Abstract
Salinity stress constrains the growth, development, and yield in crops. Rice is an important cereal crop highly affected by salinity. To ensure the agriculture production in salt-affected soils, it is enormously entail to understand the salt adaptation strategies of plants. Salinity directly affects the morphology, physiology, and metabolism of the plants. The current study was carried out to check the influence of different concentrations of sodium chloride on rice cultivar. Higher concentration of the NaCl showed significant reduction in the growth, pigment system, and metabolites in rice cultivars. Salinity also elicited the antioxidant enzymes (CAT, SOD, and POX) response and gene expression. Cell biological studies showed the H2O2 production and nuclear fragmentation due to alleviated salinity stress. To delineate the portrayal of antioxidant proteins and autophagy mechanism in salinity stress, the homologs of rice CAT1, Mn-SOD, GPX, ATG1, and ATG6 genes were retrieved from blast search. The real-time PCR analysis showed differential expression of genes and depicts new molecular insight of target genes to understand the salinity stress and autophagy-mediated stress signaling pathways.
Similar content being viewed by others
References
Amirjani MR (2010) Effect of salinity stress on growth, mineral composition, proline content antioxidant enzymes of soybean. Am J Plant Physiol 5:350–360
Amirjani MR (2011) Effect of salinity stress on growth, sugar content, pigments and enzyme activity of rice. Int J Bot 7:73–81
Atlante A, Bobba A, Calissano P, Passarella S, Marra E (2003) The apoptosis/necrosis transition in cerebellar granule cells depends on the mutual relationship of the antioxidant and the proteolytic systems which regulate ROS production and cytochrome c release en route to death. J Neurochem 84:960–971
Beauchamp CO, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287
Chandlee JM, Scandalios JG (1984) Analysis of variants affecting the catalase development program in Maize scutellum. Theor Appl Genet 69:71–77
Chen HJ, Chen JY, Wang SJ (2008) Molecular regulation of starch accumulation in rice seedling leaves in response to salt stress. Acta Physiol Plant 30:135–142
Chomczynski P (1993) A reagent for the single-step simultaneous isolation of RNA, DNA and proteins from cell and tissue samples. Biotechniques 15:532–537
Enari M, Sakahira H, Yokoyama H, Okawa K, Iwamatsu A, Nagata S (1998) A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD. Nature 391:43–50
FAO, Rice Market Monitor (2012) Trade and Markets Division, Food and Agriculture Organization of the United Nations. XV (3). http://www.fao.org
Fojtova M, Kovarik A (2000) Genotoxic effect of cadmium is associated with apoptotic changes in tobacco cells. Plant Cell Environ 23:531–537
Gechev TS, Gadjev IZ, Hille J (2004) An extensive microarray analysis of AAL-toxin-induced cell death in Arabidopsis thaliana brings new insights into the complexity of programmed cell death in plants Cell. Mol Life Sci 61:1185–1197
Golldack D, Li C, Mohan H, Probst N (2014) Tolerance to drought and salt stress in plants: unraveling the signaling networks. Front Plant Sci 5:151
Gupta B, Huang B (2014) Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. Int J Genom 1:1–18
Hashi US, Karim A, Saikat HM, Islam R, Islam MA (2015) Effect of salinity and potassium levels on different morpho-physiological characters of two soybean (Glycine max L.). Genotypes J Rice Res 3:143. doi:10.4172/2375-4338.1000143
Huang J, Klionsky DJ (2007) Autophagy and human disease. Cell Cycle 6:1837–1849
Hummon AB, Lim SR, Difilippantonio MJ, Ried T (2007) Isolation and solubilization of proteins after TRIzol® extraction of RNA and DNA from patient material following prolonged storage. Biotechniques 42:467–472
Idrees M, Naeem M, Aftab T, Khan MMA, Moinuddin (2011) Salicylic acid mitigates salinity stress by improving antioxidant defence system and enhances vincristine and vinblastine alkaloids production in periwinkle Catharanthus roseus (L.) G. Don 33:987–999
Ismail A, Takeda S, Nick P (2014) Life and death under salt stress: same players, different timing? J Exp Bot 65:2963–2979
Jamil M, Lee CC, Rehman S, Lee DB, Ashraf M, Rha ES (2005) Salinity (NaCl) tolerance of Brassica species at germination and early seedling growth. Electron J Environ Agric Food Chem 4:970–976
Jamil M, Ashraf M, Rehman S, Ahmad M, Rha ES (2012) Salinity induced changes in cell membrane stability, protein and RNA contents. Afr J Biotechnol 11:6476–6483
Jogaiah S, Ramteke SD, Sharma J, Upadhyay AK (2014) Moisture and salinity stress induced changes in biochemical constituents and water relations of different grape rootstock cultivars. Int J Agron. doi:10.1155/2014/789087
Joseph EA, Mohanan KV (2013) A study on the effect of salinity stress on the growth and yield of some native rice cultivars of Kerala state of India. Agric For Fish 2:141–150
Kamada Y, Yoshino K, Kondo C, Kawamata T, Oshiro N, Yonezawa K, Ohsumi Y (2010) Tor directly controls the Atg1 kinase complex to regulate autophagy. Mol Cell Biol 4:1049–1058
Khan MS, Hemalatha S (2015) Autophagy: molecular insight and role in plant programmed cell death and defense mechanism. Inte Res J Biol Sci 4:78–83
Khan S, Qureshi MI, Kamaluddin Tanweer A, Abdin MZ (2007) Protocol for isolation of genomic DNA from dry and fresh roots of medicinal plants suitable for RAPD and restriction digestion. Afr J Biotechnol 3:175–178
Khan S, Mirza KJ, Abdin MZ (2010) Development of RAPD markers for authentication of medicinal plant Cuscuta reflexa. Eur Asia J BioSci 4:1–7
Kim M, Ahn JW, Jin UH, Choi D, Paek KH, Pai HS (2003) Activation of the programmed cell death pathway by inhibition of proteasome function in plants. J Biol Chem 278:19406–19415
Klionsky DJ, Cregg JM, Dunn WA Jr et al (2003) A unified nomenclature for yeast autophagy related genes. Dev Cell 5:539–545
Koca H, Ozdemir F, Turkan I (2006) Effect of salt stress on lipid peroxidation and superoxide dismutase and peroxidase activities of Lycopersicon esculentum and L. pennellii. Biol Plant 50:745–748
Koukalova B, Kovarik A, Fajkus J, Siroky J (1997) Chromatin fragmentation associated with apoptotic changes in tobacco cells exposed to cold stress. FEBS Lett 414:289–292
Kumar V, Shriram V, Jawali N, Shitole MG (2007) Differential response of indica rice genotypes to NaCl stress in relation to physiological and biochemical parameters. Arch Agron Soil Sci 53:581–592
Kumar V, Singh A et al (2015) Genome-wide association mapping of salinity tolerance in rice (Oryza sativa). DNA Res 22:133–145
Lee MH, Cho EJ et al (2013) Divergences in morphological changes and antioxidant responses in salt-tolerant and salt-sensitive rice seedlings after salt stress. Plant Physiol Biochem 70:325–335
Levine B, Klionsky DJ (2004) Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell 6:463–477
Liu Y, Xiong Y, Bassham DC (2009) Autophagy is required for tolerance of drought and salt stress in plants. Autophagy 5:954–963
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275
Maathuis FJM (2013) Sodium in plants: perception, signaling, and regulation of sodium fluxes. J Exp Bot 65:849–858
Mackinney G (1941) Absorption of light by chlorophyll solutions. J Biol Chem 140:315–322
Maclachlan S, Zalik S (1963) Plastid structure, chlorophyll concentration, and free amino acid composition of a chlorophyll mutant of barley. Can J Bot 41:1053–1062
Moharramnejad S, Taherkhani T (2015) Response of antioxidant enzyme activity and pigment content in common bean (Phaseolus vulgaris L.) seedlings under salt stress. Sci J (CSJ) 36:1–6
Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250
Munns R, Tester M (2008) Mechanism of salinity tolerance. Annu Rev Plant Biol 59:651–681
Noctor G, Foyer CH (1998) Ascorbate and glutathione keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279
Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349
Rana RM, Dong S, Ali Z, Huang J, Zhang HS (2012) Regulation of ATG6/beclin-1 homologs by abiotic stresses and hormones in rice (Oryza sativa L.). Genet Mol Res 11:3676–3687
Rao PS, Mishra B, Gupta SR, Rathore A (2013) Physiological response to salinity and alkalinity of rice genotypes of varying salt tolerance grown in field lysimeters. J Stress Physiol Biochem 9:54–65
Reggiori F, Klionsky DJ (2002) Autophagy in the eukaryotic cell. Eukaryot Cell 1:11–21
Sangeeta Y, Mohd I, Aqil A, Shamsul H (2011) Causes of salinity and plant manifestations to salt stress: a review. J Environ Biol 32:667–685
Shahbaz M, Ashraf M (2013) Improving salinity tolerance in cereals. Crit Rev Plant Sci 32:237–249
Shin JH, Yoshimoto K, Ohsumi Y, Jeon JS, An G (2009) OsATG10b, an autophagosome component, is needed for cell survival against oxidative stresses in rice. Mol Cells 27:67–74
Shobbar MS, Niknam V, Shobbar ZS, Ebrahimzadeh H (2010) Effect of salt and drought stresses on some physiological traits of three rice genotypes differing in salt tolerance. JSUTOR 36:1–9
Shouval RS, Shvets E, Fass E, Shorer H, Gil L, Elazar Z (2007) Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J 26:1749–1760
Singh PK, Shahi SK, Singh AP (2015) Effects of salt stress on physico-chemical changes in maize (zea mays L.) plants in response to salicylic acid. Indian J Plant Sci 4:69–77
Slavikova S, Ufaz S, Avin-Wittenberg T, Levanony H, Galili G (2008) An autophagy-associated Atg8 protein is involved in the responses of Arabidopsis seedlings to hormonal controls and abiotic stresses. J Exp Bot 59:4029–4043
Sultana N, Ikeda T, Itoh R (2000) Corrigendum to effect of NaCl salinity on photosynthesis and dry matter accumulation in developing rice grains. Environ Exp Bot 43:181–183
Tsugane K, Kobayashi K, Niwa Y, Ohba Y, Wada K, Kobayashi H (1999) A recessive Arabidopsis mutant that grows photoautotrophically under salt stress shows enhanced active oxygen detoxification. Plant Cell 11:1195–1206
Turan S, Tripathy BC (2015) Salt-stress induced modulation of chlorophyll biosynthesis during de-etiolation of rice seedlings. Physiol Plant 153:477–491
Wyllie AH, Kerr JFR, Currie AR (1980) Cell death: the significance of apoptosis. Int Rev Cytol 68:251–306
Xiong Y, Contento AL, Nguyen PQ, Bassham DC (2007) Degradation of oxidized proteins by autophagy during oxidative stress in Arabidopsis. Plant Physiol 143:291–299
Yang Z, Klionsky DJ (2009) An overview of the molecular mechanism of autophagy. Curr Top Microbiol Immunol 335:1–32. doi:10.1007/978-3-642-00302-8-1
Zhang L, Ma H, Chen T, Pen J, Yu S, Zhao X (2014a) Morphological and physiological responses of cotton (gossypium hirsutum L.) plants to salinity. PLoS ONE 9:1–14
Zhang X, Lu G, Long W, Zou X, Li F, Nishio T (2014b) Recent progress in drought and salt tolerance studies in Brassica crops. Breed Sci 64:60–73
Zheng C, Jiang D, Liu F, Dai T, Jing Q et al (2009) Effects of salt and water logging stresses and their combination on leaf photosynthesis, chloroplast ATP synthesis, and antioxidant capacity in wheat. Plant Sci 176:575–582
Zhou J, Wang X, Jiao Y et al (2007) Global genome expression analysis of rice in response to drought and high-salinity stresses in shoot, flag leaf, and panicle. Plant Mol Biol 63:591–608
Zhu JK (2001) Cell signaling under salt, water and cold stresses. Curr Opin Plant Biol 4:401–406
Zou H, Li Y, Liu X, Wang X (1999) An APAF-1.cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J Biol Chem 17:11549–11556
Acknowledgments
The authors are thankful to B.S. Abdur Rahman University, Chennai for providing the facilities and Junior Research Fellowship to (M. S. Khan) to carry out the research project.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by K. Apostol.
Rights and permissions
About this article
Cite this article
Khan, M.S., Hemalatha, S. Biochemical and molecular changes induced by salinity stress in Oryza sativa L.. Acta Physiol Plant 38, 167 (2016). https://doi.org/10.1007/s11738-016-2185-8
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-016-2185-8