Skip to main content
Log in

Primary responses to salt stress in a halophyte, smooth cordgrass (Spartina alterniflora Loisel.)

  • Original Paper
  • Published:
Functional & Integrative Genomics Aims and scope Submit manuscript

Abstract

The response of a grass halophyte Spartina alterniflora at early stages of salt stress was investigated through generation and systematic analysis of expressed sequence tags (ESTs) from both leaf and root tissues. Random EST sequencing produced 1,227 quality ESTs, which were clustered into 127 contigs, and 368 were singletons. Of the 495 unigenes, 27% represented genes for stress response. Comparison of the 368 singletons against the Oryza sativa gene index showed that >85% of these genes had similarity with the rice unigenes. Moreover, the phylogenetic analysis of an EST similar to myo-inositol 1-phosphate synthase of Spartina and some selected grasses and halophytes showed closeness of Spartina with maize and rice. Transcript abundance analysis involving eight known genes of various metabolic pathways and nine transcription factor genes showed temporal and tissue-dependent variation in expression under salinity. Reverse northern analysis of a few selected unknown and ribosomal genes exhibited much higher abundance of transcripts in response to salt stress. The results provide evidence that, in addition to several unknown genes discovered in this study, genes involved in ion transport, osmolyte production, and house-keeping functions may play an important role in the primary responses to salt stress in this grass halophyte.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller D, Lipman DJ (1997) Gapped BLAST and PSI–BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Ayala FO, Leary JW, Schumaker KS (1996) Increased vacuolar and plasma membrane H+-ATPase activities in Salicornia bigelovii Torr. in response to NaCl. J Exp Bot 47:25–32

    Article  CAS  Google Scholar 

  • Baisakh N, Subudhi PK, Parami NP (2006) cDNA–AFLP analysis reveals differential gene expression in response to salt stress in a halophyte Spartina alterniflora Loisel. Plant Sci 170:1141–1149

    Article  CAS  Google Scholar 

  • Berardini TZ, Mundodi S, Reiser R, Huala E, Garcia-Hernandez M, Zhang P, Mueller LM, Yoon J, Doyle A, Lander G, Moseyko N, Yoo D, Xu I, Zoeckler B, Montoya M, Miller N, Weems D, Rhee SY (2004) Functional annotation of the Arabidopsis genome using controlled vocabularies. Plant Physiol 135:1–11

    Article  CAS  Google Scholar 

  • Bohnert HJ, Gong Q, Li P, Ma S (2006) Unravelling abiotic stress tolerance mechanisms-getting genomics going. Curr Opin Plant Biol 9:180–188

    Article  PubMed  CAS  Google Scholar 

  • Chung HJ, Ferl RJ (1999) Arabidopsis alcohol dehydrogenase expression in both shoots and roots is conditioned by root growth environment. Plant Physiol 121:429–436

    Article  PubMed  CAS  Google Scholar 

  • Cushman JC, Bohnert HJ (2000) Genomics approaches to plant salt tolerance. Curr Opin Biotechnol 3:117–124

    CAS  Google Scholar 

  • Das-Chatterjee A, Goswami L, Maitra S, Dastidar KG, Ray S, Majumder AL (2006) Introgression of a novel salt-tolerant l-myo-inositol 1-phosphate synthase from Porteresia coarctata (Roxb.) Tateoka (PcINO1) confers salt tolerance to evolutionary diverse organisms. FEBS Lett 580:3980–3988

    Article  PubMed  CAS  Google Scholar 

  • Dolferus R, Jacobs M, Peacock WJ, Dennis ES (1994) Differential interactions of promoter elements in stress responses of the Arabidopsis Adh gene. Plant Physiol 105:1075–1087

    Article  PubMed  CAS  Google Scholar 

  • Ewing B, Green P (1998) Base-calling of automated sequencer traces using Phred. II. Error probabilities. Genome Res 8:186–194

    PubMed  CAS  Google Scholar 

  • Feliciello I, Chinali G (1993) A modified alkaline lysis method for the preparation of highly purified plasmid DNA from Escherichia coli. Anal Biochem 212:394–401

    Article  PubMed  CAS  Google Scholar 

  • Flowers TJ (2004) Improving crop salt tolerance. J Exp Bot 55:307–319

    Article  PubMed  CAS  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Calif Agric Exp Stn Circ 347

  • Imai J, Yahara I (2000) Role of HSP90 in salt stress tolerance via stabilization and regulation of calcineurin. Mol Cell Biol 20:9262–9270

    Article  PubMed  CAS  Google Scholar 

  • Inada M, Ueda A, Shi W, Takabe T (2005) A stress-inducible plasma membrane protein 3 (AcPMP3) in a monocotyledonous halophyte, Aneurolepidium chinense, regulates cellular Na+ and K+ accumulation under salt stress. Planta 220:395–402

    Article  PubMed  CAS  Google Scholar 

  • Ishitani M, Majumder AL, Bornhouser A, Michalowski CB, Jensen RG, Bohnert HJ (1996) Coordinate transcriptional induction of myo-inositol metabolism during environmental stress. Plant J 9:537–548

    Article  PubMed  CAS  Google Scholar 

  • Jeong MJ, Park SC, Byun MO (2001) Improvement of salt tolerance in transgenic potato plants by glyceraldehyde-3 phosphate dehydrogenase gene transfer. Mol Cells 12:185–189

    PubMed  CAS  Google Scholar 

  • Kawasaki S, Borchert C, Deyholos M, Wang H, Brazille S, Kawai K, Galbraith D, Bohnert HJ (2001) Gene expression profiles during the initial phase of salt stress in rice. Plant Cell 13:889–906

    Article  PubMed  CAS  Google Scholar 

  • Liu D, Zhang X, Cheng Y, Takano T, Liu S (2006) rHsp90 gene expression in response to several environment stresses in rice (Oryza sativa L.). Plant Physiol Biochem 44:380–386

    Article  PubMed  CAS  Google Scholar 

  • Low R, Rockel B, Kirsch M, Ratajczak R, Hortensteiner S, Martinoia E, Luttge U, Rausch T (1996) Early salt stress effects on the differential expression of vacuolar H+-ATPase genes in roots and leaves of Mesembryathemum crystallinum. Plant Physiol 110:259–265

    Article  PubMed  CAS  Google Scholar 

  • Majumder AL, Chatterjee A, Ghosh Dastidar K, Majee M (2003) Diversification and evolution of l-myo inositol 1-phosphate synthase. FEBS Lett 553:3–10

    Article  PubMed  CAS  Google Scholar 

  • McIntosh KB, Bonham-Smith PC (2005) The two ribosomal protein L23A genes are differentially transcribed in Arabidopsis thaliana. Genome 48:443–454

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Mukhopadhyay A, Vij S, Tyagi A (2004) Overexpression of a zinc-finger protein gene from rice confers tolerance to cold, dehydration, and salt stress in transgenic tobacco. Proc Natl Acad Sci U S A 101:6309–6314

    Article  PubMed  CAS  Google Scholar 

  • Nadal E, Zapater M, Alepuz PM, Sumoy L, Mas G, Posas F (2004) The MAPK Hog1 recruits Rpd3 histone deacetylase to activate osmoresponsive genes. Science 427:370–374

    Google Scholar 

  • Nadeau K, Das A, Walsh CT (1993) Hsp90 chaperonins possess ATPase activity and bind heat shock transcription factors and peptidyl prolyl isomerases. J Biol Chem 268:1479–1487

    PubMed  CAS  Google Scholar 

  • Niu X, Wang H, Bressan RA, Hasegawa PM (1994) Molecular cloning and expression of a glyceraldehyde-3-phosphate dehydrogenase gene in a desert halophyte, Atriplex nummularia L. Plant Physiol 104:1105–1106

    Article  PubMed  CAS  Google Scholar 

  • Ouellet F, Carpentier E, Cop MJTV, Monroy AF, Sarhan F (2001) Regulation of a wheat actin-depolymerizing factor during cold acclimation. Plant Physiol 125:360–368

    Article  PubMed  CAS  Google Scholar 

  • Owttrim GW (2006) RNA helicases and abiotic stress. Nucleic Acids Res 34:3220–3230

    Article  PubMed  CAS  Google Scholar 

  • Pareek A, Singla SL, Grover A (1995) Immunological evidence for accumulation of two high-molecular-weight (104 and 90 kDa) HSPs in response to different stresses in rice and in response to high temperature stress in diverse plant genera. Plant Mol Biol 29:293–301

    Article  PubMed  CAS  Google Scholar 

  • Park JM, Park CJ, Lee SB, Ham BK, Shin R, Paek KH (2001) Overexpression of the tobacco Tsi1 gene encoding an EREBP/AP2-type transcription factor enhances resistance against pathogen attack and osmotic stress in tobacco. Plant Cell 13:1035–1046

    Article  PubMed  CAS  Google Scholar 

  • Paul AL, Ferl RJ (1991) Adh1 and Adh2 regulation. Maydica 36:129–143

    Google Scholar 

  • 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 19:651–652

    Article  PubMed  CAS  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:2002–2007

    Article  Google Scholar 

  • Qi Y, Yamauchi Y, Ling J, Kawano N, Li D, Tanaka K (2005) The submergence-induced gene OsCTP in rice (Oryza sativa L.) is similar to Escherichia coli cation transport protein ChaC. Plant Sci 168:15–22

    Article  CAS  Google Scholar 

  • Sahi C, Singh A, Kumar K, Blumwald E, Grover A (2006) Salt stress response in rice: genetics, molecular biology, and comparative genomics. Funct Integr Genomics 6:263–284

    Article  PubMed  CAS  Google Scholar 

  • Sakamoto H, Maruyama K, Sakuma Y, Meshi T, Iwabuchi M, Shinozaki K, Yamaguchi-Shinozaki K (2004) Arabidopsis cys2/his2-type zinc-finger proteins function as transcription repressors under drought, cold, and high-salinity stress conditions. Plant Physiol 136:2734–2746

    Article  PubMed  CAS  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6:405–409

    Article  PubMed  CAS  Google Scholar 

  • Taji T, Seki M, Satou M, Sakurai T, Kobayashi M, Ishiyama K, Narusaka Y, Narusaka M, Zhu JK, Shinozaki K (2004) Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis microarray. Plant Physiol 135:1697–1709

    Article  PubMed  CAS  Google Scholar 

  • Telles GP, da Silva FR (2001) Trimming and clustering sugarcane ESTs. Genet Mol Biol 24:17–23

    CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Vashisht AA, Pradhan A, Tuteja R, Tuteja N (2005) Cold and salinity stress-inducible bipolar pea DNA helicase 47 is involved in protein synthesis and stimulated by phosphorylation with protein kinase C. Plant J 44:76–87

    Article  PubMed  CAS  Google Scholar 

  • Wang Z, Li P, Fredricksen M, Gong Z, Kim CS, Zhang C, Bohnert HJ, Zhu JK, 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 166:609–614

    Article  CAS  Google Scholar 

  • Wong CE, Li Y, Whitty BR, Dı’az-Camino C, Akhter SR, Brandle JE, Golding GB, Weretilnyk EA, Moffatt BA, Griffith M (2005) Expressed sequence tags from the Yukon ecotype of Thellungiella reveal that gene expression in response to cold, drought and salinity shows little overlap. Plant Mol Biol 58:561–574

    Article  PubMed  CAS  Google Scholar 

  • Xia H, Mao Q, Paulson HL, Davidson BL (2002) siRNA-mediated gene silencing in vitro and in vivo. Nat Biotechnol 20:1006–1010

    Article  PubMed  CAS  Google Scholar 

  • Xu WF, Shi WM (2006) Expression profiling of the 14-3-3 gene family in response to salt stress and potassium and iron deficiencies in young tomato (Solanum lycopersicum) roots: analysis by real-time RT-PCR. Ann Bot 98:965–974

    Article  PubMed  CAS  Google Scholar 

  • Zhang L, Ma XL, Zhang Q, Ma CL, Wang PP, Sun YF, Zhao YX, Zhang H (2001) Expressed sequence tags from a NaCl-treated Suaeda salsa cDNA library. Gene 267:193–200

    Article  PubMed  CAS  Google Scholar 

  • Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgment

The authors thank Dr. M. A. Cohn and Dr. M. S. Kang for reviewing the manuscript before submission. The financial support for this study from the USDA–CSREES is gratefully acknowledged. This manuscript is approved for publication by the Director of Louisiana Agricultural Experiment Station as manuscript number 07-14-0423.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Prasanta K. Subudhi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Baisakh, N., Subudhi, P.K. & Varadwaj, P. Primary responses to salt stress in a halophyte, smooth cordgrass (Spartina alterniflora Loisel.). Funct Integr Genomics 8, 287–300 (2008). https://doi.org/10.1007/s10142-008-0075-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10142-008-0075-x

Keywords

Navigation