcodinglife.org). Molecular Ecology Notes 7, 355364.Google Scholar
Rivnay, E. (1962) Field Crop Pests in the Near East, Monographiae Biologicae X. The Hague, The Netherlands, Dr W. Junk.Google Scholar
Rohfritsch, O. (1987) Different food supply strategies in midge-induced plant galls. pp. 195200in Labeyrie, V., Fabres, G. & Lachaise, D. (Eds) Insect-plants. The Hague, The Netherlands, Dr W. Junk.Google Scholar
Salamini, F., Ozkan, H., Brandolini, A., Schäfer-Pregl, R. & Martin, W. (2002) Genetics and geography of wild cereal domestication in the Near East. Genetics 3l 429441.Google Scholar
Sardesai, N., Nemacheck, J.A., Subramanyam, S. & Williams, C.E. (2005) Identification and mapping of H32, a new wheat gene conferring resistance to Hessian fly. Theoretical Applied Genetics 111, 11671173.Google Scholar
Schemerhorn, B.J., Crane, Y.M. & Morton, P.M. (2008) Development of polymorphic microsatellite markers in Hessian fly, Mayetiola destructor (Say). Molecular Ecology Resources 8, 13601362.CrossRefGoogle ScholarPubMed
Schemerhorn, B.J., Crane, Y.M., Morton, P.K., Aggarwal, R. & Benatti, T. (2009) Localization and characterization of 170 BAC-derived clones and mapping of 94 microsatellites in Hessian fly. Journal of Heredity 100, 790797.Google Scholar
Shachar, G. (2010) Israel: Local Grain Market Situation. USDA Foreign Agricultural Service Global Information Network, GAIN No-IS1011.Google Scholar
Shachar, G. (2011) USDA Foregin Agricultural Service Global Information Network, GAIN No-IS1102.Google Scholar
Sharon, D. & Kutiel, H. (1986) The distribution of rainfall intensity in Israel, its regional and seasonal variation and its climatological evaluation. Journal of Climatology 6, 277291.Google Scholar
Simms, S.R. & Russell, K.W. (1997) Bedouin hand harvesting of wheat and barley: implications for early cultivation in southwestern Asia. Current Anthropology 38l 696702.Google Scholar
Smith, A.A., Fisher, B.L. & Hebert, P.D.N. (2005) DNA barcoding for effective biodiversity assessment of a hyperdiversive arthropod group: the ants of Madagascar. Philosophical Transactions of the Royal Society, Series B 360, 18281834.Google Scholar
Stukenbrock, E.H., Banke, S. & McDonald, B.A. (2006) Global migration patterns in the fungal wheat pathogen Phaeosphaeria nodorum. Molecular Ecology 15, 28952904.Google Scholar
Svoray, T. & Karnieli, A. (2011) Rainfall, topography, and primary production relationships in a semiarid ecosystem. Ecohydrology 4, 5666.Google Scholar
Swofford, D.L. (2003) Phylogenetic Analysis Using Parsimony (* and other methods). Version 4. Sunderland, MA, USA, Sinauer Associates.Google Scholar
Van Oosterhout, C., Hutchinson, W.F., Wills, D.P.M. & Shipley, P. (2004) MICRO-CHECKER: software for identifying and correcting genotype errors in microsatellite data. Molecular Ecology Notes 4, 535538.Google Scholar
Williams, C.E., Collier, C.C., Sardesai, N., Ohm, H.W. & Cambron, S.E. (2003) Phenotypic assessment and mapped markers for H31, a new wheat gene conferring resistance to Hessian fly (Diptera: Cecidomyiidae). Theoretical and Applied Genetics 107, 15161523.Google Scholar
Zohary, D. & Hopf, M. (2000) Domestication of Plants in the Old World. 3rd edn. New York, USA, Oxford University Press.Google Scholar