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Understanding Abiotic Stress Tolerance Mechanisms: Recent Studies on Stress Response in Rice
Ji-Ping Gao,
Dai-Yin Chao,
Hong-Xuan Lin,
Ji-Ping Gao
National Key Laboratory of Plant Molecular Genetics, Shanghai Institute of Plant Physiology and Ecology, Shanghai Institute for Biological Sciences, the Chinese Academy of Sciences, Graduate School of the Chinese Academy of Sciences, Shanghai 200032, China
Search for more papers by this authorDai-Yin Chao
National Key Laboratory of Plant Molecular Genetics, Shanghai Institute of Plant Physiology and Ecology, Shanghai Institute for Biological Sciences, the Chinese Academy of Sciences, Graduate School of the Chinese Academy of Sciences, Shanghai 200032, China
Search for more papers by this authorCorresponding Author
Hong-Xuan Lin
National Key Laboratory of Plant Molecular Genetics, Shanghai Institute of Plant Physiology and Ecology, Shanghai Institute for Biological Sciences, the Chinese Academy of Sciences, Graduate School of the Chinese Academy of Sciences, Shanghai 200032, China
*Author for correspondence. Tel: +86 (0)21 5492 4129, +86 (0)21 5492 4132; Fax: +86 (0)21 5492 4015; E-mail: <[email protected]>.Search for more papers by this authorJi-Ping Gao,
Dai-Yin Chao,
Hong-Xuan Lin,
Ji-Ping Gao
National Key Laboratory of Plant Molecular Genetics, Shanghai Institute of Plant Physiology and Ecology, Shanghai Institute for Biological Sciences, the Chinese Academy of Sciences, Graduate School of the Chinese Academy of Sciences, Shanghai 200032, China
Search for more papers by this authorDai-Yin Chao
National Key Laboratory of Plant Molecular Genetics, Shanghai Institute of Plant Physiology and Ecology, Shanghai Institute for Biological Sciences, the Chinese Academy of Sciences, Graduate School of the Chinese Academy of Sciences, Shanghai 200032, China
Search for more papers by this authorCorresponding Author
Hong-Xuan Lin
National Key Laboratory of Plant Molecular Genetics, Shanghai Institute of Plant Physiology and Ecology, Shanghai Institute for Biological Sciences, the Chinese Academy of Sciences, Graduate School of the Chinese Academy of Sciences, Shanghai 200032, China
*Author for correspondence. Tel: +86 (0)21 5492 4129, +86 (0)21 5492 4132; Fax: +86 (0)21 5492 4015; E-mail: <[email protected]>.Search for more papers by this authorSupported by the State Key Basic Research and Development Plan of China (2006CB100100), the Knowledge Innovation Program of the Chinese Academy of Sciences (KSCX2-YW-N-011), the Shanghai Key Basic Research Foundation and Program of Shanghai Subject Chief Scientist (05DJ14008 and 06XD14023).
Publication of this paper is supported by the National Natural Science Foundation of China (30624808).
Abstract
Abiotic stress is the main factor negatively affecting crop growth and productivity worldwide. The advances in physiology, genetics, and molecular biology have greatly improved our understanding of plant responses to stresses. Rice plants are sensitive to various abiotic stresses. In this short review, we present recent progresses in adaptation of rice to salinity, water deficit and submergence. Many studies show that salt tolerance is tightly associated with the ability to maintain ion homeostasis under salinity. Na+ transporter SKC1 unloads Na+ from xylem, plasma membrane Na+/H+ antiporter SOS1 excludes sodium out of cytosol and tonoplast Na+/H+ antiporter NHX1 sequesters Na+ into the vacuole. Silicon deposition in exodermis and endodermis of rice root reduces sodium transport through the apoplastic pathway. A number of transcription factors regulate stress-inducible gene expression that leads to initiating stress responses and establishing plant stress tolerance. Overexpression of some transcription factors, including DREB/CBF and NAC, enhances salt, drought, and cold tolerance in rice. A variant of one of ERF family genes, Sub1A-1, confers immersion tolerance to lowland rice. These findings and their exploitation will hold promise for engineering breeding to protect crop plants from certain abiotic stresses.
References
- Adkins SW, Shiraishi T, McComb JA (1990). Submergence tolerance of rice—a new glasshouse method for the experimental submergence of plants. Physiol. Plant. 80, 642–646.
- Ahmad R, Zaheer SH, Ismail S (1992). Role of silicon in salt tolerance of wheat (Triticum aestivum L.). Plant Sci. 85, 43–50.
- Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P (2002). Development of multicellular organisms. In: B Alberts, A Johnson, J Lewis, M Raff, K Roberts, P Walter, eds. Molecular Biology of the Cell. Garland Science Taylor & Francis Group, New York . pp. 1157–1258.
- Amtmann A, Sanders D (1999). Mechanisms of Na+ uptake by plant cells. Adv. Bot. Res. 29, 76–112.
- Apse MP, Aharon GS, Snedden WA, Blumwald E (1999). Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport i. Arabidopsis. Science 285, 1256–1258.
- Bañuelos MA, Garciadeblás B, Cubero B, Rodríguez-Navarro A (2002). Inventory and functional characterization of the HAK potassium transporters of rice. Plant Physiol. 130, 784–795.
- Berthomieu P, Conéjéro G, Nublat A, Brackenbury WJ, Lambert C, Savio C et al. (2003). Functional analysis of AtHKT1 in Arabidopsis shows that Na+ recirculation by the phloem is crucial for salt tolerance. EMBO J. 22, 2004–2014.
-
Catling D (1992). Rice in Deep Water. Macmillan,
London
.
10.1007/978-1-349-12309-4 Google Scholar
- 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 WQ, Provart NJ, Glazebrook J, Katagiri F, Chang HS, Eulgem T et al. (2002). Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell 14, 559–574.
- Chinnusamy V, Schumaker K, Zhu JK (2004). Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J. Exp. Bot. 55, 225–236.
- Chinnusamy V, Zhu JH, Zhu JK (2006). Gene regulation during cold acclimation in plants. Physiol. Plant. 126, 52–61.
- Das KK, Sarkar RK, Ismail AM (2005). Elongation ability and nonstructural carbohydrate levels in relation to submergence tolerance in rice. Plant Sci. 168, 131–136.
- Dubouzet JG, Sakuma Y, Ito Y, Kasuga M, Dubouzet EG, Miura S 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.
- Epstein E (1972). Mineral Nutrition of Plants: Principles and Perspectives. John Wiley and Sons, New York .
- Epstein E (1973). Mechanisms of ion transport through plant cell membranes. Int. Rev. Cytol. 34, 123–167.
- Epstein E (1999). Silicon. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 641–664.
- Flowers TJ (2004). Improving crop salt tolerance. J. Exp. Bot. 55, 307–319.
- Fowler S, Thomashow MF (2002). Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14, 1675–1690.
- Fu HH, Luan S (1998). AtKUP1: A dual-affinity K+ transporter fro. Arabidopsis. Plant Cell 10, 63–73.
- Fukao T, Xu K, Ronald PC, Bailey-Serres J (2006). A variable cluster of ethylene response factor-like genes regulates metabolic and developmental acclimation responses to submergence in rice. Plant Cell 18, 2021–2034.
- Fukuda A, Nakamura A, Tanaka Y (1999). Molecular cloning and expression of the Na+/H+ exchanger gene i. Oryza sativa. Biochim. Biophys. Acta 1446, 149–155.
- 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.
- Golldack D, Su H, Quigley F, Kamasani UR, Munoz-Garay C, Balderas E et al. (2002). Characterization of a HKT-type transporter in rice as a general alkali cation transporter. Plant J. 31, 529–542.
- Garcia A, Rizzo CA, Ud-din J, Bartos SL, Senadhira D, Flowers TJ et al. (1997). Sodium and potassium transport to the xylem are inherited independently in rice, and the mechanism of sodium: potassium selectivity differs between rice and wheat. Plant Cell Environ. 20, 1167–1174.
- Garciadeblás B, Senn ME, Bañuelos MA, Rodríguez-Navarro A (2003). Sodium transport and HKT transporters: The rice model. Plant J. 34, 788–801.
- 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.
- Haake V, Cook D, Riechmann JL, Pineda O, Thomashow MF, Zhang JZ (2002). Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis. Plant Physiol. 130, 639–648.
- Haro R, Bañuelos MA, Senn ME, Barrero-Gil J, Rodríguez-Navarro A (2005). HKT1 mediates sodium uniport in roots. Pitfalls in the expression of HKT1 in yeast. Plant Physiol. 139, 1495–1506.
- 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.
- Horie T, Yoshida K, Nakayama H, Yamada K, Oiki S, Shinmyo A (2001). Two types of HKT transporters with different properties of Na+ and K+ transport in Oryza sativa. Plant J. 27, 129–138.
- Hu HH, Dai MQ, Yao JL, Xiao BZ, Li XH, Zhang QF et al. (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.
- Ito Y, Katsura K, Maruyama K, Taji T, Kobayashi M, Seki M et al. (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.
- Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998). Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280, 104–106.
- Jackson MB, Ram PC (2003). Physiological and molecular basis of susceptibility and tolerance of rice plants to complete submergence. Ann. Bot. 91, 227–241.
- Kawasaki S, Borchert C, Deyholos M, Wang H, Brazille S, Kawai K et al. (2001). Gene expression profiles during the initial phase of salt stress in rice. Plant Cell 13, 889–905.
- Kiyosue T, Yamaguchi-Shinozaki K, Shinozaki K (1993). Characterization of cDNA for a dehydration-inducible gene that encodes a CLP A, B-like protein in Arabidopsis thaliana L. Biochem. Biophys. Res. Commun. 196, 1214–1220.
- Kochian LV, Lucas WJ (1988). Potassium transport in roots. Adv. Bot. Res. 15, 93–178.
- Lafitte HR, Ismail A, Bennett J (2004). Abiotic stress tolerance in rice for Asia: Progress and the future. In: T Fischer, N Turner, J Angus, L McIntyre, M Robertson, A Borrell, et al. eds. New Directions for a Diverse Planet: Proceedings for the 4th International Crop Science Congress. The Regional Institute Ltd. The proceedings are available online at: http://www.cropscience.org.au/icsc2004.
- Laurie S, Feeney KA, Maathuis FJM, Heard PJ, Brown SJ, Leigh RA (2002). A role for HKT1 in sodium uptake by wheat roots. Plant J. 32, 139–149.
- Liang Y, Chen Q, Liu Q, Zhang W, Ding R (2003). Exogenous silicon (Si) increases antioxidant enzyme activity and reduces lipid peroxidation in roots of salt-stressed barley (Hordeum vulgare L.). J. Plant Physiol. 160, 1157–1164.
- Lin HX, Zhu MZ, Yano M, Gao JP, Liang ZW, Su WA 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 Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K et al. (1998). Two transcription factors, DREB1and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, i. Arabidopsis. Plant Cell 10, 1391–1406.
- Ma JF (2004). Role of silicon in enhancing the resistance of plants to biotic and abiotic stresses. Soil Sci. Plant Nutr. 50, 11–18.
- Ma JF, Tamai K, Yamaji N, Mitani N, Konishi S, Katsuhara M et al. (2006). A silicon transporter in rice. Nature 440, 688–691.
- Maas EV (1990). Crop salt tolerance. In: KK Tanji, ed. Agricultural Salinity Assessment and Management. ASCE Manuals and Reports on Engineering No. 71. American Society of Civil Engineers, New York . pp. 262–304.
- Mackill DJ (1986). Varietal improvement for rainfed lowland rice in South and Southeast Asia: Results of a survey. Progress in Rainfed Lowland Rice. International Rice Research Institute, Manila . pp. 115–144.
- Martinez-Atienza J, Jiang XY, Garciadeblas B, Mendoza I, Zhu JK, Pardo JM et al. (2007). Conservation of the salt overly sensitive pathway in rice. Plant Physiol. 143, 1001–1012.
- Mäser P, Hosoo Y, Goshima S, Horie T, Eckelman B, Yamada K 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. USA 99, 6428–6433.
- Matoh T, Kairusmee P, Takahashi E (1986). Salt-induced damage to rice plants and alleviation effect of silicate. Soil Sci. Plant Nutr. 32, 295–304.
- Medina J, Bargues M, Terol J, Perez-Alonso M, Salinas J (1999). The Arabidopsis CBF gene family is composed of three genes encoding AP2 domain-containing proteins whose expression is regulated by low temperature but not by abscisic acid or dehydration. Plant Physiol. 119, 463–470.
- Mullan DJ, Colmer TD, Francki MG (2007). Arabidopsis-rice-wheat gene orthologues for Na+ transport and transcript analysis in wheat-L. elongatum aneuploids under salt stress. Mol. Genet. Genomics 277, 199–212.
- Nakashima K, Kiyosue T, Yamaguchi-Shinozaki K, Shinozaki K (1997). A nuclear gene, erd1, encoding a chloroplast-targeted Clp protease regulatory subunit homolog is not only induced by water stress but also developmentally up-regulated during senescence i. Arabidopsis thaliana. Plant J. 12, 851–861.
- Oh SJ, Song SI, Kim YS, Jang HJ, Kim SY, Kim M et al. (2005). Arabidopsis CBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth. Plant Physiol. 138, 341–351.
- Ohnishi T, Sugahara S, Yamada T, Kikuchi K, Yoshiba Y, Hirano HY et al. (2005). OsNAC6, a member of the NAC gene family, is induced by various stresses in rice. Genes Genet. Syst. 80, 135–139.
- Olsen AN, Ernst HA, Leggio LL, Skriver K (2005). NAC transcription factors: Structurally distinct, functionally diverse. Trends Plant Sci. 10, 79–87.
- Ooka H, Satoh K, Doi K, Nagata T, Otomo Y, Murakami K et al. (2003). Comprehensive analysis of NAC family genes in Oryza sativa an. Arabidopsis thaliana. DNA Res. 10, 239–247.
- Platten JD, Cotsaftis O, Berthomieu P, Bohnert H, Davenport RJ, Fairbairn DJ et al. (2006). Nomenclature for HKT transporters, key determinants of plant salinity tolerance. Trends Plant Sci. 11, 372–374.
- Rabbani MA, Maruyama K, Abe H, Khan MA, Katsura K, Ito Y et al. (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.
- Ren ZH, Gao JP, Li LG, Cai XL, Huang W, Chao DY et al. (2005). A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nat. Genet. 37, 1141–1146.
- Richmond KE, Sussman M (2003). Got silicon? The non-essential beneficial plant nutrient. Curr. Opin. Plant Biol. 6, 268–272.
- Sakuma Y, Maruyama K, Osakabe Y, Qin F, Seki M, Shinozaki K et al. (2006). Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell 18, 1292–1309.
- Savant NK, Snyder GH, Datnoff LE (1997). Silicon management and sustainable rice production. Adv. Agron. 58, 151–199.
- Setter TL, Ellis M, Laureles EV, Ella ES, Senadhira D, Mishra SB et al. (1997). Physiology and genetics of submergence tolerance in rice. Ann. Bot. 79 (Suppl.), 67–77.
- Simpson SD, Nakashima K, Narusaka Y, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003). Two different novel cis-acting elements of erd1, a clpA homologous Arabidopsis gene function in induction by dehydration stress and dark-induced senescence. Plant J. 33, 259–270.
- Shi HZ, Lee BH, Wu SJ, Zhu JK (2003). Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance i. Arabidopsis thaliana. Nat. Biotechnol. 21, 81–85.
- Shi HZ, 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 HZ, Zhu JK (2002). Regulation of expression of the vacuolar Na+/H+ antiporter gene AtNHX1 by salt stress and abscisic acid. Plant Mol. Biol. 50, 543–550.
- Shu LZ, Liu YH (2001). Effects of silicon on growth of maize seedlings under salt stress. Agro-environmental Protection 20, 38–40.
- Stockinger EJ, Gilmour SJ, Thomashow MF (1997). Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc. Natl. Acad. Sci. USA 94, 1035–1040.
- Sunarpi, Horie T, Motoda J, Kubo M, Yang H, Yoda K et al. (2005). Enhanced salt tolerance mediated by AtHKT1 transporter-induced Na+ unloading from xylem parenchyma cells. Plant J. 44, 928–938.
- Tran LS, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, Maruyama K 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.
- Tester M, Davenport R (2003). Na+ tolerance and Na+ transport in higher plants. Ann. Bot. 91, 503–527.
- Uozumi N, Kim EJ, Rubio F, Yamaguchi T, Muto S, Tsuboi A et al. (2000). The Arabidopsis HKT1 gene homolog mediates inward Na+ currents in Xenopus laevis oocytes and Na+ uptake i. Saccharomyces cerevisiae. Plant Physiol. 122, 1249–1259.
- Véry AA, Sentenac H (2003). Molecular mechanism and regulation of K+ transport in higher plants. Annu. Rev. Plant Biol. 54, 575–603.
- Wu CQ, Hu HH, Zeng Y, Liang DC, Xie KB, Zhang JW et al. (2006). Identification of novel stress-responsive transcription factor genes in rice by cDNA array analysis. J. Integr. Plant Biol. 48, 1216–1224.
- Xu J, Li HD, Chen LQ, Wang Y, Liu LL, He L et al. (2006a). A protein kinase, interacting with two calcineurin B-like proteins, regulates K+ transporter AKT1 in Arabidopsis. Cell 125, 1347–1360.
- Xu KN, Deb R, Mackill DJ (2004). A microsatellite marker and a codominant PCR-based marker for marker-assisted selection of submergence tolerance in rice. Crop Sci. 44, 248–253.
- Xu KN, Mackill DJ (1996). A major locus for submergence tolerance mapped on rice chromosome 9. Mol. Breeding 2, 219–224.
- Xu KN, Xu X, Fukao T, Canlas P, Maghirang-Rodriguez R, Heuer S et al. (2006b). Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature 442, 705–708.
- Yadav R, Flowers TJ, Yeo AR (1996). The involvement of the transpirational bypass flow in sodium uptake by high- and low-sodium-transporting lines of rice developed through intravarietal selection. Plant Cell Environ. 19, 329–336.
- 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.
- Yamaguchi-Shinozaki K, Shinozaki K (2005). Organization of cis- acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends Plant Sci. 10, 88–94.
- Yeo AR, Flowers SA, Rao G, Welfare K, Senanayake N, Flowers TJ (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.
- Zhang HX, Blumwald E (2001). Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nat. Biotechnol. 19, 765–768.
- Zhu JK (2002). Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 53, 247–273.
- Zhu JK (2003). Regulation of ion homeostasis under salt stress. Curr. Opin. Plant Biol. 6, 441–445.
- Zimmermann S, Ehrhardt T, Plesch G, Müller-Röber B (1999). Ion channels in plant signaling. Cell Mol. Life Sci. 55, 183–203.
