A heterozygous moth genome provides insights into herbivory and detoxification

Nature Genetics

Volumn 45, Issue 2, 2013, Pages 220-225

  You, Minsheng ^a,b   Yue, Zhen ^c   He, Weiyi ^a,b   Yang, Xinhua ^c   Yang, Guang ^a,b   Xie, Miao ^a,b   Zhan, Dongliang ^c   Baxter, Simon W ^d,e   Vasseur, Liette ^a,b,f   Gurr, Geoff M ^a,b,g   Douglas, Carl J ^a,b,h   Bai, Jianlin ^a,b   Wang, Ping ⁱ   Cui, Kai ^a,b   Huang, Shiguo ^a,b   Li, Xianchun ^j   Zhou, Qing ^c   Wu, Zhangyan ^c   Chen, Qilin ^c   Liu, Chunhui ^a,b   Wang, Bo ^c   Li, Xiaojing ^a,b   Xu, Xiufeng ^a,b   Lu, Changxin ^c   Hu, Min ^c   Davey, John W ^k   Smith, Sandy M ^a,b,l   Chen, Mingshun ^m   Xia, Xiaofeng ^a,b   Tang, Weiqi ^a,b   Ke, Fushi ^a,b   Zheng, Dandan ^a,b   Hu, Yulan ^a,b   Song, Fengqin ^a,b   You, Yanchun ^a,b   Ma, Xiaoli ^a,b   Peng, Lu ^a,b   Zheng, Yunkai ^a,b   Liang, Yong ^a,b   Chen, Yaqiong ^a,b   Yu, Liying ^a,b   Zhang, Younan ^a,b   Liu, Yuanyuan ^h   Li, Guoqing ^c   Fang, Lin ^c   Li, Jingxiang ^c   Zhou, Xin ^c   Luo, Yadan ^c   Gou, Caiyun ^c   Wang, Junyi ^c   Wang, Jian ^c   Yang, Huanming ^c   Wang, Jan ^c,n   more..

^a FUJIAN AGRICULTURE AND FORESTRY UNIVERSITY   (China)

^b AGRO ENVIRONMENTAL PROTECTION INSTITUTE   (China)

^c BGI SHENZHEN   (China)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e UNIVERSITY OF ADELAIDE   (Australia)

^f BROCK UNIVERSITY   (Canada)

^g CHARLES STURT UNIVERSITY   (Australia)

^h UNIVERSITY OF BRITISH COLUMBIA   (Canada)

ⁱ New York State Agricultural Experiment Station   (United States)

^j UNIVERSITY OF ARIZONA   (United States)

^k UNIVERSITY OF EDINBURGH   (United Kingdom)

^l UNIVERSITY OF TORONTO   (Canada)

^m KANSAS STATE UNIVERSITY   (United States)

ⁿ UNIVERSITY OF COPENHAGEN   (Denmark)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CHROMOSOME REPLICATION; DETOXIFICATION; GENE SEQUENCE; HERBIVORY; INSECT GENOME; INSECTICIDE RESISTANCE; LEPIDOPTERA; MOTH; NONHUMAN; PEST MANAGEMENT; PHYLOGENY; PRIORITY JOURNAL; PROTEIN METABOLISM; RETROPOSON; SINGLE NUCLEOTIDE POLYMORPHISM;

ADAPTATION, BIOLOGICAL; ANIMALS; BASE SEQUENCE; CHINA; CHROMOSOMES, ARTIFICIAL, BACTERIAL; COMPUTATIONAL BIOLOGY; EVOLUTION, MOLECULAR; EXPRESSED SEQUENCE TAGS; FEMALE; GENE EXPRESSION PROFILING; GENETIC VARIATION; GENOME; GLUCOSINOLATES; HERBIVORY; HETEROZYGOTE; MALE; MOLECULAR SEQUENCE ANNOTATION; MOLECULAR SEQUENCE DATA; MOTHS; MUTATION; PEST CONTROL; PHYLOGENY; POLYMORPHISM, SINGLE NUCLEOTIDE; REAL-TIME POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; SULFATASES;

HEXAPODA; LEPIDOPTERA; PLUTELLA XYLOSTELLA;

EID: 84873087245     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.2524     Document Type: Article

References (85)

1. Whiteman, N.K. & Jander, G. Genome-enabled research on the ecology of plant-insect interactions. Plant Physiol. 154, 475-478 (2010).
2. Ali, J.G. & Agrawal, A.A. Specialist versus generalist insect herbivores and plant defense. Trends Plant Sci. 17, 293-302 (2012).
3. Ratzka, A., Vogel, H., Kliebenstein, D.J., Mitchell-Olds, T. & Kroymann, J. Disarming the mustard oil bomb. Proc. Natl. Acad. Sci. USA 99, 11223-11228 (2002).
4. Talekar, N.S. & Shelton, A.M. Biology, ecology, and management of the diamondback moth. Annu. Rev. Entomol. 38, 275-301 (1993).
5. Furlong, M.J., Wright, D.J. & Dosdall, L.M. Diamondback moth ecology and management: problems, progress, and prospects. Annu. Rev. Entomol. published online; doi:10.1146/annurev-ento-120811-153605 (27 September 2012).
6. Zalucki, M.P. et al. Estimating the economic cost of one of the world's major insect pests, Plutella xylostella (Lepidoptera: Plutellidae): just how long is a piece of string? J. Econ. Entomol. 105, 1115-1129 (2012).
7. Ankersmit, G.W. DDT-resistance in Plutella maculipennis (Curt.) (Lep.) in Java. Bull. Entomol. Res. 44, 421-425 (1953).
8. Heckel, D.G., Gahan, L.J., Liu, Y.B. & Tabashnik, B.E. Genetic mapping of resistance to Bacillus thuringiensis toxins in diamondback moth using biphasic linkage analysis. Proc. Natl. Acad. Sci. USA 96, 8373-8377 (1999).
9. Tabashnik, B.E. et al. Efficacy of genetically modified Bt toxins against insects with different genetic mechanisms of resistance. Nat. Biotechnol. 29, 1128-1131 (2011).
10. Baxter, S.W. et al. Parallel evolution of Bacillus thuringiensis toxin resistance in Lepidoptera. Genetics 189, 675-679 (2011).
11. He, W. et al. Developmental and insecticide-resistant insights from the de novo assembled transcriptome of the diamondback moth, Plutella xylostella. Genomics 99, 169-177 (2012).
12. Baxter, S.W. et al. Mis-spliced transcripts of nicotinic acetylcholine receptor α6 are associated with field evolved spinosad resistance in Plutella xylostella (L.). PLoS Genet. 6, e1000802 (2010).
13. Xia, Q. et al. A draft sequence for the genome of the domesticated silkworm (Bombyx mori). Science 306, 1937-1940 (2004).
14. Zhan, S., Merlin, C., Boore, J.L. & Reppert, S.M. The monarch butterfly genome yields insights into long-distance migration. Cell 147, 1171-1185 (2011).
15. Zimmer, A. et al. Dating the early evolution of plants: detection and molecular clock analyses of orthologs. Mol. Genet. Genomics 278, 393-402 (2007).
16. Wang, X. et al. The genome of the mesopolyploid crop species Brassica rapa. Nat. Genet. 43, 1035-1039 (2011).
17. Baxter, S.W. et al. Linkage mapping and comparative genomics using next-generation RAD sequencing of a non-model organism. PLoS ONE 6, e19315 (2011).
18. Heliconius Genome Consortium. Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature 487, 94-98 (2012).
19. Mutanen, M., Wahlberg, N. & Kaila, L. Comprehensive gene and taxon coverage elucidates radiation patterns in moths and butterflies. Proc. R. Soc. 277, 2839-2848 (2010).
20. Regier, J.C. et al. Toward reconstructing the evolution of advanced moths and butterflies (Lepidoptera: Ditrysia): an initial molecular study. BMC Evol. Biol. 9, 280 (2009).
21. Buono, M. & Cosma, M.P. Sulfatase activities towards the regulation of cell metabolism and signaling in mammals. Cell. Mol. Life Sci. 67, 769-780 (2010).
22. Cosma, M.P. et al. The multiple sulfatase deficiency gene encodes an essential and limiting factor for the activity of sulfatases. Cell 113, 445-456 (2003).
23. Rausch, T. & Wachter, A. Sulfur metabolism: a versatile platform for launching defence operations. Trends Plant Sci. 10, 503-509 (2005).
24. Pauchet, Y., Muck, A., Svatos, A., Heckel, D.G. & Preiss, S. Mapping the larval midgut lumen proteome of Helicoverpa armigera, a generalist herbivorous insect. J. Proteome Res. 7, 1629-1639 (2008).
25. Henniges-Janssen, K., Reineke, A., Heckel, D.G. & Groot, A.T. Complex inheritance of larval adaptation in Plutella xylostella to a novel host plant. Heredity 107, 421-432 (2011).
26. Eichenseer, H., Mathews, M.C., Powell, J.S. & Felton, G.W. Survey of a salivary effector in caterpillars: glucose oxidase variation and correlation with host range. J. Chem. Ecol. 36, 885-897 (2010).
27. Wanner, K.W. & Robertson, H.M. The gustatory receptor family in the silkworm moth Bombyx mori is characterized by a large expansion of a single lineage of putative bitter receptors. Insect Mol. Biol. 17, 621-629 (2008).
28. Tao, X.-Y., Xue, X.-Y., Huang, Y.-P., Chen, X.-Y. & Mao, Y.-B. Gossypol-enhancedP450 gene pool contributes to cotton bollworm tolerance to a pyrethroid insecticide. Mol. Ecol. 21, 4371-4385 (2012).
29. Li, X., Schuler, M.A. & Berenbaum, M.R. Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu. Rev. Entomol. 52, 231-253 (2007).
30. Labbé, R., Caveney, S. & Donly, C. Genetic analysis of the xenobiotic resistance-associated ABC gene subfamilies of the Lepidoptera. Insect Mol. Biol. 20, 243-256 (2011).
31. Cui, F. et al. Two single mutations commonly cause qualitative change of nonspecific carboxylesterases in insects. Insect Biochem. Mol. Biol. 41, 1-8 (2011).
32. Chen, S. & Li, X. Transposable elements are enriched within or in close proximity to xenobiotic-metabolizing cytochrome P450 genes. BMC Evol. Biol. 7, 46 (2007).
33. Hu, T.T. et al. The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nat. Genet. 43, 476-481 (2011).
34. Kvist, J. et al. Temperature treatments during larval development reveal extensive heritable and plastic variation in gene expression and life history traits. Mol. Ecol. published online; doi:10.1111/j.1365-294X.2012.05521.x (19 March 2012).
35. Li, R. et al. SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25, 1966-1967 (2009).
36. Li, R. et al. The sequence and de novo assembly of the giant panda genome. Nature 463, 311-317 (2010).
37. Xu, X. et al. Genome sequence and analysis of the tuber crop potato. Nature 475, 189-195 (2011).
38. Boetzer, M., Henkel, C.V., Jansen, H.J., Butler, D. & Pirovano, W. Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 27, 578-579 (2011).
39. Kiełbasa, S.M., Wan, R., Sato, K., Horton, P. & Frith, M.C. Adaptive seeds tame genomic sequence comparison. Genome Res. 21, 487-493 (2011).
40. Mortazavi, A., Williams, B.A., McCue, K., Schaeffer, L. & Wold, B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 5, 621-628 (2008).
41. Stanke, M. & Morgenstern, B. AUGUSTUS: a web server for gene prediction in eukaryotes that allows user-defined constraints. Nucleic Acids Res. 33, W465-W467 (2005).
42. Burge, C. & Karlin, S. Prediction of complete gene structures in human genomic DNA. J. Mol. Biol. 268, 78-94 (1997).
43. Korf, I. Gene finding in novel genomes. BMC Bioinformatics 5, 59 (2004).
44. Birney, E., Clamp, M. & Durbin, R. GeneWise and Genomewise. Genome Res. 14, 988-995 (2004).
45. Elsik, C.G. et al. Creating a honey bee consensus gene set. Genome Biol. 8, R13 (2007).
46. Trapnell, C., Pachter, L. & Salzberg, S.L. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105-1111 (2009).
47. Trapnell, C. et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28, 511-515 (2010).
48. Hunter, S. et al. InterPro: the integrative protein signature database. Nucleic Acids Res. 37, D211-D215 (2009).
49. Pillai, S. et al. SOAP-based services provided by the European Bioinformatics Institute. Nucleic Acids Res. 33, W25-W28 (2005).
50. Ogata, H. et al. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res. 27, 29-34 (1999).
51. Apweiler, R. et al. UniProt: the universal protein knowledgebase. Nucleic Acids Res. 32, D115-D119 (2004).
52. Jurka, J. et al. Repbase Update, a database of eukaryotic repetitive elements. Cytogenet. Genome Res. 110, 462-467 (2005).
53. Price, A.L., Jones, N.C. & Pevzner, P.A. De novo identification of repeat families in large genomes. Bioinformatics 21, i351-i358 (2005).
54. Edgar, R.C. & Myers, E.W. PILER: identification and classification of genomic repeats. Bioinformatics 21, i152-i158 (2005).
55. Xu, Z. & Wang, H. LTR-FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Res. 35, W265-W268 (2007).
56. Benson, G. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 27, 573-580 (1999).
57. McCarthy, E.M. & McDonald, J.F. LTR-STRUC: a novel search and identification program for LTR retrotransposons. Bioinformatics 19, 362-367 (2003).
58. Edgar, R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797 (2004).
59. Rice, P., Longden, I. & Bleasby, A. EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet. 16, 276-277 (2000).
60. Lowe, T.M. & Eddy, S.R. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25, 955-964 (1997).
61. Wuyts, J., Perrière, G. & Van de Peer, Y. The European ribosomal RNA database. Nucleic Acids Res. 32, D101-D103 (2004).
62. Griffiths-Jones, S., Bateman, A., Marshall, M., Khanna, A. & Eddy, S.R. Rfam: an RNA family database. Nucleic Acids Res. 31, 439-441 (2003).
63. Nawrocki, E.P., Kolbe, D.L. & Eddy, S.R. Infernal 1.0: inference of RNA alignments. Bioinformatics 25, 1335-1337 (2009).
64. Adams, M.D. et al. The genome sequence of Drosophila melanogaster. Science 287, 2185-2195 (2000).
65. Holt, R.A. et al. The genome sequence of the malaria mosquito Anopheles gambiae. Science 298, 129-149 (2002).
66. Richards, S. et al. The genome of the model beetle and pest Tribolium castaneum. Nature 452, 949-955 (2008).
67. Werren, J.H. et al. Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 327, 343-348 (2010).
68. HoneyBee Genome Sequencing Consortium. . Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443, 931-949 (2006).
69. Bonasio, R. et al. Genomic comparison of the ants Camponotus floridanus and Harpegnathos saltator. Science 329, 1068-1071 (2010).
70. Kirkness, E.F. et al. Genome sequences of the human body louse and its primary endosymbiont provide insights into the permanent parasitic lifestyle. Proc. Natl. Acad. Sci. USA 107, 12168-12173 (2010).
71. International Aphid Genomics Consortium. Genome sequence of the pea aphid Acyrthosiphon pisum. PLoS Biol. 8, e1000313 (2010).
72. Grbić, M. et al. The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature 479, 487-492 (2011).
73. Li, H. et al. TreeFam: a curated database of phylogenetic trees of animal gene families. Nucleic Acids Res. 34, D572-D580 (2006).
74. Yang, Z. PAML 4: Phylogenetic Analysis by Maximum Likelihood. Mol. Biol. Evol. 24, 1586-1591 (2007).
75. Lunter, G. & Goodson, M. Stampy: a statistical algorithm for sensitive and fast mapping of Illumina sequence reads. Genome Res. 21, 936-939 (2011).
76. McKenna, A. et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297-1303 (2010).
77. Ooijen, V.A.N.J. Multipoint maximum likelihood mapping in a full-sib family of an outbreeding species. Genet. Res. 93, 343-349 (2011).
78. Tang, H. et al. Synteny and collinearity in plant genomes. Science 320, 486-488 (2008).
79. Li, R. et al. SNP detection for massively parallel whole-genome resequencing. Genome Res. 19, 1124-1132 (2009).
80. Li, R., Li, Y., Kristiansen, K. & Wang, J. SOAP: short oligonucleotide alignment program. Bioinformatics 24, 713-714 (2008).
81. Quevillon, E. et al. InterProScan: protein domains identifier. Nucleic Acids Res. 33, W116-W120 (2005).
82. Marchler-Bauer, A. et al. CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res. 39, D225-D229 (2011).
83. Kent, W.J. BLAT-The BLAST-Like Alignment Tool. Genome Res. 12, 656-664 (2002).
84. Li, A., Yang, Y., Wu, S., Li, C. & Wu, Y. Investigation of resistance mechanisms to fipronil in diamondback moth (Lepidoptera: Plutellidae). J. Econ. Entomol. 99, 914-919 (2006).
85. Livak, K.J. & Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25, 402-408 (2001).