Transcriptome analysis of Portunus trituberculatus in response to salinity stress provides insights into the molecular basis of osmoregulation

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Lv, Jianjian ^a   Liu, Ping ^a   Wang, Yu ^a,b   Gao, Baoquan ^a   Chen, Ping ^a   Li, Jian ^a  

^a YELLOW SEA FISHERIES RESEARCH INSTITUTE   (China)

^b SHANGHAI OCEAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CHITIN; TRANSCRIPTOME;

AMINO ACID METABOLISM; ARTICLE; BIOINFORMATICS; CARBOHYDRATE METABOLISM; CONTROLLED STUDY; DNA LIBRARY; DNA SEQUENCE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENE ONTOLOGY; GENETIC ANALYZER; GENETIC PROCEDURES; GENOME ANALYSIS; GENOMICS; ION TRANSPORT; NEXT GENERATION SEQUENCING TECHNIQUE; NONHUMAN; OSMOREGULATION; PORTUNUS TRITUBERCULATUS; PROTEIN DEGRADATION; QUALITATIVE RESEARCH; RNA ANALYSIS; SALT STRESS; SALT TOLERANCE; TRANSCRIPTOMICS;

ANIMALS; BRACHYURA; GENE EXPRESSION PROFILING; GENE ONTOLOGY; MOLECULAR SEQUENCE ANNOTATION; OSMOREGULATION; SALINITY; STRESS, PHYSIOLOGICAL;

EID: 84891793137     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0082155     Document Type: Article

References (71)

1. Dai A, Yang S, Song Y (1986) Marine crabs in China Sea. Marine Publishing Company, Beijing.
2. Yu C, Song H, Yao G (2003) Geographical distribution and faunal analysis of crab resources in the East China Sea. J Zhejiang Ocean Univ 22: 108-113
3. Liu L, Li J, Liu P, Zhao FZ, Gao BQ et al. (2012) A genetic linkage map of swimming crab (Portunus trituberculatus) based on SSR and AFLP markers. Aquaculture 344: 66-81.
4. Romano N, Zeng CS (2012) Osmoregulation in decapod crustaceans: implications to aquaculture productivity, methods for potential improvement and interactions with elevated ammonia exposure. Aquaculture 334: 12-23.
5. Xu QH, Liu Y (2011) Gene expression profiles of the swimming crab Portunus trituberculatus exposed to salinity stress. Marine Biology 158: 2161-2172. doi:10.1007/s00227-011-1721-8.
6. Charmantier G, Charmantier-Daures M, Towle D (2008) Osmotic and ionic regulation in aquatic arthropods.
7. Fu L, Jintian H, Yebing Y, Wenping Y (2010) AFFECTS OF SALINITY ON GROWTH, MUSCLE COMPOSITION,AND PROTEASE ACTIVITY OF PORTUNUS TRITUBERCULATUS. Transactions of Oceanology and Limnology: 137-142
8. Ping-ping Z, Chun-lin W, wei SW, Dan-hua W (2010) Effect of Salinity Stress on Serum Non-specific Immune Factors in Swimming Crab; Portunus trituberculatus. Fisheries Science: 634-638.
9. Shan J, Qiang-hua X (2011) Influence of salinity stress on the activity of gill Na+/K+-ATPase in swimming crab (Portunus trituberculatus). Journal Fisheries of China: 1475-1480.
10. Yan-ming S, Bao-quan G, Ping L, Xian-yun R, Yang L, et al. (2012) The tolerance to and optimal salinity for growth in swimming crab Portunus trituberculatus "Huangxuan No. 1". JOURNAL OF DALIAN OCEAN UNIVERSITY: 398-401
11. Yun-liang L, Fang W, Qin-feng G, Shuang-lin D (2012) Effects of salinity on the respiratory metabolism of pre-and post-maturity swimming crab (Portunus trituberculatus). Journal Fisheries of China: 1392-1399.
12. Yunliang L, Fang W, Zhuoying Z, Shuanglin D, Shen M (2012) Effects of salinity on growth, molt and energy utilization of juvenileswimming crab Portunus trituberculatus. Journal Fishery Sciences of China: 237-245.
13. Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10: 57-63. doi:10.1038/nrg2484. PubMed: 19015660.
14. Ramayo-Caldas Y, Mach N, Esteve-Codina A, Corominas J, Castelló A et al. (2012) Liver transcriptome profile in pigs with extreme phenotypes of intramuscular fatty acid composition. BMC Genomics 13: 547-. PubMed: 23051667.
15. Sánchez CC, Weber GM, Gao G, Cleveland BM, Yao J et al. (2011) Generation of a reference transcriptome for evaluating rainbow trout responses to various stressors. BMC Genomics 12: 626-. PubMed: 22188770.
16. Wang XW, Luan JB, Li JM, Su YL, Xia J et al. (2011) Transcriptome analysis and comparison reveal divergence between two invasive whitefly cryptic species. BMC Genomics 12: 458-. PubMed: 21939539.
17. Zeng D, Chen X, Xie D, Zhao Y, Yang C et al. (2013) Transcriptome Analysis of Pacific White Shrimp (Litopenaeus vannamei) Hepatopancreas in Response to Taura Syndrome Virus (TSV) Experimental. Infection - PLOS ONE 8: e57515. doi:10.1371/journal.pone.0057515.
18. Li S, Zhang X, Sun Z, Li F, Xiang J (2013) Transcriptome Analysis on Chinese Shrimp Fenneropenaeus chinensis during WSSV Acute. Infection - PLOS ONE 8: e58627. doi:10.1371/journal.pone.0058627.
19. He L, Jiang H, Cao D, Liu L, Hu S, et al. (2013) Comparative Transcriptome Analysis of the Accessory Sex Gland and Testis from the Chinese Mitten Crab (Eriocheir sinensis). PLoS ONE 8: e53915
20. Ma KY, Qiu GF, Feng JB, Li JL (2012) Transcriptome Analysis of the Oriental River Prawn, Macrobrachium nipponense Using 454 Pyrosequencing for Discovery of Genes and Markers. PLOS ONE 7: e39727. PubMed: 22745820.
21. He L, Wang Q, Jin XK, Wang Y, Chen LL et al. (2012) Transcriptome Profiling of Testis during Sexual Maturation Stages in Eriocheir sinensis Using Illumina Sequencing. PLOS ONE 7: e33735. PubMed: 22442720.
22. Marguerat S, Bähler J (2010) RNA-seq: from technology to biology. Cell Mol Life Sci 67: 569-579. doi:10.1007/s00018-009-0180-6. PubMed: 19859660.
23. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA et al. (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29: 644-652. doi:10.1038/nbt.1883. PubMed: 21572440.
24. Altschul SF, Madden TL, Schäffer 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. doi:10.1093/nar/25.17.3389. PubMed: 9254694.
25. Storey JD, Tibshirani R (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci U S A 100: 9440-9445. doi:10.1073/pnas.1530509100. PubMed: 12883005.
26. de Hoon MJ, Imoto S, Nolan J, Miyano S (2004) Open source clustering software. Bioinformatics 20: 1453-1454. doi:10.1093/bioinformatics/bth078. PubMed: 14871861.
27. Young MD, Wakefield MJ, Smyth GK, Oshlack A (2010) Method Gene ontology analysis for RNA-seq: accounting for selection bias.
28. Xu QH, Liu Y, Liu RL (2010) Expressed sequence tags from cDNA library prepared from gills of the swimming crab, Portunus trituberculatus. Journal of Experimental Marine Biology and Ecology 394: 105-115. doi:10.1016/j.jembe.2010. 08.002.
29. Liu Y, Cui ZX, Song CW, Wang SY, Li QQ (2011) Multiple isoforms of immune-related genes from hemocytes and eyestalk cDNA libraries of swimming crab Portunus trituberculatus. Fish Shellfish Immunol 31: 29-42. PubMed: 21362485.
30. Wang SY, Cui ZX, Liu Y, Li QQ, Song CW (2012) The first homolog of pacifastin-related precursor in the swimming crab (Portunus trituberculatus): Characterization and potential role in immune response to bacteria and fungi. Fish Shellfish Immunol 32: 331-338. PubMed: 22154999.
31. Wang SY, Cui ZX, Liu Y, Li QQ, Song CW (2012) Identification and characterization of a serine protease inhibitor (PtSerpin) in the swimming crab Portunus trituberculatus. Fish Shellfish Immunol 32: 544-550. PubMed: 22245590.
32. Nie QH, Sandford EE, Zhang XQ, Nolan LK, Lamont SJ (2012) Deep Sequencing-Based Transcriptome Analysis of Chicken Spleen in Response to Avian Pathogenic Escherichia coli (APEC). Infection - PLOS ONE 7.
33. Péqueux A (1995) Osmotic regulation in crustaceans. Journal of Crustacean Biology 15: 1-60. doi:10.1163/193724095X00578.
34. Rainbow P, Black W (2001) Effects of changes in salinity on the apparent water permeability of three crab species:< i> Carcinus maenas,< i> Eriocheir sinensis and< i> Necora puber. Journal of Experimental Marine Biology and Ecology 264: 1-13
35. Morris R, Lockwood A, Dawson M (1982) An effect of acclimation salinity on the fatty acid composition of the gill phospholipids and water flux of the amphipod crustacean Gammarus duebeni. Comparative Biochemistry and Physiology Part A: Physiology 72: 497-503
36. Freire CA, Onken H, McNamara JC (2008) A structure-function analysis of ion transport in crustacean gills and excretory organs. Comparative Biochemistry and Physiology A:-Molecular and Integrative Physiology 151: 272-304. doi:10.1016/j.cbpa.2007.05.008.
37. McNamara JC, Faria SC (2012) Evolution of osmoregulatory patterns and gill ion transport mechanisms in the decapod Crustacea: a review. J Comp Physiol B 182: 997-1014. doi:10.1007/s00360-012-0665-8. PubMed: 22534792.
38. Meng J, Zhu Q, Zhang L, Li C, Li L, et al. (2013) Genome and Transcriptome Analyses Provide Insight into the Euryhaline Adaptation Mechanism of Crassostrea gigas. PLoS ONE 8: e58563
39. King LS, Kozono D, Agre P (2004) From structure to disease: the evolving tale of aquaporin biology. Nat Rev Mol Cell Biol 5: 687-698. doi:10.1038/nrm1469. PubMed: 15340377.
40. Cerdà J, Finn RN (2010) Piscine aquaporins: an overview of recent advances. J Exp Zool A Ecol Genet Physiol 313: 623-650. PubMed: 20717996.
41. Tipsmark CK, Sørensen KJ, Madsen SS (2010) Aquaporin expression dynamics in osmoregulatory tissues of Atlantic salmon during smoltification and seawater acclimation. J Exp Biol 213: 368-379. doi:10.1242/jeb.034785. PubMed: 20086120.
42. Kwong RWM, Kumai Y, Perry SF (2013) The Role of Aquaporin and Tight Junction Proteins in the Regulation of Water Movement in Larval Zebrafish (Danio rerio). PLOS ONE 8.
43. Tournaire-Roux C, Sutka M, Javot H, Gout E, Gerbeau P et al. (2003) Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins. Nature 425: 393-397. doi:10.1038/nature01853. PubMed: 14508488.
44. Santoni V, Vinh J, Pflieger D, Sommerer N, Maurel C (2003) A proteomic study reveals novel insights into the diversity of aquaporin forms expressed in the plasma membrane of plant roots. Biochem J 373: 289-296. doi:10.1042/ BJ20030159. PubMed: 12678916.
45. Azad AK, Katsuhara M, Sawa Y, Ishikawa T, Shibata H (2008) Characterization of four plasma membrane aquaporins in tulip petals: A putative homolog is regulated by phosphorylation. Plant Cell Physiol 49: 1196-1208. doi:10.1093/pcp/pcn095. PubMed: 18567892.
46. Boursiac Y, Chen S, Luu D-T, Sorieul M, van den Dries N et al. (2005) Early effects of salinity on water transport in Arabidopsis roots. Molecular and cellular features of aquaporin expression. Plant Physiol 139: 790-805. doi:10.1104/pp.105.065029. PubMed: 16183846.
47. Weihrauch D, Ziegler A, Siebers D, Towle DW (2002) Active ammonia excretion across the gills of the green shore crab Carcinus maenas: participation of Na+/K+-ATPase, V-type H+-ATPase and functional microtubules. J Exp Biol 205: 2765-2775. PubMed: 12177142.
48. Henry RP, Garrelts EE, McCarty MM, Towle DW (2002) Differential induction of branchial carbonic anhydrase and Na+/K+ ATPase activity in the euryhaline crab, Carcinus maenas, in response to low salinity exposure. J Exp Zool 292: 595-603. doi:10.1002/jez.10075. PubMed: 12115925.
49. Luquet CM, Weihrauch D, Senek M, Towle DW (2005) Induction of branchial ion transporter mRNA expression during acclimation to salinity change in the euryhaline crab Chasmagnathus granulatus. J Exp Biol 208: 3627-3636. doi:10.1242/jeb.01820. PubMed: 16169940.
50. Jayasundara N, Towle DW, Weihrauch D, Spanings-Pierrot C (2007) Gill-specific transcriptional regulation of Na+/K+-ATPase α-subunit in the euryhaline shore crab Pachygrapsus marmoratus: sequence variants and promoter structure. J Exp Biol 210: 2070-2081. doi:10.1242/jeb.004309. PubMed: 17562880.
51. Tsai J-R, Lin H-C (2007) V-type H+-ATPase and Na+,K+-ATPase in the gills of 13 euryhaline crabs during salinity acclimation. J Exp Biol 210: 620-627. doi:10.1242/jeb.02684. PubMed: 17267648.
52. Drews G, Graszynski K (1987) The transepithelial potential difference in the gills of the fiddler crab, Uca tangeri: influence of some inhibitors. Journal of Comparative Physiology B 157: 345-353. doi:10.1007/BF00693361.
53. Krippeit-Drews P, Drews G, Graszynski K (1989) Effects of ion substitution on the transepithelial potential difference of the gills of the fiddler crabUca tangeri: evidence for a H+-pump in the apical membrane. Journal of Comparative Physiology B, Biochemical, Systemic, and Environmental Physiology 159: 43-49. doi:10.1007/BF00692682.
54. Onken H, Putzenlechner M (1995) A V-ATPase drives active, electrogenic and Na+-independent Cl-absorption across the gills of Eriocheir sinensis. Journal of Experimental Biology 198: 767-774. PubMed: 9318532.
55. Huong DTT, Yang WJ, Okuno A, Wilder MN (2001) Changes in free amino acids in the hemolymph of giant freshwater prawn Macrobrachium rosenbergii exposed to varying salinities: relationship to osmoregulatory ability. Comparative Biochemistry and Physiology A:-Molecular and Integrative Physiology 128: 317-326. doi:10.1016/S1095-6433(00)00310-X. PubMed: 11223393.
56. Tan C, Choong K (1981) Effect of hyperosmotic stress on hemolymph protein, muscle ninhydrin-positive substances and free amino acids in Macrobrachium rosenbergii(de man). Comparative Biochemistry and Physiology Part A: Physiology 70: 485-489. doi:10.1016/0300-9629(81)92559-7.
57. Dalla Via G (1986) Salinity responses of the juvenile penaeid shrimp Penaeus japonicus: I. Oxygen consumption and estimations of productivity. Aquaculture 55: 297-306
58. Dalla Via G (1986) Salinity responses of the juvenile penaeid shrimp Penaeus japonicus: II. Free amino acids. Aquaculture 55: 307-316
59. Lang MA (1987) Correlation between osmoregulation and cell volume regulation. Am J Physiol 252: R768-R773. PubMed: 3565606.
60. Dooley PC, Long BM, West JM (2000) Amino acids in haemolymph, single fibres and whole muscle from the claw of freshwater crayfish acclimated to different osmotic environments. Comp Biochem Physiol A Mol Integr Physiol 127: 155-165. doi:10.1016/S0305-0491(00)00247-9. PubMed: 11064283.
61. Trachootham D, Lu W, Ogasawara MA, Valle NR-D, Huang P (2008) Redox regulation of cell survival. Antioxid Redox Signal 10: 1343-1374. PubMed: 18522489.
62. Mann M, Jensen ON (2003) Proteomic analysis of post-translational modifications. Nat Biotechnol 21: 255-261. doi:10.1038/nbt0303-255. PubMed: 12610572.
63. Johnston M, Hutvagner G (2011) Posttranslational modification of Argonautes and their role in small RNA-mediated gene regulation. Silence 2: 1-4. doi:10.1186/1758-907X-2-1. PubMed: 21247442.
64. Huang QS, Yan JH, Tang JY, Tao YM, Xie XL et al. (2010) Cloning and tissue expressions of seven chitinase family genes in Litopenaeus vannamei. Fish Shellfish Immunol 29: 75-81. PubMed: 20202477.
65. Salma U, Uddowla MH, Kim M, Kim JM, Kim BK et al. (2012) Five hepatopancreatic and one epidermal chitinases from a pandalid shrimp (Pandalopsis japonica): cloning and effects of eyestalk ablation on gene expression. Comp Biochem Physiol B Biochem Mol Biol 161: 197-207. doi:10.1016/j.cbpb.2011.11.005. PubMed: 22138334.
66. Proespraiwong P, Tassanakajon A, Rimphanitchayakit V (2010) Chitinases from the black tiger shrimp Penaeus monodon: phylogenetics, expression and activities. Comp Biochem Physiol B Biochem Mol Biol 156: 86-96. doi:10.1016/j.cbpb.2010.02.007. PubMed: 20197105.
67. Tan SH, Degnan BM, Lehnert SA (2000) The Penaeus monodon Chitinase 1 Gene Is Differentially Expressed in the Hepatopancreas During the Molt. Cycles - Mar Biotechnol (NY) 2: 126-135.
68. Mirzaei M, Pascovici D, Atwell BJ, Haynes PA (2012) Differential regulation of aquaporins, small GTPases and V-ATPases proteins in rice leaves subjected to drought stress and recovery. Proteomics 12: 864-877. doi:10.1002/pmic.201100389. PubMed: 22539437.
69. Shikata Y, Rios A, Kawkitinarong K, DePaola N, Garcia JGN et al. (2005) Differential effects of shear stress and cyclic stretch on focal adhesion remodeling, site-specific FAK phosphorylation, and small GTPases in human lung endothelial cells. Exp Cell Res 304: 40-49. doi:10.1016/j.yexcr.2004.11.001. PubMed: 15707572.
70. Marešová L, Vydarený T, Sychrová H (2012) Comparison of the influence of small GTPases Arl1 and Ypt6 on yeast cells' tolerance to various stress factors. FEMS Yeast Res 12: 332-340. doi:10.1111/j.1567-1364.2011.00780.x. PubMed: 22188384.
71. Towle DW, Henry RP, Terwilliger NB (2011) Microarray-detected changes in gene expression in gills of green crabs (Carcinus maenas) upon dilution of environmental salinity. Comp Biochem Physiol Part D Genomics Proteomics 6: 115-125. PubMed: 21220218.