De Novo Transcriptome Sequencing of the Snail Echinolittorina malaccana: Identification of Genes Responsive to Thermal Stress and Development of Genetic Markers for Population Studies
详细信息 查看全文
- 作者：Wei Wang ; Jerome H. L. Hui ; Ting Fung Chan ; Ka Hou Chu
- 关键词：Littorinidae ; Transcriptome ; Thermal stress ; Gene expression ; Population genetics ; Climate change
- 刊名：Marine Biotechnology
- 出版年：2014
- 出版时间：October 2014
- 年：2014
- 卷：16
- 期：5
- 页码：547-559
- 全文大小：889 KB
- 参考文献：1. Amaral PP, Dinger ME, Mattick JS (2013) Non-coding RNAs in homeostasis, disease and stress responses: an evolutionary perspective. Brief Funct Genomics 12:254-78 CrossRef
2. Basirico L, Morera P, Primi V, Lacetera N, Nardone A, Bernabucci U (2011) Cellular thermotolerance is associated with heat shock protein 70.1 genetic polymorphisms in Holstein lactating cows. Cell Stress Chaperones 16:441-48 CrossRef
3. Boutet I, Tanguy A, Le Guen D, Piccino P, Hourdez S, Legendre P, Jollivet D (2009) Global depression in gene expression as a response to rapid thermal changes in vent mussels. Proc Biol Sci 276:3071-079 CrossRef
4. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674-676 CrossRef
5. Dunphy BJ, Ragg NL, Collings MG (2013) Latitudinal comparison of thermotolerance and HSP70 production in F2 larvae of the greenshell mussel ( / Perna canaliculus). J Exp Biol 216:1202-209 CrossRef
6. Evans TG, Hofmann GE (2012) Defining the limits of physiological plasticity: how gene expression can assess and predict the consequences of ocean change. Phil Trans R Soc B 367:1733-745 CrossRef
7. Feder ME, Walser JC (2005) The biological limitations of transcriptomics in elucidating stress and stress responses. J Evol Biol 18:901-10 CrossRef
8. Franks SJ, Hoffmann AA (2012) Genetics of climate change adaptation. Annu Rev Genet 46:185-08 CrossRef
9. Fu N, Wang Q, Shen HL (2013) / De novo assembly, gene annotation and marker development using Illumina paired-end transcriptome sequences in celery ( / Apium graveolens L.). PLoS One 8:e57686 CrossRef
10. Galindo J, Moran P, Rolan-Alvarez E (2009) Comparing geographical genetic differentiation between candidate and noncandidate loci for adaptation strengthens support for parallel ecological divergence in the marine snail / Littorina saxatilis. Mol Ecol 18:919-30 CrossRef
11. 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, Di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644-52 CrossRef
12. Gracey AY, Chaney ML, Boomhower JP, Tyburczy WR, Connor K, Somero GN (2008) Rhythms of gene expression in a fluctuating intertidal environment. Curr Biol 18:1501-507 CrossRef
13. Hammond LM, Hofmann GE (2010) Thermal tolerance of / Strongylocentrotus purpuratus early life history stages: mortality, stress-induced gene expression and biogeographic patterns. Mar Biol 157:2677-687 CrossRef
14. Helmuth B, Harley CD, Halpin PM, O’donnell M, Hofmann GE, Blanchette CA (2002) Climate change and latitudinal patterns of intertidal thermal stress. Science 298:1015-017 CrossRef
15. Henderson B (2010) Integrating the cell stress response: a new view of molecular chaperones as immunological and physiological homeostatic regulators. Cell Biochem Funct 28:1-4 CrossRef
16. Hofmann GE, Todgham AE (2010) Living in the now: physiological mechanisms to tolerate a rapidly changing environment. Annu Rev Physiol 72:127-45 CrossRef
17. Hollenbeck CM, Portnoy DS, Gold JR (2012) Use of comparative genomics to develop EST-SSRs for red drum ( / Sciaenops ocellatus). Mar Biotechnol (NY) 14:672-80 CrossRef
18. Iseli C, Jongeneel CV, Bucher P (1999) ESTScan: a program for detecting, evaluating, and reconstructing potential coding regions in EST sequences. Proc Int Conf Intell Syst Mol Biol :138-48
19. Ivanina AV, Taylor C, Sokolova IM (2009) Effects of elevated temperature and cadmium exposure on stress protein response in eastern oysters / Crassostrea virginica (Gmelin). Aquat Toxicol 91:245-54 CrossRef
20. Kultz D (2005) Molecular and evolutionary basis of the cellular stress response. Annu Rev Physiol 67:225-57 CrossRef
21. Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357-59 CrossRef
22. Leung AK, Sharp PA (2010) MicroRNA functions in stress responses. Mol Cell 40:205-15 CrossRef
23. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Genome Project Data Processing S (2009) The sequence alignment/map format and SAM tools. Bioinformatics 25:2078-079 CrossRef
24. Liu WG, Huang XD, Lin JS, He MX (2012) Seawater acidification and elevated temperature affect gene expression patterns of the pearl oyster / Pinctada fucata. PLoS One 7:e33679 CrossRef
25. Liu S, Wang X, Sun F, Zhang J, Feng J, Liu H, Rajendran KV, Sun L, Zhang Y, Jiang Y, Peatman E, Kaltenboeck L, Kucuktas H, Liu Z (2013) RNA-Seq reveals expression signatures of genes involved in oxygen transport, protein synthesis, folding, and degradation in response to heat stress in catfish. Physiol Genomics 45:462-76 CrossRef
26. Lockwood BL, Somero GN (2012) Functional determinants of temperature adaptation in enzymes of cold- versus warm-adapted mussels (Genus / Mytilus). Mol Biol Evol 29:3061-070 CrossRef
27. Lockwood BL, Sanders JG, Somero GN (2010) Transcriptomic responses to heat stress in invasive and native blue mussels (genus / Mytilus): molecular correlates of invasive success. J Exp Biol 213:3548-558 CrossRef
28. Maron BJ (2002) Hypertrophic cardiomyopathy: a systematic review. JAMA 287:1308-320
29. Marshall DJ, McQuaid CD (2011) Warming reduces metabolic rate in marine snails: adaptation to fluctuating high temperatures challenges the metabolic theory of ecology. Proc Biol Sci 278:281-88 CrossRef
30. Marshall DJ, Dong YW, McQuaid CD, Williams GA (2011) Thermal adaptation in the intertidal snail / Echinolittorina malaccana contradicts current theory by revealing the crucial roles of resting metabolism. J Exp Biol 214:3649-657 CrossRef
31. Martinez-Fernandez M, Bernatchez L, Rolan-Alvarez E, Quesada H (2010) Insights into the role of differential gene expression on the ecological adaptation of the snail / Littorina saxatilis. BMC Evol Biol 10:356 CrossRef
32. Micallef G, Bickerdike R, Reiff C, Fernandes JMO, Bowman AS, Martin SM (2012) Exploring the transcriptome of Atlantic salmon ( / Salmo salar) skin, a major defense organ. Mar Biotechnol (NY) 14:559-69 CrossRef
33. Mutz KO, Heilkenbrinker A, Lonne M, Walter JG, Stahl F (2013) Transcriptome analysis using next-generation sequencing. Curr Opin Biotechnol 24:22-0 CrossRef
34. Negri A, Oliveri C, Sforzini S, Mignione F, Viarengo A, Banni M (2013) Transcriptional response of the mussel Mytilus galloprovincialis (Lam.) following exposure to heat stress and copper. PLoS One 8:e66802 CrossRef
35. Nezis IP, Simonsen A, Sagona AP, Finley K, Gaumer S, Contamine D, Rusten TE, Stenmark H, Brech A (2008) Ref(2)P, the Drosophila melanogaster homologue of mammalian p62, is required for the formation of protein aggregates in adult brain. J Cell Biol 180:1065-071 CrossRef
36. Parsell DA, Lindquist S (1993) The function of heat-shock proteins in stress tolerance—degradation and reactivation of damaged proteins. Annu Rev Genet 27:437-96 CrossRef
37. Pertea G, Huang X, Liang F, Antonescu V, Sultana R, Karamycheva S, Lee Y, White J, Cheung F, Parvizi B, Tsai J, Quackenbush J (2003) TIGR gene indices clustering tools (TGICL): a software system for fast clustering of large EST datasets. Bioinformatics 19:651-52 CrossRef
38. Podrabsky JE, Somero GN (2004) Changes in gene expression associated with acclimation to constant temperatures and fluctuating daily temperatures in an annual killifish / Austrofundulus limnaeus. J Exp Biol 207:2237-254 CrossRef
39. Portner HO (2010) Oxygen- and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems. J Exp Biol 213:881-93 CrossRef
40. Posner M, Kiss AJ, Skiba J, Drossman A, Dolinska MB, Hejtmancik JF, Sergeev YV (2012) Functional validation of hydrophobic adaptation to physiological temperature in the small heat shock protein αA-crystallin. PLoS One 7:e34438 CrossRef
41. Rebl A, Verleih M, Kobis JM, Kuhn C, Wimmers K, Kollner B, Goldammer T (2013) Transcriptome profiling of gill tissue in regionally bred and globally farmed rainbow trout strains reveals different strategies for coping with thermal stress. Mar Biotechnol (NY) 15:445-60 CrossRef
42. Reid DG, Lal K, Mackenzie-Dodds J, Kaligis F, Littlewood DTJ, Williams ST (2006) Comparative phylogeography and species boundaries in / Echinolittorina snails in the central Indo-West Pacific. J Biogeogr 33:990-006 CrossRef
43. Richter K, Haslbeck M, Buchner J (2010) The heat shock response: life on the verge of death. Mol Cell 40:253-66 CrossRef
44. Robinson MD, Mccarthy DJ, Smyth GK (2010) edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139-40 CrossRef
45. Robinson N, Sahoo PK, Baranski M, Das Mahapatra K, Saha JN, Das S, Mishra Y, Das P, Barman HK, Eknath AE (2012) Expressed sequences and polymorphisms in rohu carp ( / Labeo rohita, Hamilton) revealed by mRNA-seq. Mar Biotechnol (NY) 14:620-33 CrossRef
46. Ronges D, Walsh JP, Sinclair BJ, Stillman JH (2012) Changes in extreme cold tolerance, membrane composition and cardiac transcriptome during the first day of thermal acclimation in the porcelain crab / Petrolisthes cinctipes. J Exp Biol 215:1824-836 CrossRef
47. Runcie DE, Garfield DA, Babbitt CC, Wygoda JA, Mukherjee S, Wray GA (2012) Genetics of gene expression responses to temperature stress in a sea urchin gene network. Mol Ecol 21:4547-562 CrossRef
48. Sanford E, Kelly MW (2011) Local adaptation in marine invertebrates. Annu Rev Mar Sci 3:509-35 CrossRef
49. Schoville SD, Barreto FS, Moy GW, Wolff A, Burton RS (2012) Investigating the molecular basis of local adaptation to thermal stress: population differences in gene expression across the transcriptome of the copepod / Tigriopus californicus. BMC Evol Biol 12:170 CrossRef
50. Smith S, Bernatchez L, Beheregaray LB (2013) RNA-seq analysis reveals extensive transcriptional plasticity to temperature stress in a freshwater fish species. BMC Genomics 14:375 CrossRef
51. Somero GN (2010) The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners-and ‘losers- J Exp Biol 213:912-20 CrossRef
52. Sorensen JG, Nielsen MM, Kruhoffer M, Justesen J, Loeschcke V (2005) Full genome gene expression analysis of the heat stress response, in / Drosophila melanogaster. Cell Stress Chaperones 10:312-28 CrossRef
53. Stenseng E, Braby CE, Somero GN (2005) Evolutionary and acclimation-induced variation in the thermal limits of heart function in congeneric marine snails (genus / Tegula): implications for vertical zonation. Biol Bull 208:138-44 CrossRef
54. Stillman JH, Tagmount A (2009) Seasonal and latitudinal acclimatization of cardiac transcriptome responses to thermal stress in porcelain crabs, / Petrolisthes cinctipes. Mol Ecol 18:4206-226 CrossRef
55. Thiel T, Michalek W, Varshney RK, Graner A (2003) Exploiting EST databases for the development and characterization of gene-derived SSR-markers in barley ( / Hordeum vulgare L). Theor Appl Genet 106:411-22
56. Thomas JO, Travers AA (2001) HMG1 and 2, and related ‘architectural-DNA-binding proteins. Trends Biochem Sci 26:167-74 CrossRef
57. Tomanek L (2010) Variation in the heat shock response and its implication for predicting the effect of global climate change on species-biogeographical distribution ranges and metabolic costs. J Exp Biol 213:971-79 CrossRef
58. Truebano M, Burns G, Thorne MS, Hillyard G, Peck LS, Skibinski DOF, Clark MS (2010) Transcriptional response to heat stress in the Antarctic bivalve / Laternula elliptica. J Exp Mar Biol Ecol 391:65-2 CrossRef
59. Vandenkoornhuyse P, Dufresne A, Quaiser A, Gouesbet G, Binet F, Francez AJ, Mahe S, Bormans M, Lagadeuc Y, Couee I (2010) Integration of molecular functions at the ecosystemic level: breakthroughs and future goals of environmental genomics and post-genomics. Ecol Lett 13:776-91 CrossRef
60. Verghese J, Abrams J, Wang Y, Morano KA (2012) Biology of the heat shock response and protein chaperones: budding yeast ( / Saccharomyces cerevisiae) as a model system. Microbiol Mol Biol Rev 76:115-58 CrossRef
61. Walters RJ, Blanckenhorn WU, Berger D, Woods A (2012) Forecasting extinction risk of ectotherms under climate warming: an evolutionary perspective. Funct Ecol 26:1324-338 CrossRef
62. Wei Z, Wang W, Hu P, Lyon GJ, Hakonarson H (2011) SNVer: a statistical tool for variant calling in analysis of pooled or individual next-generation sequencing data. Nucleic Acids Res 39:e132 CrossRef
63. Werner GD, Gemmell P, Grosser S, Hamer R, Shimeld SM (2013) Analysis of a deep transcriptome from the mantle tissue of / Patella vulgata Linnaeus (Mollusca: Gastropoda: Patellidae) reveals candidate biomineralising genes. Mar Biotechnol (NY) 15:230-43 CrossRef
64. Whitehead A (2012) Comparative genomics in ecological physiology: toward a more nuanced understanding of acclimation and adaptation. J Exp Biol 215:884-91 CrossRef
65. Zuo W, Moses ME, West GB, Hou C, Brown JH (2012) A general model for effects of temperature on ectotherm ontogenetic growth and development. Proc Biol Sci 279:1840-846 CrossRef - 作者单位：Wei Wang (1)
Jerome H. L. Hui (1)
Ting Fung Chan (1)
Ka Hou Chu (1)
1. School of Life Sciences, The Chinese University of Hong Kong, Shatin, Hong Kong - ISSN：1436-2236
文摘
Echinolittorina snails inhabit the upper intertidal rocky shore and face strong selection pressures from thermal extremes and fluctuations. Revealing the molecular processes of adaptive significance is greatly obstructed by the scarcity of genomic resource for these taxa. Here, we reported the first comprehensive transcriptome dataset for the genus Echinolittorina. Using Illumina HiSeq 2000 platform, about 52?M and 54?M paired-end clean reads were, respectively, generated for the control and heat-stressed libraries. Totally, 115,211 unique transcript fragments (unigenes) were assembled, with an average length of 453?bp and a N50 size of 492?bp. Approximately one third of the unigenes could be annotated according to their homology matches against the Nr, Swiss-Prot, COG, or KEGG databases, and they were found to represent 23,098 non-redundant genes. Gene expression comparison revealed that 1,267 and 6,663 annotated genes were, respectively, up- and downregulated with at least twofold changes upon heat stress. Gene Ontology and KEGG pathway analyses indicated that there were overrepresented amount of genes enriched in a broad spectrum of biological processes and pathways, including those associated with cytoskeleton organization, developmental regulation, signaling transduction, infection, and cardiac function. In addition, a transcriptome-wide search for polymorphic loci yielded a total of 11,228 simple sequence repeats (SSRs) from 9,938 unigenes and 138,631 single nucleotide polymorphism (SNP) and insertion/deletion (INDEL) sites among 22,770 unigenes. The large number of transcript sequences acquired, the biological pathways identified, and the candidate microsatellite and SNP/INDEL loci discovered in the study will serve as valuable resources for further investigations of genetic differentiation and thermal adaptation among populations.