doi: 10.15389/agrobiology.2013.3.3eng
UDC 633.18:631.522/.524:631.524:[577.2+581.1
ON GENETIC AND PHYSIOLOGICAL MECHANISMS OF SALT RESISTANCE IN RICE Oryza sativa L. (review)
E.M. Kharitonov, Yu.K. Goncharova
All-Russian Institute of Rice, Russian Academy of Agricultural Sciences,
pos. Belozernyi, Krasnodar, 350921 Russia,
e-mail: serggontchar@mail.ru
Received October 22, 2013
The data are summarized on physiological, morphological and phenological traits contributing to salt resistance in Oryza sativa L. At seedling phase, the salt resistance is realized through an excretion of excess amount of salts, or due to their low consumption, or because of concentration of harmful ions in cell compartments, or by changes in stomata functions and regulation of antioxidant systems, as well as by an active growth which allows to decrease salt content in plant tissues. In the resistant genotypes, at the reproductive phase a trend occurs for restriction of salt flow to leaves, next to panicle, flag leaf particularly, and to a panicle itself. Of 12 genes used in plant transgenesis to increase the salt resistance, 4 genes can also increase both cold resistance and drought resistance, and 2 ones increase a resistance to all abiotic stressors, and 6 genes enable the drought and cold resistance. So, under selection for salt resistance, a gene complex is created simultaneously which provides for general increasing an adaptive ability in addition to resistance to specific stress factor.
Keywords: rice, salt-tolerance, phases of development, mechanisms of tolerance.
REFERENCES
1. Rice and problem soils in South and Southeast Asia. IRRI Discussion Paper Series No. 4 /D. Senadhira (ed.). International Rice Research Institute, Manila, Philippines, 1994: 1-2.
2. Ponnamperuma F.N. Evaluation and improvement of lands for wetland rice production. In: Rice and problem soils in South and Southeast Asia. IRRI Discussion Paper Series No. 4 /D. Senadhira (ed.). International Rice Research Institute, Manila, Philippines, 1994: 4-25.
3. Bohnert H.J., Gong Q., Li P., Ma S. Unraveling abiotic stress tolerance mechanisms —getting genomics going. Curr. Opin. Plant. Biol., 2006, 9: 180-188. CrossRef
4. Hirochika H., Guiderdoni E., An G., Hsing Y., Eun M.Y., Han C.D., Upadhyaya N., Ramachandran S., Zhang Q., Pereira A., Sundaresan V., Leung H. Rice mutant resources for gene discovery. Plant Mol. Biol., 2004, 54: 325-334. CrossRef
5. Zhang J., Jia W., Yang J., Ismail A.M. Role of ABA in integrating plant responses to drought and salt stresses. Field Crops Res., 2006, 97: 111-119. CrossRef
6. Singh R.K., Gregorio G.B., Jain R.K. QTL mapping for salinity tolerance in rice. Physiol Mol. Biol. Plants., 2007, 13: 87-99.
7. Singh R.K., Redoña E.D., Refuerzo L. Varietal improvement for abiotic stress tolerance in crop plants: special reference to salinity in rice. In: Abiotic stress adaptation in plants: physiological, molecular and genomic foundation /A. Pareek, S.K. Sopory, H.J. Bohnert et al. (eds). NY, Springer, 2010: 387-415. CrossRef
8. Mackill D.J. Breeding for resistance to abiotic stresses in rice: the value of quantitative trait loci. Proc. Plant breeding. International symposium /K.R. Lamkey, M. Lee (eds.). Blackwell Pub., Ames, IA, 2006: 201-212. CrossRef
9. Munns R., James R., Lauchli A. Approaches to increasing the salt tolerance of wheat and other cereals. J. Exp. Bot., 1999, 5: 1025-1043. CrossRef
10. Pessarakli M., Szabolcs I. Soil salinity and sodicity as particular plant/crop stress factors. In: Handbook of plant and crop stress /M. Pessarakli (ed.). NY, Dekker, 1999: 1-16. CrossRef
11. Obara M., Tamura W., Ebitani T., Yano M., Sato T., Yamaya T. Fine-mapping of qRL6.1, a major QTL for root length of rice seedlings grown under a wide range of NH4+ concentrations in hydroponic conditions Theor. Appl. Genet., 2010, 121:535–547.
12. Grattan S.R., Zeng L., Shannon M.C., Roberts S.R. Rice is more sensitive to salinity than previously thought. Cal. Agric., 2002, 56: 189-195. CrossRef
13. Bhumbla D.R., Abrol I.P. Saline and sodic soils. In: Soils and rice. International Rice Research Institute, Manila, Philippines, 1978: 719-738.
14. Akbar M., Yabuno T., Nakao S. Breeding for saline resistant varieties of rice. I. Variability for salt tolerance among some rice varieties. Jpn. J. Breed., 1972, 22: 277-284. CrossRef
15. Walia H., Wilson C., Condamine P., Liu X., Ismail A.M., Zeng L.H., Wanamaker S.I., Mandal J., Xu J., Cui X.P., Close T.J. Comparative transcriptional profiling of two contrasting rice genotypes under salinity stress during the vegetative growth stage. Plant Physiol., 2005, 139: 822-835. CrossRef
16. Flowers T.J., Yeo A.R. Variability in the resistance of sodium chloride salinity within rice (Oryza sativa L.) varieties. New Phytol., 1981, 88: 363-373. CrossRef
17. Pearson G.A., Bernstein L. Salinity effects at several growth stages of rice. Agron. J., 1959, 51: 654-657.
18. Moradi F., Ismail A.M. Responses of photosynthesis, chlorophyll fluorescence and ROS scavenging system to salt stress during seedling and reproductive stages in rice. Ann. Bot., 2007, 99: 1161-1173. CrossRef
19. Moradi F., Ismail A.M., Gregorio G.B., Egdane J.A. Salinity tolerance of rice during reproductive development and association with tolerance at the seedling stage. Ind. J. Plant Physiol., 2003, 8: 105-116.
20. Yeo A.R., Yeo M.E., Flowers S.A., Flowers T.J. Screening of rice (Oryza sativa L.) genotypes for physiological characters contributing to salinity resistance, and their relationship to overall performance. Theor. Appl. Genet., 1990, 79: 377-384. CrossRef
21. Peng S., Ismail A.M. Physiological basis of yield and environmental adaptation in rice. In: Physiology and biotechnology integration for plant breeding /H.T. Nguyen, A. Blum (eds.). Marcel Dekker, NY, 2004: 83-140. CrossRef
22. Yeo A.R., Flowers T.J. Varietal differences in the toxicity of sodium ions in rice leaves. Physiol. Plant., 1983, 59: 189-195. CrossRef
23. Sexcion F.H., Egdane J.A., Ismail A.M., Sese M.L. Morpho-physiological traits associated with tolerans of salinity during seegling stage in rice (Oryza sativa L.). Phillippine Journal of Crop Science, 2009, 34: 27-37.
24. Goncharova Yu.K., Ivanov A.N. Sel’skokhozyaistvennaya Biologiya [Agricultural Biology], 2006, 5: 92-97.
25. Mcnally K.L., Bruskiewich R., Mackill D., Buell C.R., Leach J.E., Leung H. Sequencing multiple and diverse rice varieties. Connecting whole-genome variation with phenotypes. Plant Physiol., 2006, 141: 26-31. CrossRef
26. Yeo A.R., Flowers T.J. Salinity resistance in rice (Oryza sativa L.) and a pyramiding approach to breeding varieties for saline soils. Aust. J. Plant. Physiol., 1986, 13: 161-173.
27. Garcia A., Rizzo C.A., Uddin J., Bartos S.L., Senadhira D., Flowers T.J., Yeo A.R. 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., 1997, 20: 1167-1174. CrossRef
28. Garciadeblas B., Senn M.E., Banuelos A., Rodriguez-Navarro A. Sodium transport and HKT transporters: the rice model. Plant J., 2003, 34: 788-801. CrossRef
29. Horie T., Schroeder J.I. Sodium transporters in plants: diverse genes and physiological functions. Plant Physiol., 2004, 136: 2457-2462. CrossRef
30. Horie T., Yoshida K., Nakayama H., Yamada K., Oiki S., Shinmyo A. Two types of HKT transporters with different properties of Na+ and K+ transport in Oriza sativa. Plant J., 2001, 27: 115-128.
31. Turan S., Cornish K., Kumar S. Salinity tolerance in plants: breeding and genetic engineering. Australian Journal Crop Science AJCS, 2012, 6(9): 1337-1348.
32. Yao M.Z., Wang J.F., Chen H.Y., Zhai H.Q., Zhang H.S. Inheritance and QTL mapping of salt tolerance in rice. Rice Sci., 2005, 12: 25-32.
33. Chinnusamy V., Jagendorf A., Jian-Kang Z. Understanding and improving salt tolerance in plants. Crop Sci., 2005, 45: 437-448. CrossRef
34. Zhang X., Wang L., Meng H., Wen H., Fan Y., Zhao J. Maize ABP9 enhances tolerance to multiple stresses in transgenic Arabidopsis by modulating ABA signaling and cellular levels of reactive oxygen species. Plant. Mol. Biol., 2011, 75: 365-378. CrossRef
35. Wang Z., Wang J., Bao Y., Wu Y., Zhang H. Quantitative trait loci controlling rice seed germination under salt stress. Euphytica, 2011, 178: 297-307. CrossRef
36. Rodriguez-Navarro A., Rubio F. High-affinity potassium and sodium transport systems in plants. J. Exp. Bot., 2006, 57: 1149-1160. CrossRef
37. Yeo A.R., Flowers S.A., Rao G., Welfare K., Senanayake N., Flowers T.J. 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., 1999, 22: 559-565.
38. Akita S., Cabuslay G.S. Physiological basis of differential response to salinity in rice cultivars. Plant Soil, 1990, 123: 277-294. CrossRef
39. Flowers T.J., Duque E., Hajibagheri M., McGonigle T.P., Yeo A.R. The effect of salinity on the ultrastructure and net photosynthesis of two varieties of rice: further evidence for a cellular component of salt resistance. New Phytol., 1985, 100: 37-43. CrossRef
40. Senadheera P., Singh R.K., Frans J.M. Differentially expressed membrane transporters in rice roots may contribute to cultivar dependent salt tolerance. J. Exp. Bot., 2009 July, 60(9): 2553-2563. CrossRef
41. Schroeder J.I., Ward J.M., Gassmann W. Perspectives on the physiology and structure of inward-rectifying K+ channels in higher plants: biophysical implications for K+ uptake. Annu. Rev. Biophys. Biomol. Struct., 1994, 23: 441-471.
42. Amtmann A., Sanders D. Mechanisms of Na+ uptake by plant cells. Adv. Bot. Res., 1999, 29: 75-112. CrossRef
43. Demidchik V., Tester M. Sodium fluxes through nonselective cation channels in the plasma membrane of protoplasts from Arabidopsis roots. Plant Physiol., 2002, 128: 379-387.
44. Davenport R.J., Tester M. A weakly voltage-dependant, nonselective cation channel mediates toxic sodium influx in wheat. Plant Physiol., 2000, 122: 823-834. CrossRef
45. Edwards J.D., Janda J., Sweeney M.T., Gaikwad A.B., Liu B., Leung H., Galbraith D.W. Development and evaluation of a high-throughput, low-cost genotyping platform based on oligonucleotide microarrays in rice. Plant Methods, 2008, 4: 13. CrossRef
46. Rengel Z. The role of calcium in salt toxicity. Plant Cell Environ., 1992, 15: 625-632. CrossRef
47. Maathuis F.J.M., Filatov V., Herzyk P., Krijger G.C., Axelsen K.B., Chen S., Green B.J., Li Y., Madagan K.L., Sánchez-Fernández R., Forde B.G., Palmgren M.G., Rea P.A., Williams L.E., Sanders D., Amtmann A. Transcriptome analysis of root transporters reveals participation of multiple gene families in the response to cation stress. Plant J., 2003, 35: 675-692. CrossRef
48. Rubio F., Gassmann W., Schroeder J.I. Sodium-driven potassium uptake by the plant potassium transporter HKT1 and mutations conferring salt tolerance. Science, 1995, 270: 1660-1663. CrossRef
49. Laurie S., Feeney K., Maathuis F. J.M., Heard P.J., Brown S.J., Leigh R.A. A role for HKT1 in sodium uptake by wheat roots. Plant J., 2002, 32: 139-149. CrossRef
50. Uozumi N., Kim E.J., Rubio F., Yamaguchi T., Muto S., Tsuboi A., Bakker E.P., Nakamura T., Schroeder J.I. The Arabidopsis HKT1 gene homolog mediates inward Na+ currents in Xenopus laevis oocytes and Na+ uptake in Saccharomyces cerevisiae. Plant Physiol., 2000, 122: 1249-1259. CrossRef
51. Golldack D., Su H., Quigley F., Kamasani U.R., Munoz-Garay C., Balderas E., Popova O.V., Bennett J., Bohnert H.J., Pantoja O. Characterization of a HKT-type transporter in rice as a general alkali cation transporter. Plant J., 2002, 31: 529-542. CrossRef
52. Carden D.E., Walker D.J., Flowers T.J., Miller A.J. Single-cell measurements of the contribution of cytosolic Na+ and K+ to salt tolerance. Plant Physiol., 2003, 131: 676-683. CrossRef
53. Ren Z.H., Gao J.P., Li L.G., Cai X.L., Huang W., Chao D.Y., Zhu M.Z., Wang Z.Y., Luan S., Lin H.X. A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nat. Genet., 2005, 37: 1141-1146. CrossRef
54. Seki M., Okamoto M., Matsui A., Kim J.-M., Kurihara Y., Ishida J., Morosawa T., Kawashima M., Kim T.T., Shinozaki K. Microarray analysis for studying the abiotic stress responses in plants. In: Molecular techniques in crop improvement / S.M. Jain, D.S. Brar (eds.). Springer, 2009: 333-355. CrossRef
55. Berthomieu P., Conejero G., Nublat A., Brackenbury W.J., Lambert C., Savio C., Uozumi N., Oiki S., Yamada K., Cellier F., Gosti F., Simonneau T., Essah P.A., Tester M., Véry A.A., Sentenac H., Casse F. Functional analysis of AtHKT1 in Arabidopsis shows that Na+ recirculation by the phloem is crucial for salt tolerance. EMBO J., 2003, 22: 2004-2014. CrossRef
56. Dionisio-Sese M.L., Tobita S. Effects of salinity on sodium content and photosynthetic responses of rice seedlings differing in salt tolerance. J. Plant Physiol., 2000, 157: 54-58. CrossRef
57. Zheng L., Shannon M.C., Lesch S.M. Timing of salinity stress affecting rice growth and yield components. Agric. Water Manag., 2001, 48: 191-206. CrossRef
58. Ren Z.H., Gao J.P., Li L.G., Cai X.L., Huang W., Chao D.Y., Zhu M.Z., Wang Z.Y., Luan S., Lin H.X. A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nat. Genet., 2005, 37: 1141-1146. CrossRef
59. Thomson M.J., Ocampo M., Egdane J., Rahman M.A., Sajise A.G., Adorada D.L., Tumimbang-Raiz E., Blumwald E., Seraj Z.I., Singh R.K., Gregorio G.B., Ismail A.M. Characterizing the saltol quantitative trait locus for salinity tolerance in rice. Rice, 2010, 3: 148-160. CrossRef
60. Rus A., Yokoi S., Sharkhuu A., Reddy M., Lee B.-H., Matsumoto T.K., Koiwa H., Zhu J.-K., Bressan R.A., Hasegawa P.M. AtHKT1 is a salt tolerance determinant that controls Na+ entry into plant roots. PNAS USA, 2001, 98: 14150-14155. CrossRef
61. Ismail M., Heuer S., Thomson M.J., Wissuwa M. Genetic and genomic approaches to develop rice germplasm for problem soils. Plant. Mol. Biol., 2007, 65(4): 547-570. CrossRef
62. Singhl R.K., Glenn B., Gregoriol K., Jain R.K. QTL mapping for salinity tolerance in rice. Physiol. Mol. Biol. Plant., 2007, 13: 87-99.
63. Kharitonov E.M., Goncharova Yu.K. Sel’skokhozyaistvennaya Biologiya [Agricultural Biology], 2009, 1: 16-20.
