期刊论文详细信息
BMC Genomics
Transcriptomic analyses reveal the adaptive features and biological differences of guts from two invasive whitefly species
Xiao-Wei Wang1  Shu-Sheng Liu1  Wen-Qiang Xia1  Qiong-Yi Zhao2  Yun-Lin Su1  Xiao-Dong Ye1 
[1] Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences, Zhejiang University, 866 Yuhangtang Road, Hangzhou 310058, China;The University of Queensland, Queensland Brain Institute, Brisbane Qld 4072, Australia
关键词: Whitefly;    Transcriptome;    Gut;    Genetic divergence;    Gene expression;   
Others  :  1217231
DOI  :  10.1186/1471-2164-15-370
 received in 2014-01-01, accepted in 2014-05-07,  发布年份 2014
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【 摘 要 】

Background

The gut of phloem feeding insects is critical for nutrition uptake and xenobiotics degradation. However, partly due to its tiny size, genomic information for the gut of phloem feeding insects is limited.

Results

In this study, the gut transcriptomes of two species of invasive whiteflies in the Bemisia tabaci complex, Middle East Asia Minor 1 (MEAM1) and Mediterranean (MED), were analyzed using the Illumina sequencing. A total of 12,879 MEAM1 transcripts and 11,246 MED transcripts were annotated with a significant Blastx hit. In addition, 7,000 and 5,771 gut specific genes were respectively identified for MEAM1 and MED. Functional analyses on these gut specific genes demonstrated the important roles of gut in metabolism of insecticides and secondary plant chemicals. To reveal the molecular difference between guts of MEAM1 and MED, a comparison between gut transcriptomes of the two species was conducted and 3,910 pairs of orthologous genes were identified. Based on the ratio of nonsynonymous and synonymous substitutions, 15 genes were found evolving under positive selection. Many of those genes are predicted to be involved in metabolism and insecticide resistance. Furthermore, many genes related to detoxification were expressed at an elevated level in the gut of MED compared to MEAM1, which might be responsible for the MED’s higher resistance to insecticides and environmental stresses.

Conclusion

The sequencing of MED and MEAM1 gut transcriptomes and extensive comparisons of MEAM1 and MED gut transcripts provide substantial sequence information for revealing the role of gut in whiteflies.

【 授权许可】

   
2014 Ye et al.; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Ziegler H: Nature of transported substances. In Transport in Plants I. Volume 1. Edited by Zimmermann MH, Milburn JA. Berlin Heidelberg: Springer; 1975::59-100.
  • [2]Douglas AE: The nutritional physiology of aphids. Adv Insect Physiol 2013, 31:73-140.
  • [3]Terra WR: Evolution of digestive systems of insects. Annu Rev of Entomol 1990, 35:181-200.
  • [4]Cristofoletti PT, Ribeiro AF, Deraison C, Rahbe Y, Terra WR: Midgut adaptation and digestive enzyme distribution in a phloem feeding insect, the pea aphid Acyrthosiphon pisum. J Insect Physiol 2003, 49:11-24.
  • [5]Douglas AE: Phloem-sap feeding by animals: problems and solutions. J Exp Bot 2006, 57:747-754.
  • [6]Walz C, Giavalisco P, Schad M, Juenger M, Klose J, Kehr J: Proteomics of curcurbit phloem exudate reveals a network of defence proteins. Phytochemistry 2004, 65:1795-1804.
  • [7]Parde VD, Sharma HC, Kachole MS: In vivo inhibition of Helicoverpa armigera gut pro-proteinase activation by non-host plant protease inhibitors. J Insect Physiol 2010, 56:1315-1324.
  • [8]Bolter C, Jongsma MA: The adaptation of insects to plant protease inhibitors. J Insect Physiol 1997, 43:885-895.
  • [9]Broadway RM, Duffey SS: Plant proteinase inhibitors: Mechanism of action and effect on the growth and digestive physiology of larval Heliothis zea and Spodoptera exiqua. J Insect Physiol 1986, 32:827-833.
  • [10]Matthews HJ, Down RE, Audsley N: Effects of Manduca sexta allatostatin and an analogue on the peach-potato aphid Myzus persicae (hemiptera: aphididae) and degradation by enzymes in the aphid gut. Arch Insect Biochem Physiol 2010, 75:139-157.
  • [11]Candas M, Loseva O, Oppert B, Kosaraju P, Bulla LA Jr: Insect resistance to Bacillus thuringiensis: alterations in the indianmeal moth larval gut proteome. Mol Cell Proteomics 2003, 2:19-28.
  • [12]Down RE, Matthews HJ, Audsley N: Oral activity of FMRFamide-related peptides on the pea aphid Acyrthosiphon pisum (Hemiptera: Aphididae) and degradation by enzymes from the aphid gut. Regul Pept 2011, 171:11-18.
  • [13]Ranson H, Claudianos C, Ortelli F, Abgrall C, Hemingway J, Sharakhova MV, Unger MF, Collins FH, Feyereisen R: Evolution of supergene families associated with insecticide resistance. Science 2002, 298:179-181.
  • [14]Jones RT, Bakker SE, Stone D, Shuttleworth SN, Boundy S, McCart C, Daborn PJ, ffrench-Constant RH, van den Elsen JM: Homology modelling of Drosophila cytochrome P450 enzymes associated with insecticide resistance. Pest Manag Sci 2010, 66:1106-1115.
  • [15]Puinean AM, Foster SP, Oliphant L, Denholm I, Field LM, Millar NS, Williamson MS, Bass C: Amplification of a cytochrome P450 gene is associated with resistance to neonicotinoid insecticides in the aphid Myzus persicae. PLoS Genet 2010, 6:e1000999.
  • [16]Enayati AA, Ranson H, Hemingway J: Insect glutathione transferases and insecticide resistance. Insect Mol Biol 2005, 14:3-8.
  • [17]Despres L, David JP, Gallet C: The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol Evol 2007, 22:298-307.
  • [18]Yan L, Yang P, Jiang F, Cui N, Ma E, Qiao C, Cui F: Transcriptomic and phylogenetic analysis of Culex pipiens quinquefasciatus for three detoxification gene families. BMC Genomics 2012, 13:609. BioMed Central Full Text
  • [19]Jiu M, Zhou XP, Tong L, Xu J, Yang X, Wan FH, Liu SS: Vector-Virus mutualism accelerates population Increase of an invasive whitefly. PLoS One 2007, 2:e182.
  • [20]Crowder DW, Horowitz AR, De Barro PJ, Liu SS, Showalter AM, Kontsedalov S, Khasdan V, Shargal A, Liu J, Carriere Y: Mating behaviour, life history and adaptation to insecticides determine species exclusion between whiteflies. J Anim Ecol 2010, 79:563-570.
  • [21]Gorman K, Slater R, Blande JD, Clarke A, Wren J, McCaffery A, Denholm I: Cross-resistance relationships between neonicotinoids and pymetrozine in Bemisia tabaci (Hemiptera: Aleyrodidae). Pest Manag Sci 2010, 66:1186-1190.
  • [22]Ghanim M, Morin S, Czosnek H: Rate of Tomato yellow leaf curl virus translocation in the circulative transmission pathway of its vector, the whitefly Bemisia tabaci. Phytopathology 2001, 91:188-196.
  • [23]Bing XL, Yang J, Zchori-Fein E, Wang XW, Liu SS: Characterization of a newly discovered symbiont of the whitefly Bemisia tabaci (Hemiptera: Aleyrodidae). Appl Environ Microbiol 2013, 79:569-575.
  • [24]De Barro PJ, Liu SS, Boykin LM, Dinsdale AB: Bemisia tabaci: A statement of species status. Ann Rev Entomol 2011, 56:1-19.
  • [25]Dinsdale A, Cook L, Riginos C, Buckley YM, De Barro P: Refined global analysis of Bemisia tabaci (Hemiptera: Sternorrhyncha: Aleyrodoidea: Aleyrodidae) mitochondrial cytochrome oxidase 1 toidentify species level genetic boundaries. Ann Enomol Soc Am 2010, 103:196-208.
  • [26]Boykin LM, Shatters RG, Rosell RC, McKenzie CL, Bagnall RA, De Barro P, Frohlich DR: Global relationships of Bemisia tabaci (Hemiptera: Aleyrodidae) revealed using Bayesian analysis of mitochondrial COI DNA sequences. Mol Phylogenet Evol 2007, 44:1306-1319.
  • [27]Hu J, De Barro P, Zhao H, Wang J, Nardi F, Liu SS: An extensivefield survey combined with a phylogenetic analysis reveals rapid and widespread invasion of two alien whiteflies in China. PLoS One 2011, 6:e16061.
  • [28]Firdaus S, Vosman B, Hidayati N, Supena J, Darmo E, Visser RGF, van Heusden AW: The Bemisia tabaci species complex: Additions from different parts of the world. Insect Sci 2013, 6:723-733.
  • [29]Hogenhout SA, Ammar ED, Whitfield AE, Redinbaugh MG: Insect vector interactions with persistently transmitted viruses. Annu Rev Phytopathol 2008, 46:327-359.
  • [30]Chu D, Zhang YJ, Brown JK, Cong B, Xu BY, Wu QJ, Zhu GR: The introduction of the exotic Q biotype of Bemisia tabaci from the Mediterranean region into China on ornamental crops. Florida Entomologist 2006, 89:168-174.
  • [31]Chu D, Wan FH, Zhang YJ, Brown JK: Change in the biotype composition of Bemisia tabaci in Shandong Province of China from 2005 to 2008. Environ Entomol 2010, 39:1028-1036.
  • [32]Pan H, Chu D, Ge D, Wang S, Wu Q, Xie W, Jiao X, Liu B, Yang X, Yang N, Su Q, Xu B, Zhang Y: Further spread of and domination by Bemisia tabaci (Hemiptera: Aleyrodidae) biotype Q on field crops in China. J Econ Entomol 2011, 104:978-985.
  • [33]Sun DB, Liu YQ, Qin L, Xu J, Li FF, Liu SS: Competitive displacement between two invasive whiteflies: insecticide application and host plant effects. Bull Entomol Res 2013, 103:344-353.
  • [34]Wang XW, Zhao QY, Luan JB, Wang YJ, Yan GH, Liu SS: Analysis of a native whitefly transcriptome and its sequence divergence with two invasive whitefly species. BMC Genomics 2012, 13:529. BioMed Central Full Text
  • [35]Horowitz AR, Denholm I, Gorman K, Cenis JL, Kontsedalov S, Ishaaya I: Biotype Q of Bemisia tabaci identified in Israel. Phytoparasitica 2003, 31:94-98.
  • [36]Fernandez E, Gravalos C, Haro PJ, Cifuentes D, Bielza P: Insecticide resistance status of Bemisia tabaci Q-biotype in south-eastern Spain. Pest Manag Sci 2009, 65:885-891.
  • [37]Wang XW, Luan JB, Li JM, Su YL, Xia J, Liu SS: Transcriptome analysis and comparison reveal divergence between two invasive whitefly cryptic species. BMC Genomics 2011, 12:458. BioMed Central Full Text
  • [38]Su YL, Li JM, Li M, Luan JB, Ye XD, Wang XW, Liu SS: Transcriptomic analysis of the salivary glands of an invasive whitefly. PLoS One 2012, 7:e39303.
  • [39]Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, Palma F, Birren B, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A: Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 2011, 29:644-652.
  • [40]Mao X, Cai T, Olyarchuk JG, Wei L: Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 2005, 21:3787-3793.
  • [41]Fukushima A, Kusano M, Redestig H, Arita M, Saito K: Metabolomic correlation-network modules in Arabidopsis based on a graph-clustering approach. BMC Syst Biol 2011, 5:1. BioMed Central Full Text
  • [42]Lehane MJ, Blakemore D, Williams S, Moffatt MR: Regulation of digestive enzyme levels in insects. Comp Biochem Physiol B Biochem Mol Biol 1995, 110:285-289.
  • [43]Naikkhwah W, O'Donnell MJ: Phenotypic plasticity in response to dietary salt stress: Na + and K + transport by the gut of Drosophila melanogaster larvae. J Exp Biol 2012, 215:461-470.
  • [44]Yuan L, Wang S, Zhou J, Du Y, Zhang Y, Wang J: Status of insecticide resistance and associated mutations in Q-biotype of whitefly, Bemisia tabaci, from eastern China. Crop Prot 2012, 31:67-71.
  • [45]Ghanim M, Kontsedalov S: Gene expression in pyriproxyfen-resistant Bemisia tabaci Q biotype. Pest Manag Sci 2007, 63:776-783.
  • [46]Horowitz AR, Kontsedalov S, Khasdan V, Ishaaya I: Biotypes B and Q of Bemisia tabaci and their relevance to neonicotinoid and pyriproxyfen resistance. Arch Insect Biochem 2005, 58:216-225.
  • [47]Nauen R, Stumpf N, Elbert A: Toxicological and mechanistic studies on neonicotinoid cross resistance in Q-type Bemisia tabaci (Hemiptera: Aleyrodidae). Pest Manag Sci 2002, 58:868-875.
  • [48]Li L, Stoeckert CJ Jr, Roos DS: OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 2003, 13:2178-2189.
  • [49]Wang XW, Luan JB, Li JM, Bao YY, Zhang CX, Liu SS: De novo characterization of a whitefly transcriptome and analysis of its gene expression during development. BMC Genomics 2010, 11:400. BioMed Central Full Text
  • [50]Elmer KR, Fan S, Gunter HM, Jones JC, Boekhoff S, Kuraku S, Meyer A: Rapid evolution and selection inferred from the transcriptomes of sympatric crater lake cichlid fishes. Mol Ecol 2010, 19(Suppl 1):197-211.
  • [51]Osada N, Hashimoto K, Kameoka Y, Hirata M, Tanuma R, Uno Y, Inoue I, Hida M, Suzuki Y, Sugano S, Terao K, Kusuda J, Takahashi I: Large-scale analysis of Macaca fascicularis transcripts and inference of genetic divergence between M. fascicularis and M. mulatta. BMC Genomics 2008, 9:90. BioMed Central Full Text
  • [52]Swanson WJ, Yang Z, Wolfner MF, Aquadro CF: Positive Darwinian selection drives the evolution of several female reproductive proteins in mammals. Proc Natl Acad Sci U S A 2001, 98:2509-2514.
  • [53]Li JM, Su YL, Gao XL, He J, Liu SS, Wang XW: Molecular characterization and oxidative stress response of an intracellular Cu/Zn superoxide dismutase (CuZnSOD) of the whitefly, Bemisia tabaci. Arch Insect Biochem Physiol 2011, 77:118-133.
  • [54]Yin Y, Martin J, Abubucker S, Scott AL, McCarter JP, Wilson RK, Jasmer DP, Mitreva M: Intestinal transcriptomes of nematodes: comparison of the parasites Ascaris suum and Haemonchus contortus with the free-living Caenorhabditis elegans. PLoS Negl Trop Dis 2008, 2:e269.
  • [55]Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402.
  • [56]Yang Z, Nielsen R: Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol 2000, 17:32-43.
  • [57]Zhang Z, Li J, Zhao XQ, Wang J, Wong GK, Yu J: KaKs_Calculator: calculating Ka and Ks through model selection and model averaging. Genomics Proteomics Bioinformatics 2006, 4:259-263.
  • [58]Audic S, Claverie JM: The significance of digital gene expression profiles. Genome Res 1997, 7:986-995.
  • [59]Benjamini Y, Yekutieli D: The control of the false discovery rate in multiple testing under dependency. Ann Stat 2001, 29:1165-1188.
  • [60]Livak KJ, Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method. Methods 2001, 25:402-408.
  • [61]Su Y, He WB, Wang J, Li JM, Liu SS, Wang XW: Selection of endogenous reference genes for gene expression analysis in the Mediterranean species of the Bemisia tabaci (Hemiptera: Aleyrodidae) complex. J Econ Entomol 2013, 106:1446-1455.
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