Sequencing, de Novo assembly and annotation of the colorado potato beetle, Leptinotarsa decemlineata, transcriptome

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Kumar, Abhishek ^a,b   Congiu, Leonardo ^a   Lindström, Leena ^c   Piiroinen, Saija ^c   Vidotto, Michele ^a,d   Grapputo, Alessandro ^a  

^a UNIVERSITY OF PADOVA   (Italy)

^b UNIVERSITY OF KIEL   (Germany)

^c UNIVERSITY OF JYVÄSKYLÄ   (Finland)

^d Istituto di Genomica Applicata   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADAM PROTEIN; CADHERIN; CALMODULIN; CATALASE; CYTOCHROME P450; ESTERASE; GLUTATHIONE PEROXIDASE; GLUTATHIONE TRANSFERASE; SUPEROXIDE DISMUTASE;

ADULT; ARTICLE; BACILLUS THURINGIENSIS; COLORADO POTATO BEETLE; CONTIG MAPPING; CONTROLLED STUDY; DNA SEQUENCE; DROSOPHILA; DROSOPHILA MONTANA; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCUS; GENE ONTOLOGY; GENETIC TRANSCRIPTION; INSECTICIDE RESISTANCE; LARVA; NONHUMAN; NUCLEOTIDE SEQUENCE; PEST MANAGEMENT; PHYLOGENY; PYROSEQUENCING; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; UNINDEXED SEQUENCE;

ACTINS; ANIMALS; BAYES THEOREM; BEETLES; DIAPAUSE, INSECT; DRUG RESISTANCE; GENE ONTOLOGY; GENES, INSECT; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; INSECT PROTEINS; INTRODUCED SPECIES; LARVA; MICRORNAS; MOLECULAR SEQUENCE ANNOTATION; PHYLOGENY; POLYMORPHISM, SINGLE NUCLEOTIDE; SEQUENCE ANALYSIS, DNA; SERPINS; TRANSCRIPTOME;

EID: 84899860488     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0086012     Document Type: Article

References (99)

1. Alyokhin A, Baker M, Mota-Sanchez D, Dively G, Grafius E (2008) Colorado potato beetle resistance to insecticides. Am J Pot Res 85: 395-413.
2. Casagrande RA (1987) The Colorado potato beetle: 125 years of mismanagement. Bulletin of the ESA 33: 142-150.
3. Gauthier NL, Hofmaster R, Semel M (1981) History of Colorado potato beetle control. In: Lashomb JH, Casagrande RA, editors. Advances in Potato Pest Management Stroudsburg, PA.: Hutchinson Ross Publishing Company.
4. Weber DC, Ferro DN (1994) Colorado potato beetle: diverse life history poses challenge to management. In: Zehnder GW, Powelson ML, Jansson RK, Raman KV, editors. Advances in potato pest biology and management.St. Paul, Minnesota.: APS Press. pp. 256-259.
5. Smith IM, Charles LMF (1998) Distribution maps of quarantine pests for Europe: CABI.
6. Hare JD (1990) Ecology and management of the Colorado potato beetle. Annu Rev Entomol 35: 81-100.
7. Tower WL (1906) An investigation of evolution in chrysomelid beetles of the genus Leptinotarsa. Stroudsburg, PA.: Carnegie Institution of Washington.
8. Alyokhin A, Chen YH, Udalov M, Benkovskaya G, Lindström L (2013) Chapter 19 - Evolutionary considerations in potato pest management. Insect Pests of Potato. San Diego: Academic Press.pp. 543-571.
9. Weber D (2003) Colorado beetle: pest on the move. Pestic Outlook 14: 256-259.
10. Boman S, Grapputo A, Lindstrom L, Lyytinen A, Mappes J (2008) Quantitative genetic approach for assessing invasiveness: geographic and genetic variation in life-history traits. Biol Inv 10: 1135-1145.
11. EPPO (2003) Distribution maps of quarantine pests of Europe, Leptinotarsa decemlineta. European and Mediterranean plant protection organization (http://www.eppo.org).
12. Grapputo A, Boman S, Lindstrom L, Lyytinen A, Mappes J (2005) The voyage of an invasive species across continents: genetic diversity of North American and European Colorado potato beetle populations. Mol Ecol 14: 4207-4219. (Pubitemid 44943704)
13. Forgash AG (1985) Insecticide resistance in the Colorado potato beetle. In: Ferro DN, Voss RH, editors. Proceedings of the Symposium on the Colorado potato beetle: XVII International Congress of Entomology.pp. 256-259.
14. de Wilde J, Hsiao TH (1981) Geographic diversity of the Colorado potato beetle and its infestation in Eurasia. In: Lashomb JH, Casagrande RA, editors. Advances in Potato Pest Management Stroudsburg, PA.: Hutchinson Ross Publishing Company.
15. Tauber MJ, Tauber CA, Obrycki JJ, Gollands B, Wright RJ (1988) Voltinism and the induction of estival diapause in the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera, Chrysomelidae). Ann Entomol Soc Am 81: 748-754.
16. Kort CAD (1990) Thirty-five years of diapause research with the Colorado potato beetle. Entomol Exp Appl 56: 1-13.
17. Noronha C, Cloutier C (2006) Effects of potato foliage age and temperature regime on prediapause Colorado potato beetle Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). Environ Entomol 35: 590-599. (Pubitemid 44609576)
18. Yocum GD, Rinehart JP, Larson ML (2009) Down regulation of gene expression between the diapause initiation and maintenance phases of the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). Eur J Entomol 106: 471-476.
19. Baker MB, Porter AH (2008) Use of sperm precedence to infer the overwintering cost of insecticide resistance in the Colorado potato beetle. Agr Forest Entomol 10: 181-187. (Pubitemid 351977625)
20. Boivin T, Bouvier JC, Beslay D, Sauphanor B (2004) Variability in diapause propensity within populations of a temperate insect species: interactions between insecticide resistance genes and photoperiodism. Biol J Linn Soc 83: 341-351. (Pubitemid 39508993)
21. Carriere Y, Roff DA, Deland JP (1995) The joint evolution of diapause and insecticide resistance - a test of an optimality model. Ecology 76: 1497-1505.
22. Grewal PS, Power KT, Shetlar DJ (2001) Neonicotinoid insecticides alter diapause behavior and survival of overwintering white grubs (Coleoptera: Scarabaeidae). Pest Manag Sci 57: 852-857. (Pubitemid 32822984)
23. Tauber MJ, Tauber CA (1973) Quantitative response to daylength during diapause in insects. Nature 244: 296-297.
24. Tauber MJ, Tauber CA, Masaki S (1986) Seasonal adaptations of insects: Oxford University Press.
25. Denlinger DL (2008) Why study diapause? Entomol Res 38: 1-9.
26. Whalon ME, Miller DL, Hollingworth RM, Grafius EJ, Miller JC (1993) Selection of a Colorado potato beetle (Coleoptera, Chrysomelidae) strain resistant to Bacillus thuringiensis. J Econ Entomol 86: 226-233.
27. Rahardja U, Whalon ME (1995) Inheritance of resistance to Bacillus thuringiensis subsp. tenebrionis CryIIIA delta-endotoxin in Colorado potato beetle (Coleoptera: Chrysomelidae). J Econ Entomol 8: 21-26.
28. Alyokhin A (2009) Colorado potato beetle management on potatoes: current challenges and future prospects. In: Tennant P, Benkeblia N, editors. Potato II Fruit, Vegetable and Cereal Science and Biotechnology 3: Global Science Books Ltd.pp. 10-19.
29. Evans JD, Brown SJ, Consortium iK (2013) The i5K Initiative: advancing arthropod genomics for knowledge, human health, agriculture, and the environment. J Hered 104: 595-600.
30. Petek M, Turnsek N, Gasparic MB, Novak MP, Gruden K, et al. (2012) A complex of genes involved in adaptation of Leptinotarsa decemlineata larvae to induced potato defense. Arch Insect Biochem Physiol 79: 153-181.
31. Yocum GD, Rinehart JP, Chirumamilla-Chapara A, Larson ML (2009) Characterization of gene expression patterns during the initiation and maintenance phases of diapause in the Colorado potato beetle, Leptinotarsa decemlineata. J Insect Physiol 55: 32-39.
32. Pauchet Y, Wilkinson P, Chauhan R, Ffrench-Constant RH (2010) Diversity of beetle genes encoding novel plant cell wall degrading enzymes. PLoS One 5: e15635.
33. Choi J-H, Kijimoto T, Snell-Rood E, Tae H, Yang Y, et al. (2010) Gene discovery in the horned beetle Onthophagus taurus . BMC Genomics 11: 703.
34. Pauchet Y, Wilkinson P, van Munster M, Augustin S, Pauron D, et al. (2009) Pyrosequencing of the midgut transcriptome of the poplar leaf beetle Chrysomela tremulae reveals new gene families in Coleoptera. Insect Biochem Mol Biol 39: 403-413.
35. Vera JC, Wheat CW, Fescemyer HW, Frilander MJ, Crawford DL, et al. (2008) Rapid transcriptome characterization for a nonmodel organism using 454 pyrosequencing. Mol Ecol 17: 1636-1647. (Pubitemid 351441703)
36. Morozova O, Hirst M, Marra MA (2009) Applications of new sequencing technologies for transcriptome analysis. Annu Rev Genomics Hum Genet 10: 135-151.
37. Schuster SC (2008) Next-generation sequencing transforms today's biology. Nat Meth 5: 16-18.
38. Pauchet Y, Wilkinson P, Vogel H, Nelson DR, Reynolds SE, et al. (2010) Pyrosequencing the Manduca sexta larval midgut transcriptome: messages for digestion, detoxification and defence. Insect Mol Biol 19: 61-75.
39. Chevreux B, Pfisterer T, Drescher B, Driesel AJ, Muller WE, et al. (2004) Using the miraEST assembler for reliable and automated mRNA transcript assembly and SNP detection in sequenced ESTs. Genome Res 14: 1147-1159. (Pubitemid 38811551)
40. Richards S, Gibbs RA, Weinstock GM, Brown SJ, Denell R, et al. (2008) The genome of the model beetle and pest Tribolium castaneum . Nature 452: 949-955.
41. Gotz S, Garcia-Gomez JM, Terol J, Williams TD, Nagaraj SH, et al. (2008) High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res 36: 3420-3435. (Pubitemid 351859009)
42. Conesa A, Gotz S (2008) Blast2GO: A comprehensive suite for functional analysis in plant genomics. Int J Plant Genomics 2008: 619832.
43. Bai X, Mamidala P, Rajarapu SP, Jones SC, Mittapalli O (2011) Transcriptomics of the bed bug (Cimex lectularius). PLoS One 6: e16336.
44. Bai X, Rivera-Vega L, Mamidala P, Bonello P, Herms DA, et al. (2011) Transcriptomic signatures of ash (Fraxinus spp.) phloem. PLoS One 6: e16368.
45. Bai X, Zhang W, Orantes L, Jun TH, Mittapalli O, et al. (2010) Combining next-generation sequencing strategies for rapid molecular resource development from an invasive aphid species, Aphis glycines. PLoS One 5: e11370.
46. Mittapalli O, Bai X, Mamidala P, Rajarapu SP, Bonello P, et al. (2010) Tissue-specific transcriptomics of the exotic invasive insect pest emerald ash borer (Agrilus planipennis). PLoS One 5: e13708.
47. Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136: 215-233.
48. He L, Hannon GJ (2004) MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 5: 522-531. (Pubitemid 38868508)
49. Kozomara A, Griffiths-Jones S (2011) miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 39: D152-157.
50. Kumar A, Ragg H (2008) Ancestry and evolution of a secretory pathway serpin. BMC Evol Biol 8: 250.
51. Silverman G, Bird P, Carrell R, Church F, Coughlin P, et al. (2001) The serpins are an expanding superfamily of structurally similar but functionally diverse proteins. Evolution, mechanism of inhibition, novel functions, and a revised nomenclature. J Biol Chem 276: 33293-33296.
52. Reichhart JM (2005) Tip of another iceberg: Drosophila serpins. Trends Cell Biol 15: 659-665.
53. Zou Z, Evans JD, Lu Z, Zhao P, Williams M, et al. (2007) Comparative genomic analysis of the Tribolium immune system. Genome Biol 8: R177.
54. Kruger O, Ladewig J, Koster K, Ragg H (2002) Widespread occurrence of serpin genes with multiple reactive centre-containing exon cassettes in insects and nematodes. Gene 293: 97-105. (Pubitemid 34876465)
55. Kankare M, Salminen T, Laiho A, Vesala L, Hoikkala A (2010) Changes in gene expression linked with adult reproductive diapause in a northern malt fly species: a candidate gene microarray study. BMC Ecol 10: 3.
56. Ioannidis PM, Grafius E, Whalon ME (1991) Patterns of insecticide resistance to azinphosmethyl, carbofuran, and permethrin in the Colorado potato beetle (Coleoptera, Chrysomelidae). J Econ Entomol 84: 1417-1423.
57. Schuler MA (2011) P450s in plant-insect interactions. Biochim Biophys Acta 1814: 36-45.
58. Zhang S, Shukle R, Mittapalli O, Zhu YC, Reese JC, et al. (2010) The gut transcriptome of a gall midge, Mayetiola destructor . J Insect Physiol 56: 1198-1206.
59. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402. (Pubitemid 27359211)
60. Yan L, Yang P, Jiang F, Cui N, Ma E, et al. (2012) Transcriptomic and phylogenetic analysis of Culex pipiens quinquefasciatus for three detoxification gene families. BMC Genomics 13: 609.
61. Enayati AA, Ranson H, Hemingway J (2005) Insect glutathione transferases and insecticide resistance. Insect Mol Biol 14: 3-8. (Pubitemid 40218079)
62. Friedman R (2011) Genomic organization of the glutathione S-transferase family in insects. Mol Phylogenet Evol 61: 924-932.
63. Che-Mendoza A, Penilla RP, Rodriguez DA (2009) Insecticide resistance and glutathione S-transferases in mosquitoes: A review. Afr J Biotechnol 8: 1386-1397.
64. Board PG, Baker RT, Chelvanayagam G, Jermiin LS (1997) Zeta, a novel class of glutathione transferases in a range of species from plants to humans. Biochem J 328 (Pt 3): 929-935. (Pubitemid 28005795)
65. Yu Q, Lu C, Li B, Fang S, Zuo W, et al. (2008) Identification, genomic organization and expression pattern of glutathione S-transferase in the silkworm, Bombyx mori. Insect Biochem Mol Biol 38: 1158-1164.
66. Fabrick J, Oppert C, Lorenzen MD, Morris K, Oppert B, et al. (2009) A novel Tenebrio molitor cadherin is a functional receptor for Bacillus thuringiensis Cry3Aa toxin. J Biol Chem 284: 18401-18410.
67. Loseva O, Ibrahim M, Candas M, Koller CN, Bauer LS, et al. (2002) Changes in protease activity and Cry3Aa toxin binding in the Colorado potato beetle: implications for insect resistance to Bacillus thuringiensis toxins. Insect Biochem Mol Biol 32: 567-577. (Pubitemid 34274826)
68. Ochoa-Campuzano C, Real MD, Martínez-Ramírez AC, Bravo A, Rausell C (2007) An ADAM metalloprotease is a Cry3Aa Bacillus thuringiensis toxin receptor. Biochemical and Biophysical Research Communications 362: 437-442. (Pubitemid 47332428)
69. Ochoa-Campuzano C, Sánchez J-RI, Real MD, Rausell C, Sánchez J (2012) Identification of a calmodulin-binding site within the domain i of Bacillus thuringiensis Cry3Aa toxin. Archives of Insect Biochemistry and Physiology 81: 53-62.
70. Park Y, Abdullah MAF, Taylor MD, Rahman K, Adang MJ (2009) Enhancement of Bacillus thuringiensis Cry3Aa and Cry3Bb toxicities to coleopteran larvae by a toxin-binding fragment of an insect cadherin. Applied and Environmental Microbiology 75: 3086-3092.
71. Sayed A, Wiechman B, Struewing I, Smith M, French W, et al. (2010) Isolation of transcripts from Diabrotica virgifera virgifera LeConte responsive to the Bacillus thuringiensis toxin Cry3Bb1. Insect Mol Biol 19: 381-389.
72. Blessing CA, Ugrinova GT, Goodson HV (2004) Actin and ARPs: action in the nucleus. Trends Cell Biol 14: 435-442. (Pubitemid 39092701)
73. Goodson HV, Hawse WF (2002) Molecular evolution of the actin family. J Cell Sci 115: 2619-2622. (Pubitemid 34846503)
74. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, et al. (2012) The Pfam protein families database. Nucleic Acids Res 40: D290-D301.
75. Knudsen T, Knudsen B (2013) CLC Genomics Benchwork 6. Available: http://www.clcbio.com. Accessed on 2013 Sept 20.
76. Klug A (1999) Zinc finger peptides for the regulation of gene expression. J Mol Biol 293: 215-218.
77. Matthews JM, Sunde M (2002) Zinc fingers-folds for many occasions. IUBMB Life 54: 351-355.
78. Liu Z, Friedrich M (2004) The Tribolium homologue of glass and the evolution of insect larval eyes. Dev Biol 269: 36-54. (Pubitemid 38471822)
79. Parthasarathy R, Tan A, Bai H, Palli SR (2008) Transcription factor broad suppresses precocious development of adult structures during larval-pupal metamorphosis in the red flour beetle, Tribolium castaneum. Mech Dev 125: 299-313.
80. Stirnimann CU, Petsalaki E, Russell RB, Muller CW (2010) WD40 proteins propel cellular networks. Trends Biochem Sci 35: 565-574.
81. Blatch GL, Lassle M (1999) The tetratricopeptide repeat: a structural motif mediating protein-protein interactions. Bioessays 21: 932-939. (Pubitemid 29530602)
82. Smith DF (2004) Tetratricopeptide repeat cochaperones in steroid receptor complexes. Cell Stress Chaperones 9: 109-121.
83. Feyereisen R (2006) Evolution of insect P450. Biochem Soc Trans 34: 1252-1255.
84. Rashkova S, Karam SE, Kellum R, Pardue ML (2002) Gag proteins of the two Drosophila telomeric retrotransposons are targeted to chromosome ends. J Cell Biol 159: 397-402. (Pubitemid 35332826)
85. Rashkova S, Karam SE, Pardue ML (2002) Element-specific localization of Drosophila retrotransposon Gag proteins occurs in both nucleus and cytoplasm. Proc Natl Acad Sci U S A 99: 3621-3626. (Pubitemid 34252156)
86. Behura SK (2006) Molecular marker systems in insects: current trends and future avenues. Mol Ecol 15: 3087-3113.
87. Zhu YY, Machleder EM, Chenchik A, Li R, Siebert PD (2001) Reverse transcriptase template switching: a SMART approach for full-length cDNA library construction. Biotechniques 30: 892-897. (Pubitemid 32319835)
88. Zhulidov PA, Bogdanova EA, Shcheglov AS, Vagner LL, Khaspekov GL, et al. (2004) Simple cDNA normalization using kamchatka crab duplex-specific nuclease. Nucleic Acids Res 32: e37.
89. Shagin DA, Rebrikov DV, Kozhemyako VB, Altshuler IM, Shcheglov AS, et al. (2002) A novel method for SNP detection using a new duplex-specific nuclease from crab hepatopancreas. Genome Res 12: 1935-1942. (Pubitemid 35469943)
90. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, et al. (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437: 376-380. (Pubitemid 41613494)
91. Papanicolaou A, Stierli R, Ffrench-Constant RH, Heckel DG (2009) Next generation transcriptomes for next generation genomes using est2assembly. BMC Bioinformatics 10: 447.
92. Schmieder R, Edwards R (2011) Fast identification and removal of sequence contamination from genomic and metagenomic datasets. PloS one 6.
93. Huson DH, Mitra S, Ruscheweyh HJ, Weber N, Schuster SC (2011) Integrative analysis of environmental sequences using MEGAN4. Genome Res 21: 1552-1560.
94. Vidotto M, Grapputo A, Boscari E, Barbisan F, Coppe A, et al. (2013) Transcriptome sequencing and de novo annotation of the critically endangered Adriatic sturgeon. BMC Genomics 14: 407.
95. Thurston MI, Field D (2005) Msatfinder: detection and characterisation of microsatellites. Available: http://www.genomics.ceh.ac.uk/msatfinder/. Accessed on 2011 April 20.
96. Marden JH, Fescemyer HW, Saastamoinen M, MacFarland SP, Vera JC, et al. (2008) Weight and nutrition affect pre-mRNA splicing of a muscle gene associated with performance, energetics and life history. Journal of Experimental Biology 211: 3653-3660.
97. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574. (Pubitemid 37038874)
98. Milne I, Lindner D, Bayer M, Husmeier D, McGuire G, et al. (2009) TOPALi v2: a rich graphical interface for evolutionary analyses of multiple alignments on HPC clusters and multi-core desktops. Bioinformatics 25: 126-127.
99. Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39: W29-37.