Global Transcriptome Profiling of Salicornia europaea L. Shoots under NaCl Treatment

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Ma, Jinbiao ^a   Zhang, Meiru ^a,b   Xiao, Xinlong ^a,b   You, Jinjin ^a   Wang, Junru ^a,b   Wang, Tao ^c   Yao, Yinan ^a   Tian, Changyan ^a  

^a XINJIANG INSTITUTE OF ECOLOGY AND GEOGRAPHY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c XINJIANG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; COMPLEMENTARY DNA; POTASSIUM ION; SODIUM CHLORIDE; SODIUM ION; TRANSCRIPTOME;

ARTICLE; BIOSYNTHESIS; CONTROLLED STUDY; DNA LIBRARY; DOWN REGULATION; EXPRESSED SEQUENCE TAG; GENE EXPRESSION; GENE SEQUENCE; HOMEOSTASIS; NONHUMAN; OSMOTIC STRESS; PLANT; PLANT TISSUE; PROTEIN SYNTHESIS; SALICORNIA EUROPAEA; SALT STRESS; SALT TOLERANCE; SEQUENCE HOMOLOGY; SHOOT; TRANSCRIPTION REGULATION; UPREGULATION; AMARANTHACEAE; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENETICS; MOLECULAR GENETICS; PLANT GENE; PROCEDURES;

SALICORNIA EUROPAEA;

CHENOPODIACEAE; GENE EXPRESSION PROFILING; GENES, PLANT; MOLECULAR SEQUENCE ANNOTATION; SODIUM CHLORIDE;

EID: 84879355506     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0065877     Document Type: Article

References (74)

1. Zhu JK, (2001) Plant salt tolerance. Trends in plant science 6: 66-71.
2. Vinocur B, Altman A, (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Current Opinion in Biotechnology 16: 123-132.
3. Flowers T, (2004) Improving crop salt tolerance. Journal of Experimental botany 55: 307-319.
4. Roy SJ, Tucker EJ, Tester M (2011) Genetic analysis of abiotic stress tolerance in crops. Current opinion in plant biology.
5. Chinnusamy V, Zhu J, Zhu JK (2006) Salt stress signaling and mechanisms of plant salt tolerance. Genetic engineering: 141-177.
6. Zhu JK, (2002) Salt and drought stress signal transduction in plants. Annual Review of Plant Biology 53: 247-273.
7. Cockburn W, Whitelam GC, Broad A, Smith J, (1996) The participation of phytochrome in the signal transduction pathway of salt stress responses in Mesembryanthemum crystallinum L. Journal of Experimental botany. 47: 647-653.
8. Liska AJ, Shevchenko A, Pick U, Katz A, (2004) Enhanced photosynthesis and redox energy production contribute to salinity tolerance in Dunaliella as revealed by homology-based proteomics. Plant physiology 136: 2806-2817.
9. Mazel A, Leshem Y, Tiwari BS, Levine A, (2004) Induction of salt and osmotic stress tolerance by overexpression of an intracellular vesicle trafficking protein AtRab7 (AtRabG3e). Plant physiology 134: 118-128.
10. Barkla B, Pantoja O (2011) Plasma membrane and abiotic stress. The Plant Plasma Membrane: 457-470.
11. Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, et al. (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. The Plant Journal 31: 279-292.
12. Kawasaki S, Borchert C, Deyholos M, Wang H, Brazille S, et al. (2001) Gene expression profiles during the initial phase of salt stress in rice. The Plant Cell Online 13: 889-906.
13. Taji T, Seki M, Satou M, Sakurai T, Kobayashi M, et al. (2004) Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis microarray. Plant physiology 135: 1697-1709.
14. Rus A, Yokoi S, Sharkhuu A, Reddy M, Lee BH, et al. (2001) AtHKT1 is a salt tolerance determinant that controls Na+ entry into plant roots. Proceedings of the National Academy of Sciences of the United States of America 98: 14150-14155.
15. Berthomieu P, Conejero G, Nublat A, Brackenbury WJ, Lambert C, et al. (2003) Functional analysis of AtHKT1 in Arabidopsis shows that Na+ recirculation by the phloem is crucial for salt tolerance. Embo Journal 22: 2004-2014.
16. Ardie SW, Xie L, Takahashi R, Liu S, Takano T, (2009) Cloning of a high-affinity K+ transporter gene PutHKT2;1 from Puccinellia tenuiflora and its functional comparison with OsHKT2;1 from rice in yeast and Arabidopsis. Journal of Experimental botany 60: 3491-3502.
17. Halfter U, Liu J, Ishitani M, Xiong L, Stevenson B, et al. (1999) The role of Arabidopsis SOS genes in plant salt tolerance. Plant Biology (Rockville) 1999: 123-123.
18. Shi H, Ishitani M, Kim C, Zhu J-K, (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Plant Biology (Rockville) 2000: 91-91.
19. Apse MP, Aharon GS, Snedden WA, Blumwald E, (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285: 1256-1258.
20. Pardo JM, Reddy MP, Yang SL, Maggio A, Huh GH, et al. (1998) Stress signaling through Ca2+/calmodulin-dependent protein phosphatase calcineurin mediates salt adaptation in plants. Proceedings of the National Academy of Sciences of the United States of America 95: 9681-9686.
21. Espinosa-Ruiz A, Belles JM, Serrano R, Culianez-Macia FA, (1999) Arabidopsis thaliana AtHAL3: a flavoprotein related to salt and osmotic tolerance and plant growth. Plant Journal 20: 529-539.
22. Zhang JS, Xie C, Li ZY, Chen SY, (1999) Expression of the plasma membrane H+-ATPase gene in response to salt stress in a rice salt-tolerant mutant and its original variety. Theoretical and Applied Genetics 99: 1006-1011.
23. Winicov I, Bastola DR, (1999) Transgenic overexpression of the transcription factor Alfin1 enhances expression of the endogenous MsPRP2 gene in alfalfa and improves salinity tolerance of the plants. Plant physiology 120: 473-480.
24. Flowers TJ, Colmer TD, (2008) Salinity tolerance in halophytes. New Phytologist 179: 945-963.
25. Ungar IA, (1996) Effect of salinity on seed germination, growth, and ion accumulation of Atriplex patula (Chenopodiaceae). American Journal of Botany 83: 604-607.
26. Guo Y, Jia W, Song J, Wang D, Chen M, et al. (2012) Thellungilla halophila is more adaptive to salinity than Arabidopsis thaliana at stages of seed germination and seedling establishment. Acta Physiologiae Plantarum 34: 1287-1294.
27. Lv S, Nie L, Fan P, Wang X, Jiang D, et al. (2012) Sodium plays a more important role than potassium and chloride in growth of Salicornia europaea. Acta Physiologiae Plantarum 34: 503-513.
28. Lv S, Jiang P, Chen X, Fan P, Wang X, et al. (2012) Multiple compartmentalization of sodium conferred salt tolerance in Salicornia europaea. Plant Physiology and Biochemistry 51: 47-52.
29. Wang D, Wang H, Han B, Wang B, Guo A, et al. (2012) Sodium instead of potassium and chloride is an important macronutrient to improve leaf succulence and shoot development for halophyte Sesuvium portulacastrum. Plant Physiology and Biochemistry 51: 53-62.
30. Kachout SS, Ben Mansoura A, Mechergui R, Leclerc JC, Rejeb MN, et al. (2012) Accumulation of Cu, Pb, Ni and Zn in the halophyte plant Atriplex grown on polluted soil. Journal of the Science of Food and Agriculture 92: 336-342.
31. Ozawa T, Wu J, Fujii S, (2007) Effect of inoculation with a strain of Pseudomonas pseudoalcaligenes isolated from the endorhizosphere of Salicornia europea on salt tolerance of the glasswort. Soil science and plant nutrition 53: 12-16.
32. Riehl TE, Ungar IA, (1982) Growth and ion accumulation in Salicornia europaea under saline field conditions. Oecologia 54: 193-199.
33. Aghaleh M, Niknam V, Ebrahimzadeh H, Razavi K, (2011) Effect of salt stress on physiological and antioxidative responses in two species of Salicornia (S. persica and S. europaea). Acta Physiologiae Plantarum 33: 1261-1270.
34. Han H, Li Y, Zhou S, (2008) Overexpression of phytoene synthase gene from Salicornia europaea alters response to reactive oxygen species under salt stress in transgenic Arabidopsis. Biotechnology letters 30: 1501-1507.
35. Yang X, Ji J, Wang G, Yang S, Zhao Q, et al. (2011) Over-expressing Salicornia europaea (SeNHX1) gene in tobacco improves tolerance to salt. African Journal of Biotechnology 10: 16452-16460.
36. Zhou S, Chen X, Zhang X, Li Y, (2008) Improved salt tolerance in tobacco plants by co-transformation of a betaine synthesis gene BADH and a vacuolar Na+/H+ antiporter gene SeNHX1. Biotechnology letters 30: 369-376.
37. Chen X, Han H, Jiang P, Nie L, Bao H, et al. (2011) Transformation of β-lycopene cyclase genes from Salicornia europaea and Arabidopsis conferred salt tolerance in Arabidopsis and tobacco. Plant and Cell Physiology 52: 909-921.
38. Wu S, Su Q, An L (2010) Isolation of choline monooxygenase (CMO) gene from Salicornia europaea and enhanced salt tolerance of transgenic tobacco with CMO genes.
39. Aghaleh M, Niknam V, Ebrahimzadeh H, Razavi K, (2009) Salt stress effects on growth, pigments, proteins and lipid peroxidation in Salicornia persica and S. europaea. Biologia Plantarum 53: 243-248.
40. Wang X, Fan P, Song H, Chen X, Lil X, et al. (2009) Comparative Proteomic Analysis of Differentially Expressed Proteins in Shoots of Salicornia europaea under Different Salinity. Journal of Proteome Research 8: 3331-3345.
41. Taji T, Sakurai T, Mochida K, Ishiwata A, Kurotani A, et al. (2008) Large-scale collection and annotation of full-length enriched cDNAs from a model halophyte, Thellungiella halophila. BMC plant biology 8: 115.
42. Chen SH, Guo SL, Wang ZL, Zhao JQ, Zhao YX, et al. (2007) Expressed sequence tags from the halophyte Limonium sinense. Mitochondrial DNA 18: 61-67.
43. Kore-eda S, Cushman MA, Akselrod I, Bufford D, Fredrickson M, et al. (2004) Transcript profiling of salinity stress responses by large-scale expressed sequence tag analysis in Mesembryanthemum crystallinum. Gene 341: 83-92.
44. 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. Nature Biotechnology 29: 644-U130.
45. Iseli C, Jongeneel CV, Bucher P. ESTScan: a program for detecting, evaluating, and reconstructing potential coding regions in EST sequences. 1999: 138-148.
46. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, et al. (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674-3676.
47. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B, (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nature methods 5: 621-628.
48. Zeller G, Henz SR, Widmer CK, Sachsenberg T, Rätsch G, et al. (2009) Stress-induced changes in the Arabidopsis thaliana transcriptome analyzed using whole-genome tiling arrays. The Plant Journal 58: 1068-1082.
49. Kyndt T, Denil S, Haegeman A, Trooskens G, De Meyer T, et al. (2012) Transcriptome analysis of rice mature root tissue and root tips in early development by massive parallel sequencing. Journal of Experimental botany 63: 2141-2157.
50. Xu H, Gao Y, Wang J (2012) Transcriptomic Analysis of Rice (Oryza sativa) Developing Embryos Using the RNA-Seq Technique. Plos One 7.
51. Ushakova S, Kovaleva N, Gribovskaya I, Dolgushev V, Tikhomirova N, (2005) Effect of NaCl concentration on productivity and mineral composition of Salicornia europaea as a potential crop for utilization NaCl in LSS. Advances in Space Research 36: 1349-1353.
52. Moghaieb REA, Saneoka H, Fujita K, (2004) Effect of salinity on osmotic adjustment, glycinebetaine accumulation and the betaine aldehyde dehydrogenase gene expression in two halophytic plants, Salicornia europaea and Suaeda maritima. Plant science 166: 1345-1349.
53. Schachtman DP, Schroeder JI, (1994) Structure and Transport Mechanism of a High-Affinity Potassium Uptake Transporter From Higher-Plants. Nature 370: 655-658.
54. Horie T, Yoshida K, Nakayama H, Yamada K, Oiki S, et al. (2001) Two types of HKT transporters with different properties of Na+ and K+ transport in Oryza sativa. Plant Journal 27: 129-138.
55. Su H, Balderas E, Vera-Estrella R, Golldack D, Quigley F, et al. (2003) Expression of the cation transporter McHKT1 in a halophyte. Plant Molecular Biology 52: 967-980.
56. Blumwald E, Aharon GS, Apse MP, (2000) Sodium transport in plant cells. Biochimica Et Biophysica Acta-Biomembranes 1465: 140-151.
57. Fukuda A, Yazaki Y, Ishikawa T, Koike S, Tanaka Y, (1998) Na+/H+ antiporter in tonoplast vesicles from rice roots. Plant and Cell Physiology 39: 196-201.
58. Rodríguez-Rosales MP, Gálvez FJ, Huertas R, Aranda MN, Baghour M, et al. (2009) Plant NHX cation/proton antiporters. Plant signaling & behavior 4: 265-276.
59. Bassil E, Ohto MA, Esumi T, Tajima H, Zhu Z, et al. (2011) The Arabidopsis Intracellular Na+/H+ Antiporters NHX5 and NHX6 Are Endosome Associated and Necessary for Plant Growth and Development. Plant Cell 23: 224-239.
60. Li HT, Liu H, Gao XS, Zhang HX, (2009) Knock-out of Arabidopsis AtNHX4 gene enhances tolerance to salt stress. Biochemical and Biophysical Research Communications 382: 637-641.
61. Subramanyam K, Sailaja KV, Rao DM, Lakshmidevi K, (2011) Ectopic expression of an osmotin gene leads to enhanced salt tolerance in transgenic chilli pepper (Capsicum annum L.). Plant Cell Tissue and Organ Culture 105: 181-192.
62. Subramanyam K, Arun M, Mariashibu TS, Theboral J, Rajesh M, et al. (2012) Overexpression of tobacco osmotin (Tbosm) in soybean conferred resistance to salinity stress and fungal infections. Planta: 1-17.
63. Yancey PH, Clark ME, Hand SC, Bowlus RD, Somero GN, (1982) Living With Water-Stress - Evolution of Osmolyte Systems. Science 217: 1214-1222.
64. Rentsch D, Hirner B, Schmelzer E, Frommer WB, (1996) Salt stress-induced proline transporters and salt stress-repressed broad specificity amino acid permeases identified by suppression of a yeast amino acid permease-targeting mutant. Plant Cell 8: 1437-1446.
65. Ashraf M, Foolad MR, (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environmental and Experimental Botany 59: 206-216.
66. Ueda A, Shi WM, Sanmiya K, Shono M, Takabe T, (2001) Functional analysis of salt-inducible proline transporter of barley roots. Plant and Cell Physiology 42: 1282-1289.
67. Waditee R, Hibino T, Tanaka Y, Nakamura T, Incharoensakdi A, et al. (2002) Functional characterization of betaine/proline transporters in betaine-accumulating mangrove. Journal of Biological Chemistry 277: 18373-18382.
68. Sokhansanj A, Noori SAS, Niknam V, (2006) Comparison of bacterial and plant genes participating in proline biosynthesis with osmotin gene, with respect to enhancing salinity tolerance of transgenic tobacco plants. Russian Journal of Plant Physiology 53: 110-115.
69. Ueda A, Kathiresan A, Inada M, Narita Y, Nakamura T, et al. (2004) Osmotic stress in barley regulates expression of a different set of genes than salt stress does. Journal of Experimental botany 55: 2213-2218.
70. Foyer C, Lelandais M, Galap C, Kunert KJ, (1991) Effects of Elevated Cytosolic Glutathione-Reductase Activity on The Cellular Glutathione Pool and Photosynthesis in Leaves Under Normal and Stress Conditions. Plant physiology 97: 863-872.
71. Torabi S, Niknam V, (2011) Effects of Iso-osmotic Concentrations of NaCl and Mannitol on some Metabolic Activity in Calluses of Two Salicornia species. In Vitro Cellular & Developmental Biology-Plant 47: 734-742.
72. Magome H, Yamaguchi S, Hanada A, Kamiya Y, Oda K, (2008) The DDF1 transcriptional activator upregulates expression of a gibberellin-deactivating gene, GA2ox7, under high-salinity stress in Arabidopsis. Plant Journal 56: 613-626.
73. Magome H, Yamaguchi S, Hanada A, Kamiya Y, Oda K, (2004) dwarf and delayed-flowering 1, a novel Arabidopsis mutant deficient in gibberellin biosynthesis because of overexpression of a putative AP2 transcription factor. Plant Journal 37: 720-729.
74. Riehl TE, Ungar IA, (1982) Growth and ion Accumulation in Salicornia-Europaea Under Saline field Conditions. Oecologia 54: 193-199.