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Differential expression of salt-responsive genes to salinity stress in salt-tolerant and salt-sensitive rice (Oryza sativa L.) at seedling stage

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Abstract

The understanding of physio-biochemical and molecular attributes along with morphological traits contributing to the salinity tolerance is important for developing salt-tolerant rice (Oryza sativa L.) varieties. To explore these facts, rice genotypes CSR10 and MI48 with contrasting salt tolerance were characterized under salt stress (control, 75 and 150 mM NaCl) conditions. CSR10 expressed higher rate of physio-biochemical parameters, maintained lower Na/K ratio in shoots, and restricted Na translocation from roots to shoots than MI48. The higher expression of genes related to the osmotic module (DREB2A and LEA3) and ionic module (HKT2;1 and SOS1) in roots of CSR10 suppresses the stress, enhances electrolyte leakage, promotes the higher compatible solute accumulation, and maintains cellular ionic homeostasis leading to better salt stress tolerance than MI48. This study further adds on the importance of these genes in salt tolerance by comparing their behaviour in contrasting rice genotypes and utilizing specific marker to identify salinity-tolerant accessions/donors among germplasm; overexpression of these genes which accelerate the selection procedure precisely has been shown.

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Abbreviations

ROS:

Reactive oxygen species

LEA:

Late embryogenesis abundant

HKT:

High-affinity K+ transporter

NHX:

Vacuolar Na+/H+ antiporter

DREB:

Dehydration-responsive element-binding protein

SOS:

Salt overly sensitive

CATA:

Catalase

POX:

Peroxidase

RWC:

Relative water content

DAB:

3,3′-Diaminobenzidine

FW:

Fresh weight

DW:

Dry weight

References

  • Annunziata MG, Ciarmiello LF, Woodrow P, Maximova E, Fuggi A, Carillo P (2017) Durum wheat roots adapt to salinity remodeling the cellular content of nitrogen metabolites and sucrose. Front Plant Sci 7:2035

    Article  Google Scholar 

  • Arnon DI (1949) Copper enzymes in intact chloroplast. Polyphenoxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  CAS  Google Scholar 

  • Ashraf M, Foolad MA (2007) Improving plant abiotic-stress resistance by exogenous application of osmoprotectants glycine betaine and proline. Environ Exp Bot 59:206–216

    Article  CAS  Google Scholar 

  • Bates LS, Waklren RP (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Bharathkumar S, Jena PP, Kumar J, Baksh SKY, Samal R, Gouda G, Mukherjee M, Donde R, Vijayan J, Parida M, Reddy JN (2016) Identification of new alleles in salt tolerant rice germplasm lines through phenotypic and genotypic screening. Int J Agric Biol 18:441–448

    Article  CAS  Google Scholar 

  • Cai W, Liu W, Wang WS, Fu ZW, Han TT, Lu YT (2015) Overexpression of rat neurons nitric oxide synthase in rice enhances drought and salt tolerance. PLoS One 10:e0131599

    Article  Google Scholar 

  • Carillo P (2018) GABA shunt in durum wheat. Front Plant Sci 9:100

    Article  Google Scholar 

  • Carillo P, Mastrolonardo G, Nacca F, Parisi D, Verlotta A, Fuggi A (2008) Nitrogen metabolism in durum wheat under salinity: accumulation of proline and glycine betaine. Funct Plant Biol 35:412–426

    Article  CAS  Google Scholar 

  • Carillo P, Annunziata MG, Pontecorvo G, Fuggi A, Woodrow P (2011) Salinity stress and salt tolerance. In: Shanker A, Venkateswarlu B (eds) Abiotic stress in plants–mechanisms and adaptations. InTech, Croatia, pp 21–38

    Google Scholar 

  • Chen Z, Cuin TA, Zhou M, Twomey A, Naidu BP (2007) Compatible solute accumulation and stress-mitigating effects in barley genotypes contrasting in their salt tolerance. J Exp Bot 58(15–16):4245–4255

    Article  CAS  Google Scholar 

  • Chen JQ, Meng XP, Zhang Y, Xia M, Wang XP (2008) Overexpression of OsDREB genes lead to enhanced drought tolerance in rice. Biotechnol Lett 30:2191–2198

    Article  Google Scholar 

  • Chunthaburee S, Dongsansuk A, Sanitchon J, Pattanagul W, Theerakulpisut P (2016) Physiological and biochemical parameters for evaluation and clustering of rice cultivars differing in salt tolerance at seedling stage. Saudi J Biol Sci 23:467–477

    Article  CAS  Google Scholar 

  • Darwish E, Testerink C, Khalil M, El-Shihy O, Munnik T (2009) Phospholipid signalling responses in salt-stressed rice leaves. Plant Cell Physiol 50(5):986–997

    Article  CAS  Google Scholar 

  • Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19:371–379

    Article  CAS  Google Scholar 

  • Djanaguiraman M, Prasad PV, Seppanen M (2010) Selenium protects sorghum leaves from oxidative damage under high temperature stress by enhancing antioxidant defense system. Plant Physiol Biochem 48(12):999–1007

    Article  CAS  Google Scholar 

  • El-Bassiouny HMS, Bekheta MA (2005) Effect of salt stress on relative water content, lipid peroxidation, polyamines, amino acids and ethylene of two wheat cultivars. Int J Agric Biol 7(3):363–368

    CAS  Google Scholar 

  • Fageria NK, Stone LF, Santos ABD (2012) Breeding for salinity tolerance. In: Fritsche-Neto R, Borém A (eds) Plant breeding for abiotic stress tolerance. Springer-Verlag, Berlin, pp 103–122

    Chapter  Google Scholar 

  • Fukuda A, Nakamura A, Tagiri A, Tanaka H, Miyao A, Hirochika H, Tanaka Y (2004) Function, intracellular localization and the importance in salt tolerance of a vacuolar Na+/H+ antiporter from rice. Plant Cell Physiol 45(2):146–159

    Article  CAS  Google Scholar 

  • Ghars MA, Parre E, Debez A, Bordenave M, Richard L (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  CAS  Google Scholar 

  • Gong HJ, Randall DP, Flowers TJ (2006) Silicon deposition in the root reduces sodium uptake in rice (Oryza sativa L.) seedlings by reducing bypass flow. Plant Cell Environ 29:1970–1979

    Article  CAS  Google Scholar 

  • Hare PD, Cress WA (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul 21:79–102

    Article  CAS  Google Scholar 

  • Hasegawa PM (2013) Sodium (Na+) homeostasis and salt tolerance of plants. Environ Exp Bot 92:19–31

    Article  CAS  Google Scholar 

  • Hauser F, Horie T (2010) A conserved primary salt tolerance mechanism mediated by HKT transporters: a mechanism for sodium exclusion and maintenance of high K+/Na+ ratio in leaves during salinity stress. Plant Cell Environ 33:552–565

    Article  CAS  Google Scholar 

  • Hirayama T, Shinozaki K (2010) Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant J 61:1041–1052

    Article  CAS  Google Scholar 

  • Hoai NTT, Shim IS, Kobayashi K, Kenji U (2003) Accumulation of some nitrogen compounds in response to salt stress and their relationships with salt tolerance in rice (Oryza sativa L.) seedlings. Plant Growth Regul 41:159–164

    Article  CAS  Google Scholar 

  • Horie T, Costa A, Kim TH, Han MJ, Horie R, Leung HY, Miyao A, Hirochika H, An G, Schroeder JI (2007) Rice OsHKT2;1 transporter mediates large Na+ influx component into K+-starved roots for growth. EMBO J 26:3003–3014

    Article  CAS  Google Scholar 

  • Jamil M, Lee DB, Jung KY, Ashraf M, Lee SC, Rhal ES (2006) Effect of salt (NaCl) stress on germination and early seedling growth of four vegetables species. J Cent Eur Agric 7:273–282

    Google Scholar 

  • Joseph B, Jini D, Sujatha S (2010) Biological and physiological perspectives of specificity in abiotic salt stress response from various rice plants. Asian J Agric Sci 2:99–105

    Google Scholar 

  • Krishnamurthy P, Ranathunge R, Nayak S, Schreiber L, Mathew MK (2011) Root barriers block Na+ traffic to shoots in rice (Oryza sativa L.). J Exp Bot 62:4215–4228

    Article  CAS  Google Scholar 

  • Lawlor D (2013) Genetic engineering to improve plant performance under drought. J Exp Bot 64:83–108

    Article  CAS  Google Scholar 

  • Li Z, Yu J, Peng Y, Huang B (2016) Metabolic pathways regulated by γ-aminobutyric acid (GABA) contributing to heat tolerance in creeping bentgrass (Agrostis stolonifera). Sci Rep 6:30338

    Article  CAS  Google Scholar 

  • Liao YD, Lin KH, Chen CC (2016) Oryza sativa protein phosphatase 1a (OsPP1a) involved in salt stress tolerance in transgenic rice. Mol Breed 36:22

    Article  Google Scholar 

  • Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought-and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406

    Article  CAS  Google Scholar 

  • Mallikarjuna G, Mallikarjuna K, Reddy MK, Kaul T (2011) Expression of OsDREB2A transcription factor confers enhanced dehydration and salt stress tolerance in rice (Oryza sativa L.). Biotechnol Lett 33:1689–1697

    Article  CAS  Google Scholar 

  • Martinez-Atienza J, Jiang X, Garciadeblas B, Mendoza I, Zhu JK, Pardo JM (2007) Conservation of the salt overly sensitive pathway in rice. Plant Physiol 143:1001–1012

    Article  CAS  Google Scholar 

  • Matsukura S, Mizoi J, Yoshida T, Todaka D, Ito Y, Maruyama K, Shinozaki K, Yamaguchi-Shinozaki K (2010) Comprehensive analysis of rice DREB2-type genes that encode transcription factors involved in the expression of abiotic stress-responsive genes. Mol Gen Genomics 283:185–196

    Article  CAS  Google Scholar 

  • Mishra P, Bhoomika K, Dubey RS (2011) Differential responses of antioxidative defense system to prolonged salinity stress in salt-tolerant and salt-sensitive Indica rice (Oryza sativa L.) seedlings. Protoplasma 250:3–19

    Article  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  CAS  Google Scholar 

  • Munns R, James RA, Xu B, Athman A, Conn SJ, Jordans C, Byrt CS, Hare RA, Tyerman SD, Tester M (2012) Wheat grain yield on saline soils is improved by an ancestral Na+ transporter gene. Nat Biotechnol 30:360–364

    Article  CAS  Google Scholar 

  • Nawaz K, Talat AI, Hussain K, Majeed A (2010) Induction of salt tolerance in two cultivars of sorghum (Sorghum bicolor L.) by exogenous application of proline at seedling stage. World Appl Sci J 10:93–99

    CAS  Google Scholar 

  • Negrão S, Schmöckel SM, Tester M (2017) Evaluating physiological responses of plants to salinity stress. Ann Bot 119:1–11

    Article  Google Scholar 

  • Oh SJ, Kim YS, Kwon CW, Park HK, Jeong JS, Kim JK (2009) Overexpression of the transcription factor AP37 in rice improves grain yield under drought conditions. Plant Physiol 150:1368–1379

    Article  CAS  Google Scholar 

  • Pandit A, Rai V, Sharma TR, Sharma PC, Singh NK (2011) Differentially expressed genes in sensitive and tolerant rice varieties in response to salt stress. J Plant Biochem Biotechnol 20:149–154

    Article  CAS  Google Scholar 

  • Passaia G, Spagnolo FL, Caverzan A, Jardim-Messeder D, Christoff AP, Gaeta ML, de Araujo Mariath JE, Margis R, Margis-Pinheiro M (2013) The mitochondrial glutathione peroxidase GPX3 is essential for H2O2 homeostasis and root and shoot development in rice. Plant Sci 208:93–101

    Article  CAS  Google Scholar 

  • Premachandra GS, Saneoka H, Ogata S (1990) Cell membrane stability an indicator of drought tolerance as affected by applied N in soybean. J Agric Sci 115:63–66

    Article  CAS  Google Scholar 

  • Shi H, Quintero FJ, Pardo JM, Zhu JK (2002) The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. Plant Cell 14:465–477

    Article  CAS  Google Scholar 

  • Singh J, Singh V, Sharma PC (2018) Elucidating the role of osmotic, ionic and major salt responsive transcript components towards salinity tolerance in contrasting chickpea (Cicer arietinum L.) genotypes. Physiol Mol Biol Plants 24(3):441–453. https://doi.org/10.1007/s12298-018-0517-4

    Article  CAS  PubMed  Google Scholar 

  • Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants, H2O2 accumulation in papillae and hypersensitive response during barley-powdery mildew interaction. Plant J 11:1187–1194

    Article  CAS  Google Scholar 

  • Turhan H, Genc L, Smith SE, Bostanci YB, Turkmen OS (2008) Assessment of the effect of salinity on the early growth stage of the common sunflower using spectral discrimination techniques. Afr J Biotechnol 7(6):750–756

    Google Scholar 

  • Wang H, Zhang M, Guo R, Shi D, Liu B, Lin X, Yang C (2012) Effects of salt stress on ion balance and nitrogen metabolism of old and young leaves in rice (Oryza sativa L.). BMC Plant Biol 12:194

    Article  Google Scholar 

  • Wang R, Jing W, Xiao L, Jin Y, Shen L, Zhang W (2015) The rice high-affinity potassium transporter1;1 is involved in salt tolerance and regulated by an MYB-type transcription factor. Plant Physiol 168:1076–1090

    Article  CAS  Google Scholar 

  • Widodo JHP, Newbigin E, Tester M, Bacic A (2009) Metabolic responses to salt stress of barley (Hordeum vulgare L.) cultivars, Sahara and Clipper, which differ in salt tolerance. J Exp Bot 60:4089–4103

    Article  CAS  Google Scholar 

  • Woodrow P, Ciarmiello L, Annunziata MG, Pacifico S, Iannuzzi F, Mirto A, D’Amelia L, Dell’Aversana E, Piccolella S, Fuggi A, Carillo P (2017) Durum wheat seedling responses to simultaneous high light and salinity involve a fine reconfiguration of amino acids and carbohydrate metabolism. Physiol Plant 159(3):290–312

    Article  CAS  Google Scholar 

  • Wu D, Cai S, Chen M, Ye L, Chen Z, Zhang H (2013) Tissue metabolic responses to salt stress in wild and cultivated barley. PLoS One 8:e55431

    Article  CAS  Google Scholar 

  • Yang Q, Chen ZZ, Zhou XF, Yin HB, Li X, Xin XF, Hong XH, Zhu JK, Gong Z (2009) Overexpression of SOS (salt overly sensitive) genes increases salt tolerance in transgenic Arabidopsis. Mol Plant 2:22–31

    Article  CAS  Google Scholar 

  • Yoshida S, Forno DA, Cock JH, Gomez KA (1976) Laboratory manual for physiological studies of rice. International Rice Research Institute, Laos Banos

    Google Scholar 

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Authors and Affiliations

  1. ICAR-Central Soil Salinity Research Institute, Karnal, Haryana, 132001, India

    Vijayata Singh, Jogendra Singh, Vineeth T. V. & P. C. Sharma

  2. National Institute of Plant Genome Research, New Delhi, 110 067, India

    Ajit Pal Singh, Jyoti Bhadoria & Jitender Giri

Authors
  1. Vijayata Singh
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  2. Ajit Pal Singh
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  3. Jyoti Bhadoria
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  4. Jitender Giri
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  5. Jogendra Singh
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  6. Vineeth T. V.
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  7. P. C. Sharma
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Correspondence to Vijayata Singh.

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Singh, V., Singh, A.P., Bhadoria, J. et al. Differential expression of salt-responsive genes to salinity stress in salt-tolerant and salt-sensitive rice (Oryza sativa L.) at seedling stage. Protoplasma 255, 1667–1681 (2018). https://doi.org/10.1007/s00709-018-1257-6

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