Skip to main content
SpringerLink
Log in

Insight into the salt tolerance factors of a wild halophytic rice, Porteresia coarctata: a physiological and proteomic approach

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Salinity poses a serious threat to yield performance of cultivated rice in South Asian countries. To understand the mechanism of salt-tolerance of the wild halophytic rice, Porteresia coarctata in contrast to the salt-sensitive domesticated rice Oryza sativa, we have compared P. coarctata with the domesticated O. sativa rice varieties under salinity stress with respect to several physiological parameters and changes in leaf protein expression. P. coarctata showed a better growth performance and biomass under salinity stress. Relative water content was conserved in Porteresia during stress and sodium ion accumulation in leaves was comparatively lesser. Scanning electron microscopy revealed presence of two types of salt hairs on two leaf surfaces, each showing a different behaviour under stress. High salt stress for prolonged period also revealed accumulation of extruded NaCl crystals on leaf surface. Changes induced in leaf proteins were studied by two-dimensional gel electrophoresis and subsequent quantitative image analysis. Out of more than 700 protein spots reproducibly detected and analyzed, 60% spots showed significant changes under salinity. Many proteins showed steady patterns of up- or downregulation in response to salinity stress. Twenty protein spots were analyzed by MALDI-TOF, leading to identification of 16 proteins involved in osmolyte synthesis, photosystem functioning, RubisCO activation, cell wall synthesis and chaperone functions. We hypothesize that some of these proteins confer a physiological advantage on Porteresia under salinity, and suggest a pattern of salt tolerance strategies operative in salt-marsh grasses. In addition, such proteins may turn out to be potential targets for recombinant cloning and introgression in salt-sensitive plants.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

MALDI-TOF:

Matrix-assisted laser desorption and ionization-time of flight

2-D PAGE:

2-Dimensional polyacrylamide gel electrophoresis

BAP:

Benzyl amino purine

WPM:

Woody plant medium

References

  • Abbasi FM, Komatsu S (2004) A proteomic approach to analyze salt-responsive proteins in rice leaf sheath. Proteomics 4(7):2072–2081

    Article  PubMed  CAS  Google Scholar 

  • Alberta KR, Mikkelsenb TN, Ro-Poulsena H (2005) Effects of ambient versus reduced UV-B radiation on high arctic Salix arctica assessed by measurements and calculations of chlorophyll a fluorescence parameters from fluorescence transients. Physiol Plant 124:208–226

    Article  Google Scholar 

  • Badger MR, Lorimer GH (1981) Interaction of sugar phosphates with the catalytic site of ribulose-1, 5-bisphosphate carboxylase. Biochemistry 20:2219–2225

    Article  PubMed  CAS  Google Scholar 

  • Bal AR, Dutt SK (1986) Mechanism of salt tolerance in wild rice (Oryza coarctata Roxb). Plant Soil 92:399–404

    Article  CAS  Google Scholar 

  • Barr HD, Weatherley PE (1962) A re-examination of the relative turgidity technique for estimating water deficit in leaves. Aust J Biol Sci 15:413–428

    Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Bucher M, Brander KA, Sbicego S, Mandel T, Kuhlemeier C (1995) Aerobic fermentation in tobacco pollen. Plant Mol Biol 28(4):739–750

    Article  PubMed  CAS  Google Scholar 

  • Chattopadhayay MK, Tiwari BS, Chattopadhyay G, Bose A, Sengupta DN, Ghosh B (2002) Protective role of exogenous polyamines on salinity-stressed rice (Oryza sativa) plants. Physiol Plant 116:192–199

    Article  PubMed  CAS  Google Scholar 

  • Chitnis PR, Xu Q, Chirnis VP, Nechustai R (1995) Function and organization of photosystem I polypeptides. Photosynth Res 44:23–40

    Article  CAS  Google Scholar 

  • Christie PJ, Hahn M, Walbot V (1991) Low-temperature accumulation of alcohol dehydrogenase-1 mRNA and protein activity in maize and rice seedlings. Plant Physiol 95:699–706

    Article  PubMed  CAS  Google Scholar 

  • Consortium S (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815

    Article  Google Scholar 

  • Das-Chatterjee A, Goswami L, Maitra S, GhoshDastider K, 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 

  • Demmig-Adams B, Adams WW (1994) Light stress and photoprotection related to the xanthophyll cycle. In: Foyer CH, Mullineaux PM (eds) Causes of photooxidative stress and amelioration of defence systems in plants, vol III. CRC Press, Boca Raton, pp 105–126

    Google Scholar 

  • Dooki AD, Franz JM, Askari H, Zaiee A (2006) Salekdeh GH (2004) Proteomic responses of rice young panicles to salinity. Proteomics 6:6498–6507

    Article  PubMed  CAS  Google Scholar 

  • Edmondson DL, Kane HJ, Andrews TJ (1990) Substrate isomerization inhibits ribulosebisphosphate carboxylase-oxygenase during catalysis. FEBS Lett 260:62–66

    Article  CAS  Google Scholar 

  • Enami I, Tohri A, Kamo M, Ohta H, Shen J (1997) Identification of domains on the 43 KDa chlorophyll-carrying protein/CP43 that are shielded from tryptic attack by binding of the extrinsic 33 KDa protein with photosystem II complex. Biochim Biophys Acta 1320:17–26

    Article  PubMed  CAS  Google Scholar 

  • Fernandes FM, Arrabaça MC, Carvalho LMM (2004) Sucrose metabolism in Lupinus albus L. under salt stress. Biologia Plantarum 48(2):317–319

    Article  CAS  Google Scholar 

  • Flowers TJ, Colmer TJ (2008) Salinity tolerance in halophytes. New Phytol 179:945–963

    Article  PubMed  CAS  Google Scholar 

  • Flowers TJ, Flowers SA, Hajibagheri MA, Yeo AR (1990) Salt tolerance in the halophytic wild rice, Porteresia coarctata. T. New Phytol 114:675–684

    Article  CAS  Google Scholar 

  • Frydman J, Hartl U (1996) Principles of chaperone-assisted protein folding: differences between in vitro and in vivo mechanisms. Science 272(5267):1497–1502

    Article  PubMed  CAS  Google Scholar 

  • Gao C, wang Y, Liu G, Yang C, Jiang J, Li H (2008) Expression profiling of salinity-alkali stress responses by large-scale expressed sequence tag analysis in Tamarix hispid. Plant Mol Biol 66(3):245–258

    Article  PubMed  CAS  Google Scholar 

  • Ge S, Sang T, Lu B, Hong D (1999) Phylogeny of rice genomes with emphasis on origins of allotetraploid species. Proc Natl Acad Sci USA 96(25):14400–14405

    Article  PubMed  CAS  Google Scholar 

  • Ghars MA, Parre E, Debez A, Bordenave M, Richard L, Leport L, Bouchereau A, Savoure′ A, Abdelly C (2008) Comparative salt tolerance analysis between Arabidopsis thaliana and Thellungiella halophila, with special emphasis on K+/Na+ selectivity and proline accumulation. J Plant Physiol 165:588–599

    Article  PubMed  CAS  Google Scholar 

  • Ghosh Dastider K, Maitra S, Goswami L, Roy D, Das KP, Majumder AL (2006) An insight into the molecular basis of salt-tolerance of L-myo inositol 1-phosphate synthase (PcINO1) from Porteresia coarctata (Roxb.) Tateoka, a halophytic wild rice. Plant Physiol 140:1279–1296

    Article  Google Scholar 

  • Hasegawa PM, Bressan RA, Zhu J, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499

    Article  PubMed  CAS  Google Scholar 

  • Hoshida H, Tanaka Y, Hibino T, Hayashi Y, Tanaka A, Takabe T, Takabe T (2000) Enhanced tolerance to salt stress in transgenic rice that overexpresses chloroplast glutamine synthetase. Plant Mol Biol 43(1):103–111

    Article  PubMed  CAS  Google Scholar 

  • Ingersoll JC, Rothenberg M, Liedl BE, Folkerts K, Garvin D, Hanson MR, Doyle JJ, Mutschler MA (1994) A novel anther-expressed adh-homologous gene in Lycopersicon esculentum. Plant Mol Biol 26:1875–1891

    Article  PubMed  CAS  Google Scholar 

  • Iraki NM, Bressan RA, Hasegawa PM, Carpita NC (1989) Alteration of the physical and chemical structure of the primary cell wall of growth-limited plant cells adapted to osmotic stress. Plant Physiol 91(1):39–47

    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(4):537–548

    Article  PubMed  CAS  Google Scholar 

  • Jelodar NB, Blackhall NW, Hartman TPV, Brar DS, Khush G, Davey MR, Cocking EC, Power JB (1999) Intergeneric somatic hybrids of rice [Oryza sativa L. (+) Porteresia coarctata (Roxb.) Tateoka]. Theor Appl Genet 99:570–577

    Article  CAS  Google Scholar 

  • Jordan DB, Chollet R, Ogren WL (1983) Binding of phosphorylated effectors by active and inactive forms of ribulose-1, 5-bisphosphate carboxylase. Biochemistry 22:3410–3418

    Article  CAS  Google Scholar 

  • Kant S, Kant P, Raveh E, Barak S (2006) Evidence that differential gene expression between the halophyte, Thellungiella halophila, and Arabidopsis thaliana is responsible for higher levels of the compatible osmolyte praline and tight control of Na+ uptake in T. halophila. Plant Cell Environ 29:1220–1234

    Article  PubMed  CAS  Google Scholar 

  • Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotech 17:287–291

    Article  CAS  Google Scholar 

  • Kotchoni SO, Bartels D (2003) Water stress induces the up-regulation of a specific set of genes in plants: aldehyde dehydrogenases as an example. Bulg J Plant Physiol special issue:37–51

  • Krause GH (1994) The role of oxygen in photoinhibition of photosynthesis. In: Foyer CH, Mullineaux PM (eds) Causes of photooxidative stress and amelioration of defence systems in plants. CRC Press, Boca Raton, pp 43–76

    Google Scholar 

  • Latha R, Rao CS, Subramaniam HMS, Eganathan P, Swaminathan MS (2004) Approaches to breeding for salinity tolerance—a case study on Porteresia coarctata. Ann Appl Biol 144(2):177–184

    Article  Google Scholar 

  • M’Rah S, Ouerghi Z, Eymery F, Rey P, Hajji M, Grignon C, Lachaal M (2007) Efficiency of biochemical protection against toxic effects of accumulated salt differentiates Thellungiella halophila from Arabidopsis thaliana. J Plant Physiol 164:375–384

    Article  PubMed  CAS  Google Scholar 

  • Majee M, Maitra S, Ghose Dastidar K, Pattanaik S, Chatterjee A, Hait N, Das KP, Majumder AL (2004) A novel salt-tolerant L-myo-inositol-1-phosphate synthase from Porteresia coarctata (Roxb.) Tateoka, a halophytic wild rice. J Biol Chem 279(27):28539–28552

    Google Scholar 

  • Matton DP, Constabel P, Brisson N (1990) Alcohol dehydrogenase gene expression in potato following elicitor and stress treatment. Plant Mol Biol 14:775–783

    Article  PubMed  CAS  Google Scholar 

  • Mizobuchi A, Yamamoto Y (1989) Assembly of photosystem II polypeptides and expression of oxygen evolution activity in the chloroplasts of Euglena gracilis Z. during the dark-light transition. Biochim Biophys Acta 977:26–32

    Article  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15(3):473–497

    Article  CAS  Google Scholar 

  • Osmond CB, Grace SC (1995) Perspectives on photoinhibition and photorespiration in the field: quintessential inefficiencies of the light and dark reactions of photosynthesis. J Exp Bot 46:1351–1362

    CAS  Google Scholar 

  • Parker R, Flowers TJ, Moore AL, Harpham NVJ (2006) An accurate and reproducible method for proteome profiling of the effects of salt stress in the rice leaf lamina. J Exp Bot 57(5):1109–1118. doi:10.1093/jxb/erj134

    Article  PubMed  CAS  Google Scholar 

  • Ramagli LS, Rodriguez LV (1985) Quantification of microgram amounts of protein in two dimensional polyacrylamide gel electrophoresis sample buffer. Electrophoresis 6:559–563

    Article  CAS  Google Scholar 

  • Renault S (2005) Response of red-osier dogwood (Cornus stolonifera) seedlings to sodium sulphate salinity: effects of supplemental calcium. Physiol Plant 123(1):75–81

    Article  CAS  Google Scholar 

  • Schauenstein E, Esterbauer H, Zollner H (1977) Dicarbonyl compounds. In: Lagnado JR (ed) Aldehydes in biological systems. Pion Ltd, London, pp 112–157

    Google Scholar 

  • Sengupta S, Patra B, Ray S, Majumder AL (2008) Inositol methyl tranferase from a halophytic wild rice, Porteresia coarctata Roxb. (Tateoka): regulation of pinitol synthesis under abiotic stress. Plant cell Environ 31(10):1442–1459

    Article  PubMed  CAS  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol 3:217–223

    PubMed  CAS  Google Scholar 

  • Somerville CR, Portis AR Jr, Ogren WL (1982) A mutant of Arabidopsis thaliana which lacks activation of RUBP carboxylase in vivo. Plant Physiol 70:381–387

    Article  PubMed  CAS  Google Scholar 

  • Strasser A, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Yunus M, Pathre U, Mohanty P (eds) Probing photosynthesis: mechanisms, regulation and adaptation. Taylor & Francis, London, pp 445–483

    Google Scholar 

  • Strasser A, Tsimilli-Michael M, Srivastava A (2004) Analysis of the fluorescence transient. In: George C, Papageorgiou C, Govindjee (ed) Chlorophyll fluorescence: a signature of photosynthesis. Advances in photosynthesis and respiration series (Govindjee, series editor). Kluwer, Dordrecht, pp 321–362

  • Sugihara K, Hanagata N, Dubinsky Z, Baba S, Karube I (2000) Molecular characterization of cDNA encoding oxygen evolving enhancer protein 1 increased by salt treatment in the mangrove Bruguiera gymnorrhiza. Plant Cell Physiol 41(11):1279–1285

    Article  PubMed  CAS  Google Scholar 

  • Sung DY, Vierling E, Guy CL (2001) Comprehensive expression profile analysis of the arabidopsis Hsp70 gene family. Plant Physiol 126(2):789–800

    Article  PubMed  CAS  Google Scholar 

  • Volkov V, Wang B, Dominy PJ, Fricke W, Amtmann A (2004) Thellungiella halophila, a salt-tolerant relative of Arabidopsis thaliana, possesses effective mechanisms to discriminate between potassium and sodium. Plant Cell Environ 27:1–14

    Article  CAS  Google Scholar 

  • Wallsgrove RM, Turner JC, Hall NP, Kendall AC, Bright SWJ (1987) Barley mutants lacking chloroplast glutamine synthetase—biochemical and genetic analysis. Plant Physiol 83:155–158

    Article  PubMed  CAS  Google Scholar 

  • Whitmarsh J, Govindjee (2001) Photosystem II In: Encyclopedia of life sciences. MacMillan, UK

  • Willekens H, Chamnongpol S, Davey M, Schraudner M, Langebartels C, Van Montagu M, Inze’ D, Van Camp W (1997) Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants. EMBO J 16:4806–4816

    Article  PubMed  CAS  Google Scholar 

  • Yan S, Tang Z, Su W, Sun W (2005) Proteomic analysis of salt stress-responsive proteins in rice root. Proteomics 5(1):235–244

    Article  PubMed  CAS  Google Scholar 

  • Yu J, Hu S, Wang J, Wong GK, Li S, Liu B, Deng Y, Dai L, Zhou Y, Zhang X et al (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296:79–92

    Article  PubMed  CAS  Google Scholar 

  • Zhong H, Laüchli A (1988) Incorporation of [14C] glucose into cell wall polysaccharides of cotton roots: effects of NaCl and CaCl2. Plant Physiol 88:511–514

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work has been supported by research grants (to ALM) from the Department of Biotechnology, Government of India. SSG thanks Council of Scientific and Industrial Research and Department of Biotechnology, Government of India for Senior Research Fellowship.

Author information

Authors and Affiliations

  1. Plant Molecular and Cellular Genetics, Bose Institute (Centenary Building), P-1/12, C.I.T Scheme VIIM, Kolkata, 700054, India

    Sonali Sengupta & Arun Lahiri Majumder

Authors
  1. Sonali Sengupta
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Arun Lahiri Majumder
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Arun Lahiri Majumder.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material (DOC 141 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sengupta, S., Majumder, A.L. Insight into the salt tolerance factors of a wild halophytic rice, Porteresia coarctata: a physiological and proteomic approach. Planta 229, 911–929 (2009). https://doi.org/10.1007/s00425-008-0878-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-008-0878-y

Keywords

Search

Navigation