Abstract
Soil salinity is a major abiotic stress that affects global agricultural productivity. Exploring the mechanisms that halophytes employ to thrive and flourish under saline environments is essential to increase the salt tolerance in sensitive crop species. Of the three halophytes used in this study Salicornia brachiata and Suaeda maritima belong to the same family Chenopodiaceae, while Sesuvium portulacastrum, a mangrove-associated halophyte, belongs to the family Aizoaceae. Assuming that halophytes of same family share similar salt tolerance mechanisms, we generated a suppression subtractive hybridization (SSH1) cDNA library from salt-treated leaf tissues of S. brachiata as tester and that of S. maritima as driver to identify salt-responsive genes unique to S. brachiata. To elucidate the difference in salt-tolerance mechanisms, and to identify salt-tolerance mechanisms amongst different families of halophytes, SSH2 library was generated from salt-treated leaf tissue of S. brachiata as tester and that of S. portulacastrum as driver. Totally, 87 and 49 EST clones representing unique genes were obtained from SSH1 and SSH2 libraries, respectively. Examination of the expression patterns of 17 (SSH1) and 15 (SSH2) differentially expressed genes using semi-quantitative RT-PCR confirmed up-regulation of these genes in shoots in response to salt treatment and elevated CO2 condition, but to a different extent. This study has provided insights into the molecular responses of S. brachiata to salt stress and elevated CO2 conditions.
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Abbreviations
- AC:
-
Ambient CO2 without salt
- EC:
-
Elevated CO2 without salt
- ACS:
-
Ambient CO2 with salt
- ECS:
-
Elevated CO2 with salt
References
Al-Zahrani AHH (1997) Salt tolerance in the halophyte Halopeplis perfoliata (Forssk.) Bge. Ex. Schweinf: seasonal variations in ion concentrations. Indian J Plant Physiol 2:135–137
Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1
Ball M, Munns R (1992) Plant responses to salinity under elevated atmospheric concentrations of CO2 Australian. J Bot 40:515–525
Blackmore S, Wortley AH, Skvarla JJ, Rowley JR (2007) Pollen wall development in flowering plants. New Phytol 174:483–498
Brown MS, Goldstein JL (1993) Mad bet for Rab. Nature 366:14–15
Covington MF, Maloof JN, Straume M, Kay SA, Harmer SL (2008) Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development. Genome Biol 9:R130
Diatchenko L et al (1996) Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci 93:6025–6030
Fu X et al (2005) Construction of a SSH library of Aegiceras corniculatum under salt stress and expression analysis of four transcripts. Plant Sci 169:147–154
Geissler N, Hussin S, Koyro H-W (2008) Elevated atmospheric CO2 concentration ameliorates effects of NaCl salinity on photosynthesis and leaf structure of Aster tripolium L. J Exp Bol 60(1):137–151
Geissler N, Hussin S, Koyro H-W (2010) Elevated atmospheric CO2 concentration enhances salinity tolerance in Aster tripolium L. Planta 231:583–594
Glenn EP, Brown JJ, Blumwald E (1999) Salt tolerance and crop potential of halophytes. Crit Rev Plant Sci 18:227–255
Guo Z-F, Ou W-Z, Lu S-Y, Zhong Q (2006) Differential responses of antioxidative system to chilling and drought in four rice cultivars differing in sensitivity. Plant Physiol Biochem 44:828–836
Habte E, Müller LM, Shtaya M, Davis SJ, KORFF M (2014) Osmotic stress at the barley root affects expression of circadian clock genes in the shoot. Plant Cell Environ 37:1321–1337
Haydon MJ, Cobbett CS (2007) A novel major facilitator superfamily protein at the tonoplast influences zinc tolerance and accumulation in Arabidopsis. Plant Physiol 143:1705–1719
Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611
Huang X, Madan A (1999) CAP3: a DNA sequence assembly program. Genome Res 9:868–877
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
Jha B, Sharma A, Mishra A (2011) Expression of SbGSTU (tau class glutathione S-transferase) gene isolated from Salicornia brachiata in tobacco for salt tolerance. Mol Biol Rep 38:4823–4832
Levitt J (1980) Responses of plants to environmental stress, vol 1. Chilling, freezing, and high temperature stresses. Academic Press, New York
Lezin G, Kosaka Y, Yost HJ, Kuehn MR, Brunelli L (2011) A one-step miniprep for the isolation of plasmid DNA and lambda phage particles. PLoS One 6:e23457
Li X, Zhang L, Li Y, Ma L, Bu N, Ma C (2012) Changes in photosynthesis, antioxidant enzymes and lipid peroxidation in soybean seedlings exposed to UV-B radiation and/or Cd. Plant Soil 352:377–387
Lokhande VH, Nikam TD, Patade VY, Ahire ML, Suprasanna P (2011) Effects of optimal and supra-optimal salinity stress on antioxidative defence, osmolytes and in vitro growth responses in Sesuvium portulacastrum L. Plant Cell Tiss Organ Cult 104(1):41–49
Low R et al (1996) Early salt stress effects on the differential expression of vacuolar H+-ATPase genes in roots and leaves of Mesembryanthemum crystallinum. Plant Physiol 110:259–265
Lutts S, Kinet J, Bouharmont J (1996) NaCl-induced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance. Ann Bot 78:389–398
Marcolino-Gomes J et al (2014) Diurnal oscillations of soybean circadian clock and drought responsive genes. PLoS One 9:e86402
Monastersky R (2013) Global carbon dioxide levels near worrisome milestone. Nature 497(7447):13–14
Pao SS, Paulsen IT, Saier MH (1998) Major facilitator superfamily. Microbiol Mol Biol Rev 62:1–34
Parida AK, Jha B (2013) Physiological and biochemical responses reveal the drought tolerance efficacy of the halophyte Salicornia brachiata. J Plant Growth Regul 32:342–352
Pérez-López U, Robredo A, Lacuesta M, Mena-Petite A, Munoz-Rueda A (2009) The impact of salt stress on the water status of barley plants is partially mitigated by elevated CO2. Environ Exp Bot 66:463–470
Pruneda-Paz JL, Kay SA (2010) An expanding universe of circadian networks in higher plants. Trends Plant Sci 15:259–265
Qi C-H, Chen M, Song J, Wang B-S (2009) Increase in aquaporin activity is involved in leaf succulence of the euhalophyte Suaeda salsa under salinity. Plant Sci 176:200–205
Ramani B, Reeck T, Debez A, Stelzer R, Huchzermeyer B, Schmidt A, Papenbrock J (2006) Aster tripolium L. and Sesuvium portulacastrum L.: two halophytes, two strategies to survive in saline habitats. Plant Physiol Biochem 44:395–408
Ratajczak R (2000) Structure, function and regulation of the plant vacuolar H+-translocating ATPase. Biochim Biophys Acta (BBA) Biomembr 1465:17–36
Rea PA (2007) Plant ATP-binding cassette transporters. Annu Rev Plant Biol 58:347–375
Roden JS, Ball MC (1996) The effect of elevated [CO2] on growth and photosynthesis of two eucalyptus species exposed to high temperatures and water deficits. Plant Physiol 111:909–919
Rozema J et al (2001) UV-B absorbance and UV-B absorbing compounds (para-coumaric acid) in pollen and sporopollenin: the perspective to track historic UV-B levels. J Photochem Photobiol B 62:108–117
Schäffer AA et al (2001) Improving the accuracy of PSI-BLAST protein database searches with composition-based statistics and other refinements. Nucleic Acids Res 29:2994–3005
Sebastiani L, Minnocci A, Tognetti R (2002) Genotypic differences in the response to elevated CO2 concentration of one-year-old olive cuttings (Olea europaea L. cv. Frantoio and Moraiolo) plant biosystems—an international journal dealing with all. Asp Plant Biol 136:199–207
Shukla PS, Agarwal PK, Jha B (2012) Improved salinity tolerance of Arachishypogaea (L.) by the interaction of halotolerant plant-growth-promoting rhizobacteria. J Plant Growth Regul 31:195–206
Silva EN, Ferreira-Silva SL, de Vasconcelos Fontenele A, Ribeiro RV, Viégas RA, Silveira JAG (2010) Photosynthetic changes and protective mechanisms against oxidative damage subjected to isolated and combined drought and heat stresses in Jatropha curcas plants. J Plant Physiol 167:1157–1164
Stanley OD (2008) Bio prospecting marine halophyte Salicornia brachiata for medical importance and salt encrusted land development. J Coast Dev 11:62–69
Tufan F, Uçarlı C, Gürel F (2015) Analysis of expressed sequence tags from cDNA library of Fusarium culmorum infected barley (Hordeum vulgare L.) roots. Bioinformation 11:34
Urban O (2003) Physiological impacts of elevated CO2 concentration ranging from molecular to whole plant responses. Photosynthetica 41:9–20
Wang S-M, Zhang J-L, Flowers TJ (2007) Low-affinity Na+ uptake in the halophyte Suaeda maritima. Plant Physiol 145:559–571
Yadav NS, Shukla PS, Jha A, Agarwal PK, Jha B (2012) The SbSOS1 gene from the extreme halophyte Salicornia brachiata enhances Na+ loading in xylem and confers salt tolerance in transgenic tobacco. BMC Plant Biol 12:188
Yi C et al (2015) High atmospheric carbon dioxide-dependent alleviation of salt stress is linked to RESPIRATORY BURST OXIDASE 1 (RBOH1)-dependent H2O2 production in tomato (Solanum lycopersicum). J Exp Bot 66:7391–7404
Zdobnov EM, Apweiler R (2001) InterProScan—an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17:847–848
Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7:203–214
Acknowledgements
The financial support (Grant number BT/01/CEIB/09/V/08) from Department of Biotechnology, Government of India is acknowledged. We thank Dr. Vinoth, St. Xavier’s College, Palayamkottai for helpful suggestions.
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Communicated by P. Wojtaszek.
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Benjamin, J.J., Krishnasamy, R., Jothiramshekar, S. et al. Identification of salt-induced transcripts by suppression subtractive hybridization and their expression analysis under the combination of salt and elevated CO2 conditions in Salicornia brachiata. Acta Physiol Plant 40, 202 (2018). https://doi.org/10.1007/s11738-018-2764-y
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DOI: https://doi.org/10.1007/s11738-018-2764-y