Western corn rootworm (Diabrotica virgifera virgifera) transcriptome assembly and genomic analysis of population structure

BMC Genomics

Andy P Michel²  Barry S Goldman¹  Thomas Clark¹  Ronald Flannagan¹  Matthew Carroll¹  Mao Chen¹  Randall A Kerstetter¹  Raman Bansal²  Lex E Flagel¹ 

[1] Monsanto Company, 700 Chesterfield Parkway W, Chesterfield, MO 63017, USA;Department of Entomology, Ohio Agricultural Research and Development Center, 1680 Madison Ave., Wooster, OH 44691, USA

关键词: Western corn rootworm;    Transcriptome;    Transgenic crop;    Insect resistance;    Diabrotica virgifera virgifera;   

Others  :  1217764
DOI  :  10.1186/1471-2164-15-195

 received in 2013-10-15, accepted in 2014-03-04,  发布年份 2014

【 摘 要 】

Background

Western corn rootworm (WCR) is one of the most significant insect pests of maize in North America. WCR has dramatically increased its range in the last century, invading key maize production areas in the US and abroad. In addition, this species has a history of evolving traits that allow it to escape various control options. Improved genetic and genomic resources are crucial tools for understanding population history and the genetic basis of trait evolution. Here we produce and analyze a transcriptome assembly for WCR. We also perform whole genome population resequencing, and combine these resources to better understand the evolutionary history of WCR.

Results

The WCR transcriptome assembly presented here contains approximately 16,000 unigenes, many of which have high similarity to other insect species. Among these unigenes we found several gene families that have been implicated in insecticide resistance in other species. We also identified over 500,000 unigene based SNPs among 26 WCR populations. We used these SNPs to scan for outliers among the candidate genes, and to understand how population processes have shaped genetic variation in this species.

Conclusions

This study highlights the utility of transcriptomic and genomic resources as foundational tools for dealing with highly adaptive pest species. Using these tools we identified candidate gene families for insecticide resistance and reveal aspects of WCR population history in light of the species’ recent range expansion.

【 授权许可】

   
2014 Flagel et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Chandler LD, Woodson WD, Ellsbury MM: Corn rootworm IPM: implementation and information management with GIS. In Proceedings of the American Seed Trade Association 52nd Annual Corn and Soybean Research Conference: 1998; Chicago Edited by Wilkinson D. 1998, 129-143.
• [2]Mitchell PD, Gray ME, Steffey KL: A composed-error model for estimating pest-damage functions and the impact of the Western Corn Rootworm soybean variant in Illinois. Am J Agr Econ 2004, 86(2):332-344.
• [3]Gray ME, Sappington TW, Miller NJ, Moeser J, Bohn MO: Adaptation and invasiveness of Western Corn Rootworm: intensifying research on a worsening pest. Annu Rev Entomol 2009, 54(1):303-321.
• [4]Miller N, Estoup A, Toepfer S, Bourguet D, Lapchin L, Derridj S, Kim KS, Reynaud P, Furlan L, Guillemaud T: Multiple transatlantic introductions of the Western Corn Rootworm. Science 2005, 310(5750):992.
• [5]Krysan J, Foster D, Branson T, Ostlie K, Cranshaw W: Two years before the hatch: rootworms adapt to crop rotation. Bull Entomol Soc Am 1986, 32:250-253.
• [6]Sammons A, Edwards R, Bledsoe L, Boeve P, Stuart J: Behavioral and feeding assays reveal a western corn rootworm (Coleoptera: Chrysomelidae) variant that is attracted to soybean. Environ Entomol 1997, 26:1336-1342.
• [7]Zhu KY, Wilde GE, Higgins RA, Sloderbeck PE, Buschman LL, Shufran RA, Whitworth RJ, Starkey SR, He F: Evidence of evolving carbaryl resistance in western corn rootworm (Coleoptera: Chrysomelidae) in areawide-managed cornfields in north central Kansas. J Econ Entomol 2001, 94(4):929-934.
• [8]Parimi S, Meinke LJ, French B, Chandler LD, Siegfried BD: Stability and persistence of aldrin and methyl-parathion resistance in western corn rootworm (Coleoptera: Chrysomelidae). Crop Prot 2006, 25:269-274.
• [9]Meinke LJ, Siegfried BD, Wright RJ, Chandler LD: Adult susceptibility of Nebraska western corn rootworm (Coleoptera: Chrysomelidae) populations to selected insecticides. J Econ Entomol 1998, 91(3):594-600.
• [10]Miller NJ, Guillemaud T, Giordano R, Siegfried BD, Gray ME, Meinke LJ, Sappington TW: Genes, gene flow and adaptation of Diabrotica virgifera virgifera. Agric For Entomol 2009, 11(1):47-60.
• [11]Gassmann AJ, Petzold-Maxwell JL, Keweshan RS, Dunbar MW: Field-evolved resistance to Bt maize by Western Corn Rootworm. PLoS ONE 2011, 6(7):e22629.
• [12]Chu C-C, Spencer JL, Curzi MJ, Zavala JA, Seufferheld MJ: Gut bacteria facilitate adaptation to crop rotation in the western corn rootworm. Proc Natl Acad Sci USA 2013, 110:11917-11922.
• [13]Curzi MJ, Zavala JA, Spencer JL, Seufferheld MJ: Abnormally high digestive enzyme activity and gene expression explain the contemporary evolution of a Diabrotica biotype able to feed on soybeans. Ecol Evol 2012, 2:2005-2017.
• [14]Wang H, Coates BS, Chen H, Sappington TW, Guillemaud T, Siegfried BD: Role of a gamma-aminobutryic acid (GABA) receptor mutation in the evolution and spread of Diabrotica virgifera virgifera resistance to cyclodiene insecticides. Insect Mol Biol 2013. Early Access; doi:10.1111/imb.12037
• [15]Siegfried BD, Waterfield N, ffrench-Constant RH: Expressed sequence tags from Diabrotica virgifera virgifera midgut identify a coleopteran cadherin and a diversity of cathepsins. Insect Mol Biol 2005, 14:137-143.
• [16]Scharf ME, Parimi S, Meinke LJ, Chandler LD, Siegfried BD: Expression and induction of three family 4 cytochrome P450 (CYP4) genes identified from insecticide-resistant and susceptible western corn rootworms, Diabrotica virgifera virgifera. Insect Mol Biol 2001, 10:139-146.
• [17]Feyereisen R: Evolution of insect P450. Biochem Soc Trans 2006, 34:1252-1255.
• [18]Zhu F, Moural TW, Shah K, Palli SR: Integrated analysis of cytochrome P450 gene superfamily in the red flour beetle. Tribolium castaneum. BMC Genomics 2013, 14:174. BioMed Central Full Text
• [19]Zhu KY, Wilde GE, Sloderbeck PE, Buschman LL, Higgins RA, Whitworth RJ, Bowling RA, Starkey SR, He F: Comparative susceptibility of western corn rootworm (Coleoptera: Chrysomelidae) adults to selected insecticides in Kansas. J Econ Entomol 2005, 98:2181-2187.
• [20]Pigott CR, Ellar DJ: Role of receptors in Bacillus thuringiensis crystal toxin activity. Microbiol Mol Biol Rev 2007, 71(2):255-281.
• [21]Coates BS, Sumerford DV, Miller NJ, Kim KS, Sappington TW, Siegfried BD, Lewis LC: Comparative performance of single nucleotide polymorphism and microsatellite markers for population genetic analysis. J Hered 2009, 100(5):556-564.
• [22]Miller NJ, Ciosi M, Sappington TW, Ratcliffe ST, Spencer JL, Guillemaud T: Genome scan of Diabrotica virgifera virgifera for genetic variation associated with crop rotation tolerance. J Appl Entomol 2007, 131(6):378-385.
• [23]Miller NJ, Kim KS, Ratcliffe ST, Estoup A, Bourguet D, Guillemaud T: Absence of genetic divergence between Western Corn Rootworms (Coleoptera: Chrysomelidae) resistant and susceptible to control by crop rotation. J Econ Entomol 2006, 99(3):685-690.
• [24]Szalanski A, Roehrdanz R, Taylor D, Chandler L: Genetic variation in geographical populations of western and Mexican corn rootworm. Insect Mol Biol 1999, 8(4):519-525.
• [25]Kim KS, Sappington TW: Genetic structuring of Western Corn Rootworm (Coleoptera: Chrysomelidae) populations in the United States based on microsatellite loci analysis. Environ Entomol 2005, 34(2):494-503.
• [26]Coates BS, Alves AP, Wang H, Walden KKO, French BW, Miller NJ, Abel CA, Robertson HM, Sappington TW, Siegfried BD: Distribution of genes and repetitive elements in the Diabrotica virgifera virgifera genome estimated using BAC sequencing. J Biomed Biotechnol 2012, 2012:9.
• [27]Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M: Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 2005, 21(18):3674-3676.
• [28]Hu Z, Bao J, Reecy JM: CateGOrizer: a web-based program to batch analyze gene ontology classification categories. Onl J Bioinform 2008, 9:108-112.
• [29]Kanehisa M, Susumu G: KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 2000, 28:27-30.
• [30]O’Neil ST, Dzurisin JD, Carmichael RD, Lobo NF, Emrich SJ, Hellmann JJ: Population-level transcriptome sequencing of nonmodel organisms Erynnis propertius and Papilio zelicaon. BMC Genomics 2010, 11:310. BioMed Central Full Text
• [31]Meihls LN, Higdon ML, Ellersieck MR, Tabashnik BE, Hibbard BE: Greenhouse-selected resistance to Cry3Bb1-producing corn in three Western Corn Rootworm populations. PLoS ONE 2012, 7(12):e51055.
• [32]Li H, Durbin R: Fast and accurate long read alignment with Burrows-Wheeler transform. Bioinformatics 2010, 26:589-595.
• [33]Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Subgroup GPDP: The sequence alignment/map format and SAMtools. Bioinformatics 2009, 25(16):2078-2079.
• [34]Konieczny A, Ausubel FM: A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. Plant J 1993, 4:403-410.
• [35]Cock PJA, Antao T, Chang JT, Chapman BA, Cox CJ, Dalke A, Friedberg I, Hamelryck T, Kauff F, Wilczynski B, de Hoon MJL: Biopython: freely available Python tools for computational molecular biology and bioinformatics. Bioinformatics 2009, 25(11):1422-1423.
• [36]Futschik A, Schlötterer C: The next generation of molecular markers from massively parallel sequencing of pooled DNA samples. Genetics 2010, 186(1):207-218.
• [37]Kofler R, Pandey RV, Schlötterer C: PoPoolation2: identifying differentiation between populations using sequencing of pooled DNA samples (Pool-Seq). Bioinformatics 2011, 27:3435-3436.
• [38]Noor MAF, Bennett SM: Islands of speciation or mirages in the desert? Examining the role of restricted recombination in maintaining species. Heredity 2009, 103:439-444.
• [39]Charlesworth B: Measures of divergence between populations and the effect of forces that reduce variability. Mol Biol Evol 1998, 15:538-543.
• [40]Nei M, Kumar S: Molecular Evolution and Phylogenetics. New York: Oxford University Press; 2000.
• [41]Willing E, Dreyer C, van Oosterhout C: Estimates of genetic differentiation measured by Fst do not necessarily require large sample sizes when using many SNP markers. PLoS ONE 2012, 7:e42649.
• [42]Pluzhnikov A, Donnelly P: Optimal sequencing strategies for surveying molecular genetic diversity. Genetics 1996, 144:1247-1262.
• [43]Bai X, Zhang W, Orantes L, Jun T-H, Mittapalli O, Mian MAR, Michel AP: Combining next-generation sequencing strategies for rapid molecular resource development from an invasive aphid species, Aphis glycines. PLoS ONE 2010, 5(6):e11370.
• [44]Chen Y, Cassone BJ, Bai X, Redinbaugh MG, Michel AP: Transcriptome of the plant virus vector Graminella nigrifrons, and the molecular interactions of Maize fine streak rhabdovirus transmission. PLoS ONE 2012, 7(7):e40613.
• [45]Mittapalli O, Bai X, Mamidala P, Rajarapu SP, Bonello P, Herms DA: Tissue-specific transcriptomics of the exotic invasive insect pest emerald ash borer (Agrilus planipennis). PLoS ONE 2010, 5(10):e13708.
• [46]Zbobnov EM, Apweiler R: InterProScan - an integration platform for the signature-recognition methods in InterPro. Bioinformatics 2001, 17:847-848.
• [47]Keeling CI, Yuen MM, Liao NY, Roderick Docking T, Chan SK, Taylor GA, Palmquist DL, Jackman SD, Nguyen A, Li M, Henderson H, Janes JK, Zhao Y, Pandoh P, Moore R, Sperling FAH, Huber DPW, Birol I, Jones SJM, Bohlmann J: Draft genome of the mountain pine beetle, Dendroctonus ponderosae Hopkins, a major forest pest. Genome Biol 2013, 14:R27. BioMed Central Full Text
• [48]Tribolium Genome Sequencing Consortium: The genome of the model beetle and pest Tribolium castaneum. Nature 2008, 452(7190):949-955.
• [49]Contreras E, Schoppmeier M, Real MD, Rausell C: Sodium solute symporter and cadherin proteins act as Bacillus thuringiensis Cry3Ba toxin functional receptors in Tribolium castaneum. J Biol Chem 2013, 288:18013-18021.
• [50]Fabrick J, Oppert C, Lorenzen MD, Morris K, Oppert B, Jurat-Fuentes JL: A novel Tenebrio molitor cadherin is a functional receptor for Bacillus thuringiensis Cry3Aa toxin. J Biol Chem 2009, 284(27):18401-18410.
• [51]Gahan LJ, Pauchet Y, Vogel H, Heckel DG: An ABC transporter mutation is correlated with insect resistance to Bacillus thuringiensis Cry1Ac toxin. PLoS Genet 2010, 6(12):e1001248.
• [52]Griffitts JS, Haslam SM, Yang T, Garczynski SF, Mulloy B, Morris H, Cremer PS, Dell A, Adang MJ, Aroian RV: Glycolipids as receptors for Bacillus thuringiensis crystal toxin. Science 2005, 307(5711):922-925.
• [53]Atsumi S, Miyamoto K, Yamamoto K, Narukawa J, Kawai S, Sezutsu H, Kobayashi I, Uchino K, Tamura T, Mita K, Kadono-Okuda K, Wada S, Kanda K, Goldsmith MR, Noda H: Single amino acid mutation in an ATP-binding cassette transporter gene causes resistance to Bt toxin Cry1Ab in the silkworm, Bombyx mori. Proc Natl Acad Sci 2012, 109(25):E1591-E1598.
• [54]Falconer DS, Mackay TFC: Introduction to Quantitative Genetics. 4th edition. Harlow, UK: Longman Group Ltd; 1996.
• [55]Kim KS, French BW, Sumerford DV, Sappington TW: Genetic diversity in laboratory colonies of Western Corn Rootworm (Coleoptera: Chrysomelidae), including a nondiapause colony. Environ Entomol 2007, 36(3):637-645.
• [56]Branson T: The selection of a non-diapause strain of Diabrotica virgifera (Coleoptera: Chrysomelidae). Entomol Exp Appl 1976, 19:148-154.
• [57]Excoffier L, Foll M, Petit R: Genetic consequences of range expansion. Annu Rev Ecol Syst 2009, 40:481-501.
• [58]Rousset F: Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 1997, 145:1219-1228.
• [59]McDonald BA, Linde C: Pathogen population genetics, evolutionary potential, and durable resistance. Annu Rev Phytopathol 2002, 40:349-379.
• [60]Denver DR, Dolan PC, Wilhelm LJ, Sung W, Lucas-Lledó JI, Howe DK, Lewis SC, Okamoto K, Thomas WK, Lynch M, Baer CF: A genome-wide view of Caenorhabditis elegans base-substitution mutation processes. Proc Natl Acad Sci 2009, 106:16310-16314.
• [61]Haag-Liautard C, Dorris M, Maside X, Macaskill S, Halligan DL, Charlesworth B, Keightley PD: Direct estimation of per nucleotide and genomic deleterious mutation rates in Drosophila. Nature 2007, 445(7123):82-85.