Abstract
Key message
This review presents a comprehensive overview of the recent research on rice salt tolerance in the areas of genomics, proteomics, metabolomics and chemical genomics.
Abstract
Salinity is one of the major constraints in rice cultivation globally. Traditionally, rice is a glycophyte except for a few genotypes that have been widely used in salinity tolerance breeding of rice. Both seedling and reproductive stages of rice are considered to be the salt-susceptible stages; however, research efforts have been biased towards improving the understanding of seedling-stage salt tolerance. An extensive literature survey indicated that there have been very few attempts to develop reproductive stage-specific salt tolerance in rice probably due to the lack of salt-tolerant phenotypes at the reproductive stage. Recently, the role of DNA methylation, genome duplication and codon usage bias in salinity tolerance of rice have been studied. Furthermore, the study of exogenous salt stress alleviants in rice has opened up another potential avenue for understanding and improving its salt tolerance. There is a need to not only generate additional genomic resources in the form of salt-responsive QTLs and molecular markers and to characterize the genes and their upstream regulatory regions, but also to use them to gain deep insights into the mechanisms useful for developing tolerant varieties. We analysed the genomic locations of diverse salt-responsive genomic resources and found that rice chromosomes 1–6 possess the majority of these salinity-responsive genomic resources. The review presents a comprehensive overview of the recent research on rice salt tolerance in the areas of genomics, proteomics, metabolomics and chemical genomics, which should help in understanding the molecular basis of salinity tolerance and its more effective improvement in rice.
Similar content being viewed by others
References
Abbasi FM, Komatsu S (2004) A proteomic approach to analyze salt-responsive proteins in rice leaf sheath. Proteomics 4:2072–2081
Abou-Zeid HM, Ismail GS (2018) The role of priming with biosynthesized silver nanoparticles in the response of Triticum aestivum L. to salt stress. Egypt J Bot 58:73–85
Agrawal GK, Agrawal SK, Shibato J, Iwahashi H, Rakwal R (2003) Novel rice MAP kinases OsMSRMK3 and OsWJUMK1 involved in encountering diverse environmental stresses and developmental regulation. Biochem Biophys Res Commun 300:775–783
Ahmadi N, Negrão S, Katsantonis D, Frouin J, Ploux J, Letourmy P, Droc G et al (2011) Targeted association analysis identified japonica rice varieties achieving Na(+)/K(+) homeostasis without the allelic make-up of the salt tolerant indica variety Nona Bokra. Theor Appl Genet 123:881–895
Alamgir A, Ali MY (1999) Effect of salinity on leaf pigments, sugar and protein concentrations and chloroplast ATPase activity of rice (Oryza sativa L.). Bangl J Bot 28:145–149
Almutairi ZM (2016) Influence of silver nano-particles on the salt resistance of tomato (Solanum lycopersicum) during germination. Int J Agric Biol 18:449–457
Asano T, Hayashi N, Kobayashi M, Aoki N, Miyao A, Mitsuhara I, Ichikawa H et al (2012) A rice calcium-dependent protein kinase OsCPK12 oppositely modulates salt-stress tolerance and blast disease resistance. Plant J 69:26–36
Barozai MYK, Kakar AG, Din M (2012) The relationship between codon usage bias and salt resistant genes in Arabidopsis thaliana and Oryza sativa. Pure Appl Biol 1:48–51
Barrera-Figueroa BE, Gao L, Wu Z, Zhou X, Zhu J, Jin H, Liu R et al (2012) High throughput sequencing reveals novel and abiotic stress-regulated microRNAs in the inflorescences of rice. BMC Plant Biol 12:132
Basu S, Roychoudhury A, Sengupta DN (2014) Deciphering the role of various cis-acting regulatory elements in controlling SamDC gene expression in rice. Plant Signal Behav 9:e28391
Benitez LC, da Maia LC, Ribeiro MV, Pegoraro C, Peters JA, de Oliveira AC, Ariano MJ et al (2013) Salt induced change of gene expression in salt sensitive and tolerant rice species. J Agric Sci 5:251–260
Bimpong IK, Manneh B, El-Namaky R, Diaw F, Amoah NKA, Sanneh B, Ghislain K et al (2014) Mapping QTLs related to salt tolerance in rice at the young seedling stage using 384-plex single nucleotide polymorphism SNP, marker sets. Mol Plant Breed 5:47–63
Bohra J, Dörffling H, Dörffling K (1995) Salinity tolerance of rice (Oryza sativa L.) with reference to endogenous and exogenous abscisic acid. J Agron Crop Sci 174:79–86
Botella MA, Rosado A, Bressan RA, Hasegawa PM (2005) Plant adaptive responses to salinity stress. In: Jenks MA, Hasegawa PM (eds) Plant abiotic stress. Wiley-Blackwell, UK, pp 37–70
Boyko A, Kovalchuk I (2011) Genome instability and epigenetic modification–heritable responses to environmental stress? Curr Opin Plant Biol 14:260–266
Cao Y, Wu Y, Zheng Z, Song F (2006) Overexpression of the rice EREBP-like gene OsBIERF3 enhances disease resistance and salt tolerance in transgenic tobacco. Physiol Mol Plant Path 67:202–211
Chatterjee P, Kanagendran A, Samaddar S, Pazouki L, Sa TM, Niinemets Ü (2018a) Inoculation of Brevibacterium linens RS16 in Oryza sativa genotypes enhanced salinity resistance: impacts on photosynthetic traits and foliar volatile emissions. Sci Total Environ 645:721–732
Chatterjee P, Samaddar S, Niinemets Ü, Sa TM (2018b) Brevibacterium linens RS16 confers salt tolerance to Oryza sativa genotypes by regulating antioxidant defense and H+ ATPase activity. Microbiol Res. https://doi.org/10.1016/j.micres.2018.06.007
Chen X, Wang Y, Li J, Jiang A, Cheng Y, Zhang W (2009) Mitochondrial proteome during salt stress-induced programmed cell death in rice. Plant Physiol Biochem 47:407–415
Chen Y, Li F, Ma Y, Chong K, Xu Y (2013) Overexpression of OrbHLH001, a putative helix–loop–helix transcription factor, causes increased expression of AKT1 and maintains ionic balance under salt stress in rice. J Plant Physiol 170:93–100
Cheng Y, Long M (2007) A cytosolic NADP-malic enzyme gene from rice (Oryza sativa L.) confers salt tolerance in transgenic Arabidopsis. Biotechnol Lett 29:1129–1134
Cheng Y, Qi Y, Zhu Q, Chen X, Wang N, Zhao X, Chen H et al (2009) New changes in the plasma-membrane-associated proteome of rice roots under salt stress. Proteomics 9:3100–3114
Choe YH, Kim YS, Kim IS, Bae MJ, Lee EJ, Kim YH, Park HM et al (2013) Homologous expression of γ-glutamylcysteine synthetase increases grain yield and tolerance of transgenic rice plants to environmental stresses. J Plant Physiol 170:610–618
Chowrasia S, Panda AK, Rawal HC, Kaur H, Mondal TK (2018) Identification of jumonjiC domain containing gene family among the Oryza species and their expression analysis in FL478, a salt tolerant rice genotype. Plant Physiol Biochem 130(130):43–53
Comai L, Young K, Till BJ, Reynolds SH, Greene EA, Codomo CA, Enns LC et al (2004) Efficient discovery of DNA polymorphisms in natural populations by Ecotilling. Plant J 37:778–786
Dai X, Xu Y, Ma Q, Xu W, Wang T, Xue Y, Chong K et al (2007) Overexpression of an R1R2R3 MYB gene, OsMYB3R-2, increases tolerance to freezing, drought, and salt stress in transgenic Arabidopsis. Plant Physiol 143:1739–1751
Diédhiou CJ, Popova OV, Dietz KJ, Golldack D (2008) The SNF1-type serine–threonine protein kinase SAPK4 regulates stress-responsive gene expression in rice. BMC Plant Biol 8:49
Dooki AD, Mayer-Posner FJ, Askari H, Zaiee AA, Salekdeh GH (2006) Proteomic responses of rice young panicles to salinity. Proteomics 6:6498–6507
Duan J, Cai W (2012) OsLEA3-2, an abiotic stress induced gene of rice plays a key role in salt and drought tolerance. PLoS ONE 7:e45117
Duan J, Zhang M, Zhang H, Xiong H, Liu P, Ali J, Li J et al (2012) OsMIOX, a myo-inositol oxygenase gene, improves drought tolerance through scavenging of reactive oxygen species in rice (Oryza sativa L.). Plant Sci 196:143–151
Dubouzet JG, Sakuma Y, Ito Y, Kasuga M, Dubouzet EG, Miura S, Seki M et al (2003) OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt-and cold-responsive gene expression. Plant J 33:751–763
Elamawi RM, Bassiouni SM, Elkhoby WM, Zayed BA (2016) Effect of zinc oxide nanoparticles on brown spot disease and rice productivity under saline soil. J Plant Prot Path Mansoura Univ 7:171–181
FAO. (2008) Land and plant nutrition management service. Available at http://www.fao.org/ag/agl/agll/spush
Fathi A, Zahedi M, Torabian S (2017) Effect of interaction between salinity and nanoparticles (Fe2O3 and ZnO) on physiological parameters of Zea mays L. J Plant Nutr 40:2745–2755
Feng Q, Yang C, Lin X, Wang J, Ou X, Zhang C, Chen Y et al (2012) Salt and alkaline stress induced transgenerational alteration in DNA methylation of rice (Oryza sativa). Aust J Crop Sci 6:877–883
Ferreira JL, Azevedo V, Maroco J, Oliveira MM, Santos AP (2015) Salt tolerant and sensitive rice varieties display differential methylome flexibility under salt stress. PLoS ONE 10:e0124060
Fukuda A, Nakamura A, Tagiri A, Tanaka H, Miyao A, Hirochika H, et al (2004) Function, intracellular localization and the importance in salt tolerance of a vacuolar Na+/H+ antiporter from rice. Plant Cell Physiol 45:146–159
Ganguly M, Datta K, Roychoudhury A, Gayen D, Sengupta DN, Datta SK (2012) Overexpression of Rab16A gene in indica rice variety for generating enhanced salt tolerance. Plant Signal Behav 7:502–509
Ganie SA, Mondal TK (2015) Genome-wide development of novel miRNA-based microsatellite markers of rice (Oryza sativa) for genotyping applications. Mol Breed 35:51–61
Ganie SA, Karmakar J, Roychowdhury R, Mondal TK, Dey N (2014) Assessment of genetic diversity in salt-tolerant rice and its wild relatives for ten SSR loci and one allele mining primer of salT gene located on 1st chromosome. Plant Syst Evol 300:1741–1747
Ganie SA, Dey N, Mondal TK (2016) Promoter methylation regulates the abundance of osa-miR393a in contrasting rice genotypes under salinity stress. Funct Integr Genomics 16:1–11
Ganie SA, Pani DR, Mondal TK (2017a) Genome-wide analysis of DUF221 domain-containing gene family in Oryza species and identification of its salinity stress-responsive members in rice. PLoS ONE 12:e0182469
Ganie SA, Debnath AB, Gumi AM, Mondal TK (2017b) Comprehensive survey and evolutionary analysis of genome-wide miRNA genes from ten diploid Oryza species. BMC Genom 18:711
Gao P, Bai X, Yang L, Lv D, Li Y, Cai H, Ji W et al (2010) Over-expression of osa-MIR396c decreases salt and alkali stress tolerance. Planta 231:991–1001
Gao P, Bai X, Yang L, Lv D, Pan X, Li Y, Cai H et al (2011a) osa-MIR393: a salinity-and alkaline stress-related microRNA gene. Mol Biol Rep 38:237–242
Gao T, Wu Y, Zhang Y, Liu L, Ning Y, Wang D, Tong H et al (2011b) OsSDIR1 overexpression greatly improves drought tolerance in transgenic rice. Plant Mol Biol 76:145–156
Ge LF, Chao DY, Shi M, Zhu MZ, Gao JP, Lin HX (2008) Overexpression of the trehalose-6-phosphate phosphatase gene OsTPP1 confers stress tolerance in rice and results in the activation of stress responsive genes. Planta 228:191–201
Ghaffari A, Gharechahi J, Nakhoda B, Salekdeh GH (2014) Physiology and proteome responses of two contrasting rice mutants and their wild type parent under salt stress conditions at the vegetative stage. J Plant Physiol 171:31–44
Gumi AM, Guha PK, Mazumder A, Jayaswal P, Mondal TK (2018) Characterization of OglDREB2A gene from African rice (Oryza glaberrima), comparative analysis and its transcriptional regulation under salinity stress. Biotechnology 8(2):91. https://doi.org/10.1007/s13205-018-1098-1
Guo X, Wu Y, Wang Y, Chen Y, Chu C (2009) OsMSRA4.1 and OsMSRB1.1, two rice plastidial methionine sulfoxide reductases, are involved in abiotic stress responses. Planta 230:227–238
Hakim M, Juraimi AS, Hanafi M, Ismail MR, Selamat A, Rafii M, Latif MA (2014) Biochemical and anatomical changes and yield reduction in rice (Oryza sativa L.) under varied salinity regimes. Biomed Res Int 2014:208584. https://doi.org/10.1155/2014/208584
Hasthanasombut S, Ntui V, Supaibulwatana K, Mii M, Nakamura I (2010) Expression of Indica rice OsBADH1 gene under salinity stress in transgenic tobacco. Plant Biotechnol Rep 4:75–83
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
Hong CY, Hsu YT, Tsai YC, Kao CH (2007) Expression of ASCORBATE PEROXIDASE 8 in roots of rice (Oryza sativa L.) seedlings in response to NaCl. J Exp Bot 58:3273–3283
Hong CY, Chao YY, Yang MY, Cheng SY, Cho SC, Kao CH (2009) NaCl-induced expression of glutathione reductase in roots of rice (Oryza sativa L.) seedlings is mediated through hydrogen peroxide but not abscisic acid. Plant Soil 320:103–115
Horie T, Brodsky DE, Costa A, Kaneko T, Schiavo FL, Katsuhara M, Schroeder JI (2011a) K+ transport by the OsHKT2; 4 transporter from rice with atypical Na+ transport properties and competition in permeation of K+ over Mg2+ and Ca2+ ions. Plant Physiol 156:1493–1507
Horie T, Sugawara M, Okada T, Taira K, Kaothien-Nakayama P, Katsuhara M, Shinmyo A et al (2011b) Rice sodium-insensitive potassium transporter, OsHAK5, confers increased salt tolerance in tobacco BY2 cells. J Biosci Biol 111:346–356
Horie T, Karahara I, Katsuhara M (2012) Salinity tolerance mechanisms in glycophytes: an overview with the central focus on rice plants. Rice 5:11
Hossain MA, Cho JI, Han M, Ahn CH, Jeon JS, An G, Park PB (2010) The ABRE-binding bZIP transcription factor OsABF2 is a positive regulator of abiotic stress and ABA signaling in rice. J Plant Physiol 167:1512–1520
Hu H, Dai M, Yao J, Xiao B, Li X, Zhang Q, Xiong L (2006) Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc Natl Acad Sci USA 103:12987–12992
Hu H, You J, Fang Y, Zhu X, Qi Z, Xiong L (2008) Characterization of transcription factor gene SNAC2 conferring cold and salt tolerance in rice. Plant Mol Biol 67:169–181
Huang J, Yang X, Wang MM, Tang HJ, Ding LY, Shen Y, Zhang HS (2007) A novel rice C2H2-type zinc finger protein lacking DLN-box/EAR-motif plays a role in salt tolerance. Biochem Biophys Acta 1769:220–227
Huang XY, Chao DY, Gao JP, Zhu MZ, Shi M, Lin HX (2009) A previously unknown zinc finger protein, DST, regulates drought and salt tolerance in rice via stomatal aperture control. Genes Dev 23:1805–1817
Huh GH, Damsz B, Matsumoto TK, Reddy MP, Rus AM, Ibeas JI, Narasimhan ML et al (2002) Salt causes ion disequilibrium-induced programmed cell death in yeast and plants. Plant J 29:649–659
Hussein MM, Abou-Baker NH (2018) The contribution of nano-zinc to alleviate salinity stress on cotton plants. R Soc Open Sci 5:171809
Huyen LTN, Cuc LM, Ham L, Khanh T (2013) Introgression the SALTOL QTL into Q5DB, the elite variety of Vietnam using marker-assisted-selection (MAS). Am J Bio Sci 1:80–84
Igarashi Y, Yoshiba Y, Sanada Y, Yamaguchi-Shinozaki K, Wada K, Shinozaki K (1997) Characterization of the gene for Δ1-pyrroline-5-carboxylate synthetase and correlation between the expression of the gene and salt tolerance in Oryza sativa L. Plant Mol Biol 33:857–865
Jain M, Tyagi AK, Khurana JP (2006) Overexpression of putative topoisomerase 6 genes from rice confers stress tolerance in transgenic Arabidopsis plants. FEBS J 273:5245–5260
Jain M, Moharana KC, Shankar R, Kumari R, Garg R (2014) Genomewide discovery of DNA polymorphisms in rice cultivars with contrasting drought and salinity stress response and their functional relevance. Plant Biotechnol J 12:253–264
Jan A, Maruyama K, Todaka D, Kidokoro S, Abo M, Yoshimura E, Shinozaki K et al (2013) OsTZF1, a CCCH-tandem zinc finger protein, confers delayed senescence and stress tolerance in rice by regulating stress-related genes. Plant Physiol 161:1202–1216
Jankangram W, Thammasirirak S, Jones MG, Hartwell J, Theerakulpisut P (2013) Proteomic and transcriptomic analysis reveals evidence for the basis of salt sensitivity in Thai jasmine rice (Oryza sativa L. cv. KDML 105). Afr J Biotechnol 10:16157–16166
Jeong MJ, Lee SK, Kim BG, Kwon TR, Cho WS, Park YT, Lee JO et al (2006) A rice (Oryza sativa L.) MAP kinase gene, OsMAPK44, is involved in response to abiotic stresses. Plant Cell Tissue Org Cult 85:151–160
Jeong JS, Kim YS, Baek KH, Jung H, Ha SH, Choi YD, Kim M et al (2010) Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. Plant Physiol 153:185–197
Jeong DH, Park S, Zhai J, Gurazada SGR, DePaoli E, Meyers BC, Green PJ (2011) Massive analysis of rice small RNAs: mechanistic implications of regulated microRNAs and variants for differential target RNA cleavage. Plant Cell 23:4185–4207
Jiang A, Gan L, Tu Y, Ma H, Zhang J, Song Z, He Y et al (2013a) The effect of genome duplication on seed germination and seedling growth of rice under salt stress. Aust J Crop Sci 7:1814–1821
Jiang SY, Ma A, Ramamoorthy R, Ramachandran S (2013b) Genome-wide survey on genomic variation, expression divergence, and evolution in two contrasting rice genotypes under high salinity stress. Genome Biol Evol 5:2032–2050
Karami A, Sepehri A (2018) Nano titanium dioxide and nitric oxide alleviate salt induced changes in seedling growth, physiological and photosynthesis attributes of barley. Zemdirbyste-Agric 105:123–132
Karan R, DeLeon T, Biradar H, Subudhi PK (2012) Salt stress induced variation in DNA methylation pattern and its influence on gene expression in contrasting rice genotypes. PLoS ONE 7:e40203
Kim JH, Chung BY, Baek MH, Wi SG, Yang DH, Lee MC, Kim JS (2005) Expression of antioxidant isoenzyme genes in rice under salt stress and effects of jasmonic acid and γ-radiation. J Appl Biol Chem 48:1–6
Kong-Ngern K, Daduang S, Wongkham C, Bunnag S, Kosittrakun M, Theerakulpisut P (2005) Protein profiles in response to salt stress in leaf sheaths of rice seedlings. Sci Asia 31:403–408
Kosová K, Vítámvás P, Prášil IT, Renaut J (2011) Plant proteome changes under abiotic stress-Contribution of proteomics studies to understanding plant stress response. J Proteom 74:1301–1322
Kosová K, Vítámvás P, Urban MO, Prášil IT (2013) Plant proteome responses to salinity stress–comparison of glycophytes and halophytes. Funct Plant Biol 40:775–786
Kumar K, Rao KP, Biswas DK, Sinha AK (2011) Rice WNK1 is regulated by abiotic stress and involved in internal circadian rhythm. Plant Signal Behav 6:316–320
Kumar G, Kushwaha HR, Panjabi-Sabharwal V, Kumari S, Joshi R, Karan R, Mittal S et al (2012a) Clustered metallothionein genes are co-regulated in rice and ectopic expression of OsMT1e-P confers multiple abiotic stress tolerance in tobacco via ROS scavenging. BMC Plant Biol 12:107
Kumar G, Kushwaha HR, Purty RS, Kumari S, Singla-Pareek SL, Pareek A (2012b) Cloning, structural and expression analysis of OsSOS2 in contrasting cultivars of rice under salinity stress. Genes Genom Genomics 6:34–41
Kumar R, Mustafiz A, Sahoo KK, Sharma V, Samanta S, Sopory SK, Pareek A et al (2012c) Functional screening of cDNA library from a salt tolerant rice genotype Pokkali identifies mannose-1-phosphate guanyl transferase gene (OsMPG1) as a key member of salinity stress response. Plant Mol Biol 79:555–568
Kumar K, Kumar M, Kim SR, Ryu H, Cho YG (2013) Insights into genomics of salt stress response in rice. Rice 6:27
Kumar V, Singh A, Mithra SA, Krishnamurthy S, Parida SK, Jain S, Tiwari KK et al (2015) Genome-wide association mapping of salinity tolerance in rice (Oryza sativa). DNA Res 22:1–13
Kumari S, Panjabi Sabharwal V, Kushwaha HR, Sopory SK, Singla-Pareek SL, Pareek A (2009) Transcriptome map for seedling stage specific salinity stress response indicates a specific set of genes as candidate for saline tolerance in Oryza sativa L. Funct Integr Genomics 9:109–123
Latha R, Rubia L, Bennett J, Swaminathan (2004) Allele mining for stress tolerance genes in Oryza species and related germplasm. Mol Biotechnol 27:101–108
Lee DG, Park WK, An YJ, Sohn GY, Ha KJ, Kim YH, Bae DW et al (2011a) Proteomics analysis of salt-induced leaf proteins in two rice germplasms with different salt sensitivity. Can J Plant Sci 91:337–349
Lee SK, Kim BG, Kwon TR, Jeong MJ, Park SR, Lee JW, Byun MO et al (2011b) Overexpression of the mitogen-activated protein kinase gene OsMAPK33 enhances sensitivity to salt stress in rice (Oryza sativa L.). J Biosci 36:139–151
Lee YW, Gould BA, Stinchcombe JR (2014) Identifying the genes underlying quantitative traits: a rationale for the QTN programme. AoB Plants 6:plu004
Li HW, Zang BS, Deng XW, Wang XP (2011) Overexpression of the trehalose-6-phosphate synthase gene OsTPS1 enhances abiotic stress tolerance in rice. Planta 234:1007–1018
Li JY, Wang J, Zeigler RS (2014) The 3,000 rice genomes project: new opportunities and challenges for future rice research. GigaScience 3:1
Lin CC, Kao CH (1996) Proline accumulation is associated with inhibition of rice seedling root growth caused by NaCl. Plant Sci 114:121–128
Lin CC, Hsu YT, Kao CH (2002) The effect of NaCl on proline accumulation in rice leaves. Plant Growth Regul 36:275–785
Lin HX, Zhu MZ, Yano M, Gao JP, Liang ZW, Su WA, Hu XH et al (2004) QTLs for Na+ and K+ uptake of the shoots and roots controlling rice salt tolerance. Theor Appl Genet 108:253–260
Liu K, Wang L, Xu Y, Chen N, Ma Q, Li F, Chong K (2007) Overexpression of OsCOIN, a putative cold inducible zinc finger protein, increased tolerance to chilling, salt and drought, and enhanced proline level in rice. Planta 226:1007–1016
Liu WY, Wang MM, Huang J, Tang HJ, Lan HX, Zhang HS (2009) The OsDHODH1 gene is involved in salt and drought tolerance in rice. J Integr Plant Biol 51:825–833
Liu S, Zheng L, Xue Y, Zhang Q, Wang L, Shou H (2010) Overexpression of OsVP1 and OsNHX1 increases tolerance to drought and salinity in rice. J Plant Biol 53:444–452
Liu C, Mao B, Ou S, Wang W, Liu L, Wu Y, Chu C et al (2014) OsbZIP71, a bZIP transcription factor, confers salinity and drought tolerance in rice. Plant Mol Biol 84:19–36
Lu Z, Liu D, Liu S (2007) Two rice cytosolic ascorbate peroxidases differentially improve salt tolerance in transgenic Arabidopsis. Plant Cell Rep 26:1909–1917
Luo D, Niu X, Yu J, Yan J, Gou X, Lu BR, Liu Y (2012) Rice choline monooxygenase (OsCMO) protein functions in enhancing glycine betaine biosynthesis in transgenic tobacco but does not accumulate in rice (Oryza sativa L. ssp. japonica). Plant Cell Rep 31:1625–1635
Ma K, Xiao J, Li X, Zhang Q, Lian X (2009) Sequence and expression analysis of the C3HC4-type RING finger gene family in rice. Gene 444:33–45
Macovei A, Tuteja N (2012) microRNAs targeting DEAD-box helicases are involved in salinity stress response in rice (Oryza sativa L.). BMC Plant Biol. 12:183
Mahakham W, Sarmah AK, Maensiri S, Theerakulpisut P (2017) Nanopriming technology for enhancing germination and starch metabolism of aged rice seeds using phytosynthesized silver nanoparticles. Sci Rep 7:8263
Malakshah SN, Rezaei MH, Heidari M, Salekdeh GH (2007) Proteomics reveals new salt responsive proteins associated with rice plasma membrane. Biosci Biotechnol Biochem 71:2144–2154
Mallikarjuna G, Mallikarjuna K, Reddy M, 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
Martínez-Atienza J, Jiang X, Garciadeblas B, Mendoza I, Zhu JK, Pardo JM, Quintero FJ (2007) Conservation of the salt overly sensitive pathway in rice. Plant Physiol 143:1001–1012
Mishra P, Singh N, Jain A, Jain N, Mishra V, Pushplatha G, Kiran P et al (2018) Identification of cis-regulatory elements associated with salinity and drought stress tolerance in rice from co-expressed gene interaction networks. Bioinformation 14:123–131
Molla KA, Debnath AB, Ganie SA, Mondal TK (2015) Identification and analysis of novel salt responsive candidate gene based SSRs (cgSSRs) from rice (Oryza sativa L.). BMC Plant Biol. 15:122
Møller IM (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Ann Rev Plant Biol 52:561–591
Mondal TK, Ganie SA (2014) Identification and characterization of salt responsive miRNA-SSR markers in rice (Oryza sativa). Gene 535:204–209
Mondal TK, Ganie SA, Debnath AB (2015) Identification of novel and conserved miRNAs from extreme halophyte, Oryza coarctata, a wild relative of rice. PLoS ONE 10:e0140675. https://doi.org/10.1371/journal.pone.0140675
Mondal TK, Rawal HC, Chowrasia S, Varshney D, Panda AK, Mazumdar A, Kaur H, Gaikwad K, Sharma TR, Singh NK (2018a) Draft genome sequence of first monocot-halophytic species Oryza coarctata reveals stress-specific genes. Sci Rep 8:13698. https://doi.org/10.1038/s41598-018-31518-y
Mondal TK, Panda AK, Rawal HC, Sharma TR (2018b) Discovery of microRNA-target modules of African rice (Oryza glaberrima) under salinity stress. Sci Rep 8:570. https://doi.org/10.1038/s41598-017-18206-z
Moons A, Bauw G, Prinsen E, Van Montagu M, Van Der Straeten D (1995) Molecular and physiological responses to abscisic acid and salts in roots of salt-sensitive and salt-tolerant Indica rice varieties. Plant Physiol 107:177–186
Mukherjee K, Choudhury AR, Gupta B, Gupta S, Sengupta DN (2006) An ABRE-binding factor, OSBZ8, is highly expressed in salt tolerant cultivars than in salt sensitive cultivars of indica rice. BMC Plant Biol 6:18
Nahm MY, Kim SW, Yun D, Lee SY, Cho MJ, Bahk JD (2003) Molecular and biochemical analyses of OsRab7, a rice Rab7 homolog. Plant Cell Physiol 44:1341–1349
Nakamura A, Fukuda A, Sakai S, Tanaka Y (2006) Molecular cloning, functional expression and subcellular localization of two putative vacuolar voltage-gated chloride channels in rice (Oryza sativa L.). Plant Cell Physiol 47:32–42
Nakashima K, Tran LSP, Van Nguyen D, Fujita M, Maruyama K, Todaka D, Ito Y et al (2007) Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J 51:617–630
Nam MH, Huh SM, Kim KM, Park WJ, Seo JB, Cho K, Kim DY et al (2012) Comparative proteomic analysis of early salt stress-responsive proteins in roots of SnRK2 transgenic rice. Proteom Sci 10:15
Naqvi S, Raza S, Hyder M, Ozalp C, Oktem H, Yucel M (2009) Sub-cellular distribution of two salt-induced peptides in roots of Oryza sativa L. var Nonabokra. Afr J Biotechnol 8:4613–4617
Naveed SA, Zhang F, Zhang J, Zheng TQ, Meng LJ, Pang YL, Li ZK et al (2018) Identification of QTN and candidate genes for salinity tolerance at the germination and seedling stages in rice by genome-wide association analyses. Sci Rep. https://doi.org/10.1038/s41598-018-24946-3
Negrão S, Courtois B, Ahmadi N, Abreu I, Saibo N, Oliveira M (2011) Recent updates on salinity stress in rice: from physiological to molecular responses. Crit Rev Plant Sci 30:329–377
Negrão S, Cecília Almadanim M, Pires IS, Abreu IA, Maroco J, Courtois B, Gregorio GB et al (2013) New allelic variants found in key rice salt-tolerance genes: an association study. Plant Biotechnol J 11:87–100
Obata T, Kitamoto HK, Nakamura A, Fukuda A, Tanaka Y (2007) Rice shaker potassium channel OsKAT1 confers tolerance to salinity stress on yeast and rice cells. Plant Physiol 144:1978–1985
Ogawa D, Abe K, Miyao A, Kojima M, Sakakibara H, Mizutani M, Morita H et al (2011) RSS1 regulates the cell cycle and maintains meristematic activity under stress conditions in rice. Nat Commun 2:278
Ono A, Izawa T, Chua NH, Shimamoto K (1996) The rab16B promoter of rice contains two distinct abscisic acid-responsive elements. Plant Physiol 112:483–491
Oomen RJ, Benito B, Sentenac H, Rodríguez-Navarro A, Talón M, Véry AA, Domingo C (2012) HKT2; 2/1, a K+-permeable transporter identified in a salt-tolerant rice cultivar through surveys of natural genetic polymorphism. Plant J. 71:750–762
Ouyang S, He S, Liu P, Zhang W, Zhang J, Chen S (2011) The role of tocopherol cyclase in salt stress tolerance of rice (Oryza sativa). Sci China Life Sci 54:181–188
Pani DR, Sarangi SK, Misra RC, Pradhan SK, Subudhi PK, Mondal TK (2013) Performance of rice germplasm (Oryza sativa L.) under coastal saline conditions. J Indian Soc Coast Agric Res 31:1–7
Park GG, Park JJ, Yoon J, Yu SN, An G (2010) A RING finger E3 ligase gene, Oryza sativa Delayed Seed Germination 1 (OsDSG1), controls seed germination and stress responses in rice. Plant Mol Biol 74:467–478
Park JJ, Yi J, Yoon J, Cho LH, Ping J, Jeong HJ, Cho SK et al (2011) OsPUB15, an E3 ubiquitin ligase, functions to reduce cellular oxidative stress during seedling establishment. Plant J 65:194–205
Park HJ, Lee SS, You YN, Yoon DH, Kim BG, Ahn JC, Cho HS (2013) A rice immunophilin gene, OsFKBP16-3, confers tolerance to environmental stress in Arabidopsis and rice. Int J Mol Sci 14:5899–5919
Parker R, Flowers TJ, Moore AL, Harpham NV (2006) An accurate and reproducible method for proteome profiling of the effects of salt stress in the rice leaf lamina. J Exp Bot 57:1109–1118
Platten JD, Egdane JA, Ismail AM (2013) Salinity tolerance, Na+ exclusion and allele mining of HKT1;5 in Oryza sativa and O. glaberrima: many sources, many genes, one mechanism? BMC Plant Biol 13:32
Qiao W, Xiao S, Yu L, Fan LM (2009) Expression of a rice gene OsNOA1 re-establishes nitric oxide synthesis and stress-related gene expression for salt tolerance in Arabidopsis nitric oxide-associated 1 mutant Atnoa1. Environ Exp Bot 65:90–98
Qiu D, Xiao J, Ding X, Xiong M, Cai M, Cao Y, Li X et al (2007) OsWRKY13 mediates rice disease resistance by regulating defense-related genes in salicylate-and jasmonate-dependent signaling. Mol Plant Microbe Interact 20:492–499
Qiu D, Xiao J, Xie W, Liu H, Li X, Xiong L, Wang S (2008) Rice gene network inferred from expression profiling of plants overexpressing OsWRKY13, a positive regulator of disease resistance. Mol Plant 1:538–551
Qiu D, Xiao J, Xie W, Cheng H, Li X, Wang S (2009) Exploring transcriptional signalling mediated by OsWRKY13, a potential regulator of multiple physiological processes in rice. BMC Plant Biol 9:74
Rajendran K, Tester M, Roy SJ (2009) Quantifying the three main components of salinity tolerance in cereals. Plant Cell Environ 32:237–249
Ren ZH, Gao JP, Li LG, Cai XL, Huang W, Chao DY, Zhu MZ et al (2005) A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nat Genet 37:1141
Roy SJ, Tucker EJ, Tester M (2011) Genetic analysis of abiotic stress tolerance in crops. Curr Opin Plant Biol 14:232–239
RoyChoudhury A, Roy C, Sengupta DN (2007) Transgenic tobacco plants overexpressing the heterologous lea gene Rab16A from rice during high salt and water deficit display enhanced tolerance to salinity stress. Plant Cell Rep 26:1839–1859
Ruan CJ, Teixeira, da Silva JA (2011a) Metabolomics: creating new potentials for unraveling the mechanisms in response to salt and drought stress and for the biotechnological improvement of xero-halophytes. Crit Rev Biotechnol 31:153–169
Ruan, S. L., Ma, H. S., Wang, S. H., Fu, Y. P., Xin, Y., Liu, W. Z., Wang, F. et al. (2011b) Proteomic identification of OsCYP2, a rice cyclophilin that confers salt tolerance in rice (Oryza sativa L.) seedlings when overexpressed. BMC Plant Biol. 11, 34
Salekdeh GH, Siopongco J, Wade L, Ghareyazie B, Bennett J (2002) A proteomic approach to analyzing drought-and salt-responsiveness in rice. Field Crops Res 76:199–219
Sarhadi E, Bazargani MM, Sajise AG, Abdolahi S, Vispo NA, Arceta M, Nejad GM et al (2012) Proteomic analysis of rice anthers under salt stress. Plant Physiol Biochem 58:280–287
Schmidt R, Schippers JH, Welker A, Mieulet D, Guiderdoni E, Mueller-Roeber B (2012) Transcription factor OsHsfC1b regulates salt tolerance and development in Oryza sativa ssp japonica. AoB Plants. https://doi.org/10.1093/aobpla/pls011
Schmidt R, Mieulet D, Hubberten HM, Obata T, Hoefgen R, Fernie AR, Fisahn J et al (2013) Salt-responsive ERF1 regulates reactive oxygen species-dependent signaling during the initial response to salt stress in rice. Plant Cell 25:2115–2131
Schröder M, Giermann N, Zrenner R (2005) Functional analysis of the pyrimidine de novo synthesis pathway in solanaceous species. Plant Physiol 138:1926–1938
Senadheera P, Singh R, Maathuis FJ (2009) Differentially expressed membrane transporters in rice roots may contribute to cultivar dependent salt tolerance. J Exp Bot 60:2553–2563
Servin A, Elmer W, Mukherjee A, De la Torre-Roche R, Hamdi H, White JC et al (2015) A review of the use of engineered nanomaterials to suppress plant disease and enhance crop yield. J Nanoparticle Res 17:92
Shen J, Xie K, Xiong L (2010) Global expression profiling of rice microRNAs by one-tube stem-loop reverse transcription quantitative PCR revealed important roles of microRNAs in abiotic stress responses. Mol Genet Genomics 284:477–488
Singha HS, Chakraborty S, Deka H (2014) Stress induced MAPK genes show distinct pattern of codon usage in Arabidopsis thaliana, Glycine max and Oryza sativa. Bioinformation 10:436–442
Smirnoff N (1996) Botanical briefing: the function and metabolism of ascorbic acid in plants. Ann Bot 78:661–669
Soltis DE, Albert VA, Leebens-Mack J, Bell CD, Paterson AH, Zheng C et al (2009) Polyploidy and angiosperm diversification. Am J Bot 96:336–348
Song Y, Zhang C, Ge W, Zhang Y, Burlingame AL, Guo Y (2011) Identification of NaCl stress-responsive apoplastic proteins in rice shoot stems by 2D-DIGE. J Proteom 74:1045–1067
Sultana N, Ikeda T, Itoh R (1999) Effect of NaCl salinity on photosynthesis and dry matter accumulation in developing rice grains. Environ Exp Bot 42:211–220
Sun SJ, Guo SQ, Yang X, Bao YM, Tang HJ, Sun H, Huang J et al (2010) Functional analysis of a novel Cys2/His2-type zinc finger protein involved in salt tolerance in rice. J Exp Bot 61:2807–2818
Sunkar R, Zhou X, Zheng Y, Zhang W, Zhu JK (2008) Identification of novel and candidate miRNAs in rice by high throughput sequencing. BMC Plant Biol 8:25
Takasaki H, Maruyama K, Kidokoro S, Ito Y, Fujita Y, Shinozaki K, Yamaguchi-Shinozaki K et al (2010) The abiotic stress-responsive NAC-type transcription factor OsNAC5 regulates stress-inducible genes and stress tolerance in rice. Mol Genet Genomics 284:173–183
Teixeira FK, Menezes-Benavente L, Galvao VC, Margis R, Margis-Pinheiro M (2006) Rice ascorbate peroxidase gene family encodes functionally diverse isoforms localized in different subcellular compartments. Planta 224:300–314
Thomson MJ, de Ocampo M, Egdane J, Rahman MA, Sajise AG, Adorada DL, Tumimbang-Raiz E et al (2010) Characterizing the Saltol quantitative trait locus for salinity tolerance in rice. Rice 3:148–160
Tilman D, Balzer C, Hill J, Befort BL (2011) Global food demand and the sustainable intensification of agriculture. Proc Natl Acad Sci USA 108:20260–20264
Todaka D, Nakashima K, Shinozaki K, Yamaguchi-Shinozaki K (2012) Toward understanding transcriptional regulatory networks in abiotic stress responses and tolerance in rice. Rice 5:1–9
Tran LS, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, Maruyama K, Fujita M et al (2004) Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell 16:2481–2498
Tu Y, Jiang A, Gan L, Hossain M, Zhang J, Peng B, Xiong Y et al (2014) Genome duplication improves rice root resistance to salt stress. Rice 7:15
Tuteja N (2007) Mechanisms of high salinity tolerance in plants. Methods Enzymol 428:419–438
Uddin MI, Qi Y, Yamada S, Shibuya I, Deng XP, Kwak SS, Kaminaka H et al (2008) Overexpression of a new rice vacuolar antiporter regulating protein OsARP improves salt tolerance in tobacco. Plant Cell Physiol 49:880–890
Ueda A, Kathiresan A, Inada M, Narita Y, Nakamura T, Shi W, Takabe T et al (2004) Osmotic stress in barley regulates expression of a different set of genes than salt stress does. J Exp Bot 55:2213–2218
Ushimaru T, Nakagawa T, Fujioka Y, Daicho K, Naito M, Yamauchi Y, Nonaka H et al (2006) Transgenic Arabidopsis plants expressing the rice dehydroascorbate reductase gene are resistant to salt stress. J Plant Physiol 163:1179–1184
Vaidyanathan R, Kuruvilla S, Thomas G (1999) Characterization and expression pattern of an abscisic acid and osmotic stress responsive gene from rice. Plant Sci 140:21–30
Vaidyanathan H, Sivakumar P, Chakrabarty R, Thomas G (2003) Scavenging of reactive oxygen species in NaCl-stressed rice (Oryza sativa L.)-differential response in salt-tolerant and sensitive varieties. Plant Sci 165:1411–1418
Vannini C, Iriti M, Bracale M, Locatelli F, Faoro F, Croce P, Pirona R et al (2006) The ectopic expression of the rice Osmyb4 gene in Arabidopsis increases tolerance to abiotic, environmental and biotic stresses. Physiol Mol Plant Pathol 69:26–42
Vu HTT, Le DD, Ismail AM, Le HH (2012) Marker-assisted backcrossing (MABC) for improved salinity tolerance in rice (Oryza sativa L.) to cope with climate change in Vietnam. Aust J Crop Sci 6:1649–1654
Wang Q, Guan Y, Wu Y, Chen H, Chen F, Chu C (2008) Overexpression of a rice OsDREB1F gene increases salt, drought, and low temperature tolerance in both Arabidopsis and rice. Plant Mol Biol 67:589–602
Wang X, Wang J, Liu H, Zou D, Zhao H (2013) Influence of natural saline-alkali stress on chlorophyll content and chloroplast ultrastructure of two contrasting rice (Oryza sativa L. japonica) cultivars. Aust J Crop Sci 7:289–292
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
Wani S, Gosal S (2011) Introduction of OsglyII gene into Oryza sativa for increasing salinity tolerance. Biol Plant 55:536–540
Wen FP, Zhang ZH, Bai T, Xu Q, Pan YH (2010) Proteomics reveals the effects of gibberellic acid (GA3) on salt-stressed rice (Oryza sativa L.) shoots. Plant Sci 178:170–175
Wu H, Shabala L, Shabala S, Giraldo JP (2018) Hydroxyl radical scavenging by cerium oxide nanoparticles improves Arabidopsis salinity tolerance by enhancing leaf mesophyll potassium retention. Environ Sci Nano. https://doi.org/10.1039/c8en00323h
Xia K, Wang R, Ou X, Fang Z, Tian C, Duan J, Wang Y et al (2012) OsTIR1 and OsAFB2 downregulation via OsmiR393 overexpression leads to more tillers, early flowering and less tolerance to salt and drought in rice. PLoS ONE 7:e30039
Xiang Y, Tang N, Du H, Ye H, Xiong L (2008) Characterization of OsbZIP23 as a key player of the basic leucine zipper transcription factor family for conferring abscisic acid sensitivity and salinity and drought tolerance in rice. Plant Physiol 148:1938–1952
Xu DQ, Huang J, Guo SQ, Yang X, Bao YM, Tang HJ, Zhang HS (2008) Overexpression of a TFIIIA-type zinc finger protein gene ZFP252 enhances drought and salt tolerance in rice (Oryza sativa L.). FEBS Lett 582:1037–1043
Yadav DK, Tuteja N (2011) Rice G-protein coupled receptor (GPCR): in silico analysis and transcription regulation under abiotic stress. Plant Signal Behav 6:1079–1086
Yan S, Tang Z, Su W, Sun W (2005) Proteomic analysis of salt stress-responsive proteins in rice root. Proteomics 5:235–244
Yang A, Dai X, Zhang WH (2012) A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice. J Exp Bot 63:2541–2556
Yang M, Sun F, Wang S, Qi W, Wang Q, Dong X, Yang J et al (2013) Down-regulation of OsPDCD5, a homolog of the mammalian PDCD5, increases rice tolerance to salt stress. Mol Breed 31:333–346
Yeo A, Flowers S, Rao G, Welfare K, Senanayake N, Flowers T (1999) Silicon reduces sodium uptake in rice (Oryza sativa L.) in saline conditions and this is accounted for by a reduction in the transpirational bypass flow. Plant Cell Environ 22:559–565
Yokotani N, Ichikawa T, Kondou Y, Maeda S, Iwabuchi M, Mori M, Hirochika H et al (2009a) Overexpression of a rice gene encoding a small C2 domain protein OsSMCP1 increases tolerance to abiotic and biotic stresses in transgenic Arabidopsis. Plant Mol Biol 71:391–402
Yokotani N, Ichikawa T, Kondou Y, Matsui M, Hirochika H, Iwabuchi M, Oda K (2009b) Tolerance to various environmental stresses conferred by the salt-responsive rice gene ONAC063 in transgenic Arabidopsis. Planta 229:1065–1075
You J, Zong W, Li X, Ning J, Hu H, Li X, Xiao J et al (2013) The SNAC1-targeted gene OsSRO1c modulates stomatal closure and oxidative stress tolerance by regulating hydrogen peroxide in rice. J Exp Bot 64:569–583
Zang X, Komatsu S (2007) A proteomics approach for identifying osmotic-stress-related proteins in rice. Phytochemistry 68:426–437
Zhang L, Tian LH, Zhao JF, Song Y, Zhang CJ, Guo Y (2009) Identification of an apoplastic protein involved in the initial phase of salt stress response in rice root by two-dimensional electrophoresis. Plant Physiol 149:916–928
Zhang XH, Rao XL, Shi HT, Li RJ, Lu YT (2011) Overexpression of a cytosolic glyceraldehyde-3-phosphate dehydrogenase gene OsGAPC3 confers salt tolerance in rice. Plant Cell Tissue Organ Cult 107:1–11
Zhang S, Haider I, Kohlen W, Jiang L, Bouwmeester H, Meijer AH, Schluepmann H et al (2012) Function of the HD-Zip I gene Oshox22 in ABA-mediated drought and salt tolerances in rice. Plant Mol Biol 80:571–585
Zhao B, Ge L, Liang R, Li W, Ruan K, Lin H, Jin Y (2009) Members of miR-169 family are induced by high salinity and transiently inhibit the NF–YA transcription factor. BMC Mol Biol 10:29
Zhao X, Wang W, Zhang F, Deng J, Li Z, Fu B (2014) Comparative metabolite profiling of Tto rice genotypes with contrasting salt stress tolerance at the seedling stage. PLoS ONE 9:e108020
Zou M, Guan Y, Ren H, Zhang F, Chen F (2008) A bZIP transcription factor, OsABI5, is involved in rice fertility and stress tolerance. Plant Mol Biol 66:675–683
Zou J, Liu C, Liu A, Zou D, Chen X (2012) Overexpression of OsHsp17.0 and OsHsp23. 7 enhances drought and salt tolerance in rice. J Plant Physiol 169:628–635
Zuther E, Koehl K, Kopka J (2007) Comparative metabolome analysis of the salt response in breeding cultivars of rice. In: Jenks MA, Hasegawa PM, Jain SM (eds) Advances in molecular breeding toward drought and salt tolerant crops. Springer, Berlin, pp 285–315
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 Rajeev K. Varshney.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Ganie, S.A., Molla, K.A., Henry, R.J. et al. Advances in understanding salt tolerance in rice. Theor Appl Genet 132, 851–870 (2019). https://doi.org/10.1007/s00122-019-03301-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-019-03301-8