Abstract
Rice is one of the glycophytes and its yield and grain quality is threatened by salinity. During the past decades, great progresses have been made on molecular mechanisms of rice dealing with salt stress. Taking advantage of genetics, transcriptome studies, and forward genetics, hundreds of genes involved in salt tolerance or salt stress response have been identified. According to their functions, these genes could be divided into at least three types: signaling components, transcriptional factors, and downstream functional molecules including transporters, enzymes for compatible solute synthesis, and ROS scavengers. Based on these knowledges and those obtained from Arabidopsis thaliana, this review summarizes these findings and tries to draw a rough picture of the gene networks controlling salt tolerance of rice.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Almeida DM, Gregorio GB, Oliveira MM, Saibo NJ (2017) Five novel transcription factors as potential regulators of OsNHX1 gene expression in a salt tolerant rice genotype. Plant Mol Biol 93:61–77
Al-Tamimi N, Brien C, Oakey H, Berger B, Saade S, Ho YS, Schmöckel SM, Tester M, Negrão S (2016) Salinity tolerance loci revealed in rice using high-throughput non-invasive phenotyping. Nat Commun 7:13342
Amin US, Biswas S, Elias SM, Razzaque S, Haque T, Malo R, Seraj ZI (2016) Enhanced salt tolerance conferred by the complete 2.3 kb cDNA of the rice vacuolar Na(+)/H(+) antiporter gene compared to 1.9 kb coding region with 5′ UTR in transgenic lines of rice. Front Plant Sci 7:14
Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285:1256–1258
Apse MP, Sottosanto JB, Blumwald E (2003) Vacuolar cation/H+ exchange, ion homeostasis, and leaf development are altered in a T-DNA insertional mutant of AtNHX1, the Arabidopsis vacuolar Na+/H+ antiporter. Plant J Cell Mol Biol 36:229–239
Asano T, Hakata M, Nakamura H, Aoki N, Komatsu S, Ichikawa H, Hirochika H, Ohsugi R (2011) Functional characterisation of OsCPK21, a calcium-dependent protein kinase that confers salt tolerance in rice. Plant Mol Biol 75:179–191
Asano T, Hayashi N, Kobayashi M, Aoki N, Miyao A, Mitsuhara I, Ichikawa H, Komatsu S, Hirochika H, Kikuchi S et al (2012) A rice calcium-dependent protein kinase OsCPK12 oppositely modulates salt-stress tolerance and blast disease resistance. Plant J Cell Mol Biol 69:26–36
Barberon M, Vermeer JEM, De Bellis D, Wang P, Naseer S, Andersen TG, Humbel BM, Nawrath C, Takano J, Salt DE, Geldner N (2016) Adaptation of root function by nutrient-induced plasticity of endodermal differentiation. Cell 164(3):447–459
Bohnert HJ, Nelson DE, Jensen RG (1995) Adaptations to environmental stresses. Plant Cell 7:1099–1111
Boursiac Y, Chen S, Luu DT, Sorieul M, van den Dries N, Maurel C (2005) Early effects of salinity on water transport in Arabidopsis roots. Mol Cell Features Aquaporin Expr Plant Physiol 139:790–805
Boursiac Y, Boudet J, Postaire O, Luu DT, Tournaire-Roux C, Maurel C (2008) Stimulus-induced downregulation of root water transport involves reactive oxygen species-activated cell signalling and plasma membrane intrinsic protein internalization. Plant J Cell Mol Biol 56:207–218
Campbell MT, Bandillo N, Al Shiblawi FRA, Sharma S, Liu K, Du Q, Schmitz AJ, Zhang C, Very AA, Lorenz AJ et al (2017) Allelic variants of OsHKT1;1 underlie the divergence between indica and japonica subspecies of rice (Oryza sativa) for root sodium content. PLoS Genet 13:e1006823
Chao DY, Luo YH, Shi M, Luo D, Lin HX (2005) Salt-responsive genes in rice revealed by cDNA microarray analysis. Cell Res 15:796–810
Chen JQ, Meng XP, Zhang Y, Xia M, Wang XP (2008) Over-expression of OsDREB genes lead to enhanced drought tolerance in rice. Biotechnol Lett 30:2191–2198
Chen G, Hu Q, Luo L, Yang T, Zhang S, Hu Y, Yu L, Xu G (2015) Rice potassium transporter OsHAK1 is essential for maintaining potassium-mediated growth and functions in salt tolerance over low and high potassium concentration ranges. Plant Cell Environ 38:2747–2765
Chen ZC, Yamaji N, Horie T, Che J, An G, Ma JF, Li J (2017) A magnesium transporter OsMGT1 plays a critical role in salt tolerance in rice. Plant Physiol 174:1837–1849
Cheung MY, Li MW, Yung YL, Wen CQ, Lam HM (2013) The unconventional P-loop NTPase OsYchF1 and its regulator OsGAP1 play opposite roles in salinity stress tolerance. Plant Cell Environ 36:2008–2020
Chinnusamy V, Ohta M, Kanrar S, Lee BH, Hong X, Agarwal M, Zhu JK (2003) ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev 17:1043–1054
Choi H, Hong J, Ha J, Kang J, Kim SY (2000) ABFs, a family of ABA-responsive element binding factors. J Biol Chem 275:1723–1730
Conklin PL, Norris SR, Wheeler GL, Williams EH, Smirnoff N, Last RL (1999) Genetic evidence for the role of GDP-mannose in plant ascorbic acid (vitamin C) biosynthesis. Proc Natl Acad Sci U S A 96:4198–4203
Cui LG, Shan JX, Shi M, Gao JP, Lin HX (2015) DCA1 acts as a transcriptional co-activator of DST and contributes to drought and salt tolerance in rice. PLoS Genet 11:e1005617
Cui Y, Wang M, Zhou H, Li M, Huang L, Yin X, Zhao G, Lin F, Xia X, Xu G (2016) OsSGL, a novel DUF1645 domain-containing protein, confers enhanced drought tolerance in transgenic rice and Arabidopsis. Front Plant Sci 7:2001
Dai X, Xu Y, Ma Q, Xu W, Wang T, Xue Y, Chong K (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
Das-Chatterjee A, Goswami L, Maitra S, Dastidar KG, 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
Dubouzet JG, Sakuma Y, Ito Y, Kasuga M, Dubouzet EG, Miura S, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. Plant J Cell Mol Biol 33:751–763
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 45:146–159
Fukuda A, Nakamura A, Hara N, Toki S, Tanaka Y (2011) Molecular and functional analyses of rice NHX-type Na+/H+ antiporter genes. Planta 233:175–188
Gao T, Wu Y, Zhang Y, Liu L, Ning Y, Wang D, Tong H, Chen S, Chu C, Xie Q (2011) OsSDIR1 overexpression greatly improves drought tolerance in transgenic rice. Plant Mol Biol 76:145–156
Garcia AB, Engler J, Iyer S, Gerats T, Van Montagu M, Caplan AB (1997) Effects of osmoprotectants upon NaCl stress in rice. Plant Physiol 115:159–169
Garciadeblas B, Senn ME, Banuelos MA, Rodriguez-Navarro A (2003) Sodium transport and HKT transporters: the rice model. Plant J Cell Mol Biol 34:788–801
Garg AK, Kim JK, Owens TG, Ranwala AP, Choi YD, Kochian LV, Wu RJ (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Natl Acad Sci U S A 99:15898–15903
Gaxiola RA, Rao R, Sherman A, Grisafi P, Alper SL, Fink GR (1999) The Arabidopsis thaliana proton transporters, AtNhx1 and Avp1, can function in cation detoxification in yeast. Proc Natl Acad Sci U S A 96:1480–1485
Gaxiola RA, Li J, Undurraga S, Dang LM, Allen GJ, Alper SL, Fink GR (2001) Drought- and salt-tolerant plants result from overexpression of the AVP1 H+-pump. Proc Natl Acad Sci U S A 98:11444–11449
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
Gevaudant F, Duby G, von Stedingk E, Zhao R, Morsomme P, Boutry M (2007) Expression of a constitutively activated plasma membrane H+-ATPase alters plant development and increases salt tolerance. Plant Physiol 144:1763–1776
Ghosh Dastidar 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-P synthase (PcINO1) from Porteresia coarctata (Roxb.) Tateoka, a halophytic wild rice. Plant Physiol 140:1279–1296
Guiltinan MJ, Marcotte WR Jr, Quatrano RS (1990) A plant leucine zipper protein that recognizes an abscisic acid response element. Science 250:267–271
Guo L, Wang ZY, Lin H, Cui WE, Chen J, Liu M, Chen ZL, Qu LJ, Gu H (2006) Expression and functional analysis of the rice plasma-membrane intrinsic protein gene family. Cell Res 16:277–286
Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499
Hazman M, Hause B, Eiche E, Nick P, Riemann M (2015) Increased tolerance to salt stress in OPDA-deficient rice ALLENE OXIDE CYCLASE mutants is linked to an increased ROS-scavenging activity. J Exp Bot 66:3339–3352
Hong Y, Zhang H, Huang L, Li D, Song F (2016) Overexpression of a stress-responsive NAC transcription factor gene ONAC022 improves drought and salt tolerance in Rice. Front Plant Sci 7:4
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
Horie T, Kaneko T, Sugimoto G, Sasano S, Panda SK, Shibasaka M, Katsuhara M (2011) Mechanisms of water transport mediated by PIP aquaporins and their regulation via phosphorylation events under salinity stress in barley roots. Plant Cell Physiol 52:663–675
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 U S A 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 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
Hubbs AF, Benkovic SA, Miller DB, O’Callaghan JP, Battelli L, Schwegler-Berry D, Ma Q (2007) Vacuolar leukoencephalopathy with widespread astrogliosis in mice lacking transcription factor Nrf2. Am J Pathol 170:2068–2076
Ismail AM, Horie T (2017) Genomics, physiology, and molecular breeding approaches for improving salt tolerance. Annu Rev Plant Biol 68:405–434
Ito Y, Katsura K, Maruyama K, Taji T, Kobayashi M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006) Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant Cell Physiol 47:141–153
Jeong JS, Kim YS, Baek KH, Jung H, Ha SH, Do Choi Y, Kim M, Reuzeau C, Kim JK (2010) Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. Plant Physiol 153:185–197
Joshi R, Karan R, Singla-Pareek SL, Pareek A (2016) Ectopic expression of Pokkali phosphoglycerate kinase-2 (OsPGK2-P) improves yield in tobacco plants under salinity stress. Plant Cell Rep 35:27–41
Kawasaki S, Borchert C, Deyholos M, Wang H, Brazille S, Kawai K, Galbraith D, Bohnert HJ (2001) Gene expression profiles during the initial phase of salt stress in rice. Plant Cell 13:889–905
Krishnamurthy P, Ranathunge K, Franke R, Prakash HS, Schreiber L, Mathew MK (2009) The role of root apoplastic transport barriers in salt tolerance of rice (Oryza sativa L.) Planta 230:119–134
Lan WZ, Wang W, Wang SM, Li LG, Buchanan BB, Lin HX, Gao JP, Luan S (2010) A rice high-affinity potassium transporter (HKT) conceals a calcium-permeable cation channel. Proc Natl Acad Sci U S A 107:7089–7094
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 L, Wang F, Yan P, Jing W, Zhang C, Kudla J, Zhang W (2017) A phosphoinositide-specific phospholipase C pathway elicits stress-induced Ca2+ signals and confers salt tolerance to rice. New Phytol 214:1172–1187
Lima-Melo Y, Carvalho FE, Martins MO, Passaia G, Sousa RH, Neto MC, Margis-Pinheiro M, Silveira JA (2016) Mitochondrial GPX1 silencing triggers differential photosynthesis impairment in response to salinity in rice plants. J Integr Plant Biol 58:737–748
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
Liu D, Chen X, Liu J, Ye J, Guo Z (2012) The rice ERF transcription factor OsERF922 negatively regulates resistance to Magnaporthe oryzae and salt tolerance. J Exp Bot 63:3899–3911
Liu J, Zhang C, Wei C, Liu X, Wang M, Yu F, Xie Q, Tu J (2016) The RING finger ubiquitin E3 ligase OsHTAS enhances heat tolerance by promoting H2O2-induced stomatal closure in rice. Plant Physiol 170:429–443
Majee M, Maitra S, Dastidar KG, Pattnaik S, Chatterjee A, Hait NC, Das KP, Majumder AL (2004) A novel salt-tolerant L-myo-inositol-1-phosphate synthase from Porteresia coarctata (Roxb.) Tateoka, a halophytic wild rice: molecular cloning, bacterial overexpression, characterization, and functional introgression into tobacco-conferring salt tolerance phenotype. J Biol Chem 279:28539–28552
Martinez-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
Maser P, Hosoo Y, Goshima S, Horie T, Eckelman B, Yamada K, Yoshida K, Bakker EP, Shinmyo A, Oiki S et al (2002) Glycine residues in potassium channel-like selectivity filters determine potassium selectivity in four-loop-per-subunit HKT transporters from plants. Proc Natl Acad Sci U S A 99:6428–6433
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 Genet Genomics MGG 283:185–196
Maurel C, Verdoucq L, Luu DT, Santoni V (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annu Rev Plant Biol 59:595–624
Nakashima K, Tran LS, Van Nguyen D, Fujita M, Maruyama K, Todaka D, Ito Y, Hayashi N, Shinozaki K, Yamaguchi-Shinozaki K (2007) Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J Cell Mol Biol 51:617–630
Nath K, Poudyal RS, Eom JS, Park YS, Zulfugarov IS, Mishra SR, Tovuu A, Ryoo N, Yoon HS, Nam HG et al (2013) Loss-of-function of OsSTN8 suppresses the photosystem II core protein phosphorylation and interferes with the photosystem II repair mechanism in rice (Oryza sativa). Plant J Cell Mol Biol 76:675–686
Nath M, Yadav S, Kumar Sahoo R, Passricha N, Tuteja R, Tuteja N (2016) PDH45 transgenic rice maintain cell viability through lower accumulation of Na(+), ROS and calcium homeostasis in roots under salinity stress. J Plant Physiol 191:1–11
Nijhawan A, Jain M, Tyagi AK, Khurana JP (2008) Genomic survey and gene expression analysis of the basic leucine zipper transcription factor family in rice. Plant Physiol 146:333–350
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
Pandey N, Ranjan A, Pant P, Tripathi RK, Ateek F, Pandey HP, Patre UV, Sawant SV (2013) CAMTA 1 regulates drought responses in Arabidopsis thaliana. BMC Genomics 14:216
Pons R, Cornejo MJ, Sanz A (2011) Differential salinity-induced variations in the activity of H(+)-pumps and Na(+)/H(+) antiporters that are involved in cytoplasm ion homeostasis as a function of genotype and tolerance level in rice cell lines. Plant Physiol Biochem PPB 49:1399–1409
Qin H, Wang Y, Wang J, Liu H, Zhao H, Deng Z, Zhang Z, Huang R, Zhang Z (2016) Knocking down the expression of GMPase gene OsVTC1-1 decreases salt tolerance of rice at seedling and reproductive stages. PLoS One 11:e0168650
Qiu QS, Guo Y, Dietrich MA, Schumaker KS, Zhu JK (2002) Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad Sci U S A 99:8436–8441
Rabbani MA, Maruyama K, Abe H, Khan MA, Katsura K, Ito Y, Yoshiwara K, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiol 133:1755–1767
Ray S, Patra B, Das-Chatterjee A, Ganguli A, Majumder AL (2010) Identification and organization of chloroplastic and cytosolic L-myo-inositol 1-phosphate synthase coding gene(s) in Oryza sativa: comparison with the wild halophytic rice, Porteresia coarctata. Planta 231:1211–1227
Ren ZH, Gao JP, Li LG, Cai XL, Huang W, Chao DY, Zhu MZ, Wang ZY, Luan S, Lin HX (2005) A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nat Genet 37:1141–1146
Ruan SL, Ma HS, Wang SH, Fu YP, Xin Y, Liu WZ, Wang F, Tong JX, Wang SZ, Chen HZ (2011) Proteomic identification of OsCYP2, a rice cyclophilin that confers salt tolerance in rice (Oryza sativa L.) seedlings when overexpressed. BMC Plant Biol 11:34
Rus A, Baxter I, Muthukumar B, Gustin J, Lahner B, Yakubova E, Salt DE (2006) Natural variants of AtHKT1 enhance Na+ accumulation in two wild populations of Arabidopsis. PLoS Genet 2:e210
Sakuraba Y, Piao W, Lim JH, Han SH, Kim YS, An G, Paek NC (2015) Rice ONAC106 inhibits leaf senescence and increases salt tolerance and tiller angle. Plant Cell Physiol 56:2325–2339
Sakurai J, Ishikawa F, Yamaguchi T, Uemura M, Maeshima M (2005) Identification of 33 rice aquaporin genes and analysis of their expression and function. Plant Cell Physiol 46:1568–1577
Sakurai J, Ahamed A, Murai M, Maeshima M, Uemura M (2008) Tissue and cell-specific localization of rice aquaporins and their water transport activities. Plant Cell Physiol 49:30–39
Sakurai-Ishikawa J, Murai-Hatano M, Hayashi H, Ahamed A, Fukushi K, Matsumoto T, Kitagawa Y (2011) Transpiration from shoots triggers diurnal changes in root aquaporin expression. Plant Cell Environ 34:1150–1163
Schachtman DP, Schroeder JI (1994) Structure and transport mechanism of a high-affinity potassium uptake transporter from higher plants. Nature 370:655–658
Sengupta S, Majumder AL (2010) Porteresia coarctata (Roxb.) Tateoka, a wild rice: a potential model for studying salt-stress biology in rice. Plant Cell Environ 33:526–542
Shen P, Wang R, Jing W, Zhang W (2011) Rice phospholipase Dalpha is involved in salt tolerance by the mediation of H(+)-ATPase activity and transcription. J Integr Plant Biol 53:289–299
Shen Y, Shen L, Shen Z, Jing W, Ge H, Zhao J, Zhang W (2015) The potassium transporter OsHAK21 functions in the maintenance of ion homeostasis and tolerance to salt stress in rice. Plant Cell Environ 38:2766–2779
Shen J, Lv B, Luo L, He J, Mao C, Xi D, Ming F (2017) The NAC-type transcription factor OsNAC2 regulates ABA-dependent genes and abiotic stress tolerance in rice. Sci Rep 7:40641
Shi H, Ishitani M, Kim C, Zhu JK (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci U S A 97:6896–6901
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
Shi CC, Feng CC, Yang MM, Li JL, Li XX, Zhao BC, Huang ZJ, Ge RC (2014) Overexpression of the receptor-like protein kinase genes AtRPK1 and OsRPK1 reduces the salt tolerance of Arabidopsis thaliana. Plant Sci Int J Exp Plant Biol 217–218:63–70
Sobahan MA, Arias CR, Okuma E, Shimoishi Y, Nakamura Y, Hirai Y, Mori IC, Murata Y (2009) Exogenous proline and glycinebetaine suppress apoplastic flow to reduce Na(+) uptake in rice seedlings. Biosci Biotechnol Biochem 73:2037–2042
Song Y, Miao Y, Song CP (2014) Behind the scenes: the roles of reactive oxygen species in guard cells. New Phytol 201:1121–1140
Sun SJ, Guo SQ, Yang X, Bao YM, Tang HJ, Sun H, Huang J, Zhang HS (2010) Functional analysis of a novel Cys2/His2-type zinc finger protein involved in salt tolerance in rice. J Exp Bot 61:2807–2818
Sunarpi H,T, Motoda J, Kubo M, Yang H, Yoda K, Horie R, Chan WY, Leung HY, Hattori K et al (2005) Enhanced salt tolerance mediated by AtHKT1 transporter-induced Na unloading from xylem vessels to xylem parenchyma cells. Plant J Cell Mol Biol 44:928–938
Suzuki K, Yamaji N, Costa A, Okuma E, Kobayashi NI, Kashiwagi T, Katsuhara M, Wang C, Tanoi K, Murata Y et al (2016) OsHKT1;4-mediated Na(+) transport in stems contributes to Na(+) exclusion from leaf blades of rice at the reproductive growth stage upon salt stress. BMC Plant Biol 16:22
Takaqi, Tamiru M, Abe A, Yoshida K, Uemura A, Yaegashi H, Obara T, Oikawa K, Utsushi H, Kanzaki E, Mitsuoka C, Natsume S, Kosugi S, Kanzaki H, Matsumura H, Urasaki N, Kamoun S, Terauchi R (2015) MutMap accelerates breeding of a salt-tolerant rice cultivar. Nat Biotechnol 33:445–449
Takasaki H, Maruyama K, Kidokoro S, Ito Y, Fujita Y, Shinozaki K, Yamaguchi-Shinozaki K, Nakashima K (2010) The abiotic stress-responsive NAC-type transcription factor OsNAC5 regulates stress-inducible genes and stress tolerance in rice. Mol Genet Genomics MGG 284:173–183
Tao Z, Kou Y, Liu H, Li X, Xiao J, Wang S (2011) OsWRKY45 alleles play different roles in abscisic acid signalling and salt stress tolerance but similar roles in drought and cold tolerance in rice. J Exp Bot 62:4863–4874
Tran LS, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, Maruyama K, Fujita M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (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
Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc Natl Acad Sci USA 97:11632–11637
Walia H, Wilson C, Condamine P, Liu X, Ismail AM, Zeng L, Wanamaker SI, Mandal J, Xu J, Cui X et al (2005) Comparative transcriptional profiling of two contrasting rice genotypes under salinity stress during the vegetative growth stage. Plant Physiol 139:822–835
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 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
Wang X, Zhang MM, Wang YJ, Gao YT, Li R, Wang GF, Li WQ, Liu WT, Chen KM (2016) The plasma membrane NADPH oxidase OsRbohA plays a crucial role in developmental regulation and drought-stress response in rice. Physiol Plant 156:421–443
Wu F, Sheng P, Tan J, Chen X, Lu G, Ma W, Heng Y, Lin Q, Zhu S, Wang J et al (2015a) Plasma membrane receptor-like kinase leaf panicle 2 acts downstream of the DROUGHT AND SALT TOLERANCE transcription factor to regulate drought sensitivity in rice. J Exp Bot 66:271–281
Wu H, Ye H, Yao R, Zhang T, Xiong L (2015b) OsJAZ9 acts as a transcriptional regulator in jasmonate signaling and modulates salt stress tolerance in rice. Plant Sci Int J Exp Plant Biol 232:1–12
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
Xu GY, Rocha PS, Wang ML, Xu ML, Cui YC, Li LY, Zhu YX, Xia X (2011) A novel rice calmodulin-like gene, OsMSR2, enhances drought and salt tolerance and increases ABA sensitivity in Arabidopsis. Planta 234:47–59
Yamaguchi-Shinozaki K, Shinozaki K (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6:251–264
Yang Z, Gao Q, Sun C, Li W, Gu S, Xu C (2009) Molecular evolution and functional divergence of HAK potassium transporter gene family in rice (Oryza sativa L.) J Genet Genomics = Yi Chuan Xue Bao 36:161–172
Yang X, Yang YN, Xue LJ, Zou MJ, Liu JY, Chen F, Xue HW (2011) Rice ABI5-Like1 regulates abscisic acid and auxin responses by affecting the expression of ABRE-containing genes. Plant Physiol 156:1397–1409
Yang T, Zhang S, Hu Y, Wu F, Hu Q, Chen G, Cai J, Wu T, Moran N, Yu L et al (2014) The role of a potassium transporter OsHAK5 in potassium acquisition and transport from roots to shoots in rice at low potassium supply levels. Plant Physiol 166:945–959
Ye H, Du H, Tang N, Li X, Xiong L (2009) Identification and expression profiling analysis of TIFY family genes involved in stress and phytohormone responses in rice. Plant Mol Biol 71:291–305
Yeo AR, Yeo ME, Flowers TJ (1987) The contribution of an Apoplastic pathway to sodium uptake by rice roots in saline conditions. J Exp Bot 38:1141–1153
Yu C, Wang L, Xu S, Zeng Y, He C, Chen C, Huang W, Zhu Y, Hu J (2015) Mitochondrial ORFH79 is essential for drought and salt tolerance in rice. Plant Cell Physiol 56:2248–2258
Yuan S, Li Z, Li D, Yuan N, Hu Q, Luo H (2015) Constitutive expression of rice MicroRNA528 alters plant development and enhances tolerance to salinity stress and nitrogen starvation in creeping Bentgrass. Plant Physiol 169:576–593
Zhang H, Cui F, Wu Y, Lou L, Liu L, Tian M, Ning Y, Shu K, Tang S, Xie Q (2015) The RING finger ubiquitin E3 ligase SDIR1 targets SDIR1-INTERACTING PROTEIN1 for degradation to modulate the salt stress response and ABA signaling in Arabidopsis. Plant Cell 27:214–227
Zhang Y, Lan H, Shao Q, Wang R, Chen H, Tang H, Zhang H, Huang J (2016) An A20/AN1-type zinc finger protein modulates gibberellins and abscisic acid contents and increases sensitivity to abiotic stress in rice (Oryza sativa). J Exp Bot 67:315–326
Zheng X, Chen B, Lu G, Han B (2009) Overexpression of a NAC transcription factor enhances rice drought and salt tolerance. Biochem Biophys Res Commun 379:985–989
Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273
Zhu N, Cheng S, Liu X, Du H, Dai M, Zhou DX, Yang W, Zhao Y (2015) The R2R3-type MYB gene OsMYB91 has a function in coordinating plant growth and salt stress tolerance in rice. Plant Sci Int J Exp Plant Biol 236:146–156
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
Acknowledgment
We thank ZR Chen and YQ Gao for proofreading. This work was supported by the National Key Research and Development Program of China (2016FYD0100700) and the Strategic Priority Research Program “Molecular Mechanism of Plant Growth and Development” of the Chinese Academy of Sciences (XDPB0404).
Author information
Authors and Affiliations
Corresponding authors
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2018 Springer Nature Singapore Pte Ltd.
About this chapter
Cite this chapter
Chao, DY., Lin, HX. (2018). The Gene Network That Regulates Salt Tolerance in Rice. In: Sasaki, T., Ashikari, M. (eds) Rice Genomics, Genetics and Breeding. Springer, Singapore. https://doi.org/10.1007/978-981-10-7461-5_16
Download citation
DOI: https://doi.org/10.1007/978-981-10-7461-5_16
Published:
Publisher Name: Springer, Singapore
Print ISBN: 978-981-10-7460-8
Online ISBN: 978-981-10-7461-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)