Abstract
Salinity stress severely affects plant growth and development causing crop loss worldwide. Suaeda asparagoides is a salt-marsh euhalophyte widely distributed in southwestern foreshore of Korea. To isolate salt tolerance genes from S. asparagoides, we constructed a cDNA library from leaf tissues of S. asparagoides that was treated with 200 mM NaCl. A total of 1,056 clones were randomly selected for EST sequencing, and 932 of them produced readable sequence. By sequence analysis, we identified 538 unigenes and registered each in National Center for Biotechnology Information. The 80 salt stress related genes were selected to study their differential expression. Reverse transcription-PCR and Northern blot analysis revealed that 23 genes were differentially expressed under the high salinity stress conditions in S. asparagoides. They are functionally diverse including transport, signal transduction, transcription factor, metabolism and stress associated protein, and unknown function. Among them dehydrin (SaDhn) and RNA binding protein (SaRBP1) were examined for their abiotic stress tolerance in yeast (Saccharomyces cerevisiae). Yeast overexpressing SaDhn and SaRBP1 showed enhanced tolerance to osmotic, freezing and heat shock stresses. This study provides the evidence that SaRBP1 and SaDhn from S. asparagoides exert abiotic stress tolerance in yeast. Information of salt stress related genes from S. asparagoides would contribute for the accumulating genetic resources to improve osmotic tolerance in plants.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl Acids Res 25:3389–3402
Ardie SW, Nishiuchi S, Liu S, Takano T (2010) Ectopic expression of the K+ channel β subunits from Puccinellia tenuiflora (KPutB1) and rice (KOB1) alters K+ homeostasis of yeast and Arabidopsis. Mol Biotechnol 48:76–86
Baisakh N, Subudhi PK, Varadwaj P (2008) Primary responses to salt stress in a halophyte smooth cordgrass (Spartina alterniflora Loisel.). Funct Integr Genomics 8:287–300
Bray EA (1993) Molecular responses to water deficit. Plant Physiol 103:1035–1040
Bray EA, Bailey-Serres J, Weretilnyk E (2000) Responses to abiotic stresses. In: Buchannan B, Gruissem W, Jones R (eds) Biochemistry and molecular biology of plants. American Society of Plant Physiologist, Rockville, pp 1158–1249
Burd CG, Dreyfuss G (1994) Conserved structures and diversity of functions of RNA-binding proteins. Science 265:615–621
Campbell SA, Close TJ (1997) Dehydrins: genes, proteins, and associations with phenotypic traits. New Phytol 137:61–74
Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci USA 81:1991–1995
Close TJ (1996) Dehydrins: emergence of a biochemical role of a family of plant dehydration proteins. Physiol Plant 97:795–803
Danyluk J, Perron A, Houde M, Limin A, Fowler B, Benhamou N, Sarhan F (1998) Accumulation of an acidic dehydrin in the vicinity of the plasma membrane during cold acclimation of wheat. Plant Cell 10:623–638
Deng W, Luo K, Li Z, Yang Y (2008) Molecular cloning and characterization of a mitochondrial dicarboxylate/tricarboxylate transporter gene in Citrus junos response to aluminum stress. Mitochondrial DNA 19(4):376–384
Dure L III (1993) Structural motifs in LEA proteins. In: Close TJ (ed) Plant responses to cellular dehydration during environmental stress. American Society of Plant Physiologist, Rockville, pp 91–103
Ewing B, Green P (1998) Base-calling of automated sequencer traces using Phred. II. Error probabilities. Genome Res 8:186–194
Fukamatsu Y, Yabe N, Hasunuma K (2003) Arabidopsis NDK1 is a component of ROS signaling by interacting with three catalases. Plant Cell Physiol 44:982–989
Gellissen G, Melber K, Janowicz ZA, Dahlems UM, Weydemann U, Piontek M, Strasser AW, Hollenberg CP (1992) Heterologous protein production in yeast. Antonie Van Leeuwenhoek 62:79–93
González-García MP, Rodríguez D, Nicolás C, Rodríguez PL, Nicolás G, Lorenzo O (2003) Negative regulation of abscisic acid signaling by the Fagus sylvatica FsPP2C1 plays a role in seed dormancy regulation and promotion of seed germination. Plant Physiol 133:135–144
Gueguen Y, Cadoret JP, Flament D, Barreau-Roumiguière C, Girardot AL, Garnier J, Hoareau A, Bachère E, Escoubas JM (2003) Immune gene discovery by expressed sequence tags generated from hemocytes of the bacteria-challenged oyster, Crassostrea gigas. Gene 303:139–145
Hara M, Terashima TF, Fukaya T, Kuboi T (2003) Enhancement of cold tolerance and inhibition of lipid peroxidation by citrus dehydrin in transgenic tobacco. Planta 217:290–298
Higgins DG, Thompson JD, Gibson TJ (1996) Using CLUSTAL for multiple sequence alignments. Methods Enzymol 266:383–402
Imai R, Chang L, Ohta A, Bray EA, Takagi M (1996) A lea-class gene of tomato confers salt and freezing tolerance when expressed in Saccharomyces cerevisiae. Gene 170:243–248
Iturriaga G, Schneider K, Salamini F, Bartels D (1992) Expression of desiccation-related proteins from the resurrection plant Craterostigma plantagineum in transgenic tobacco. Plant Mol Biol 20:555–558
Iturriaga G, Cushman MAF, Cushman JC (2006) An EST catalogue from the resurrection plant Selaginella lepidophylla reveals abiotic stress-adaptive genes. Plant Sci 170:1173–1184
Jha B, Agarwal PK, Reddy PS, Lal S, Sopory SK, Reddy MK (2009) Identification of salt-induced genes from Salicornia brachiata, an extreme halophyte through expressed sequence tags analysis. Genes Genet Syst 84:111–120
Jin H, Plaha P, Park JY, Hong CP, Lee IS, Yang ZH, Jiang GB, Kwak SS, Liu SK, Lee JS, Kim YA, Lim YP (2006) Comparative EST profiles of leaf and root of Leymus chinensis, a xerophilous grass adapted to high pH sodic soil. Plant Sci 170:1081–1086
Kore-eda S, Cushman MK, Akselrod I, Bufford D, Fredrickson M, Clark E, Cushman JC (2004) Transcript profiling of salinity stress responses by large-scale expressed sequence tag analysis in Mesembryanthemum crystallinum. Gene 341:83–92
Lång V (1993) The role ABA and ABA-induced gene expression in cold acclimation of Arabidopsis thaliana. Dissertation, Swedish University of Agricultural Sciences
Landsberger M, Lorković ZJ, Oelműller R (2002) Molecular characterization of nucleus-localized RNA-binding proteins from higher plants. Plant Mol Biol 48:413–421
Li H, Wang Y, Jiang J, Liu G, Gao C, Yang C (2009) Identification of genes responsive to salt stress on Tamarix hispida roots. Gene 433:65–71
Lorkovíc ZJ (2009) Role of plant RNA-binding proteins in development, stress response and genome organization. Trends Plant Sci 14:229–236
McCormack E, Tsai YC, Braam J (2005) Handling calcium signaling: Arabidopsis CaMs and CMLs. Trends Plant Sci 10:383–389
Mehta PA, Sivaprakash K, Parani M, Venkataraman G, Parida AK (2005) Generation and analysis of expressed sequence tags from the salt-tolerant mangrove species Avicennia marina (Forsk) Vierh. Theor Appl Genet 110:416–424
Mochida K, Yoshida T, Sakurai T, Yamaguchi-Shinozaki K, Shinozaki K, Tran PL-S (2009) In silico analysis of transcription factor repertoire and prediction of stress responsive transcription factors in soybean. DNA Res 16:353–369
Monroe-Augustus M, Zolman BK, Bartel B (2003) IBR5, a dual-specificity phosphatase-like protein modulating auxin and abscisic acid responsiveness in Arabidopsis. Plant Cell 15:2979–2991
Munns R, Cramer GR, Ball MC (1999) Interactions between rising CO2, soil salinity, and plant growth. In: Luo Y, Mooney HA (eds) Carbon dioxide and environmental stress. Academic Press, San Diego, pp 139–167
Nishiuchi S, Fujihara K, Liu S, Takano T (2010) Analysis of expressed sequence tags from a NaHCO3-treated alkali-tolerant plant, Chloris virgata. Plant Physiol Biochem 48:247–255
Swire-Clark GA, Marcotte WR Jr (1999) The wheat LEA protein Em functions as an osmoprotective molecule in Saccharomyces cerevisiae. Plant Mol Biol 39:117–128
Vinocur B, Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotechnol 16:123–132
Wang Z, Li P, Fredricksen M, Gong Z, Kim CS, Zhang C, Bohnert HJ, Zhu J-K, Bressan RA, Hasegawa PM, Zhao Y, Zhang H (2004) Expressed sequence tags from Thellungiella halophila, a new model to study plant salt-tolerance. Plant Sci 166:609–616
Wang YC, Yang CP, Liu GF, Jiang J, Wu JH (2006) Generation and analysis of expressed sequence tags from a cDNA library of Tamarix androssowii. Plant Sci 170:28–36
Zhang L, Ohta A, Takagi M, Imai R (2000) Expression of plant group 2 and group 3 lea genes in Saccharomyces cerevisiae revealed functional divergence among LEA proteins. J Biochem (Tokyo) 127:611–616
Zhang L, Ma X-L, Zhang Q, Ma C-L, Wang P-P, Sun Y-F, Zhao Y-X, Zhang H (2001) Expressed sequence tags from a NaCl-treated Suaeda salsa cDNA library. Gene 267:193–200
Zhu JK (2000) Genetic analysis of plant salt tolerance using Arabidopsis. Plant Physiol 124:941–948
Acknowledgments
This research was supported by the Genetic Evaluation of Important Biological Resources from National Institute of Biological Resources (NIBR, 2011), the Next-Generation BioGreen 21 Program (Plant Molecular Breeding Center No. PJ007970) of Rural Development Administration and Basic Science Research Program through the National Research Foundation of Korea (KRF) funded by the Ministry of Education, Science and Technology (KRF-2009-0068370 and -2009-0074413), Republic of Korea.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by J. R. Liu.
S. Ayarpadikannan and E. Chung contributed equally to this work.
Rights and permissions
About this article
Cite this article
Ayarpadikannan, S., Chung, E., Cho, CW. et al. Exploration for the salt stress tolerance genes from a salt-treated halophyte, Suaeda asparagoides . Plant Cell Rep 31, 35–48 (2012). https://doi.org/10.1007/s00299-011-1137-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-011-1137-4