Reliability of ion accumulation and growth components for selecting salt tolerant lines in large populations of rice
Tanveer Ul Haq A D F , Javaid Akhtar B , Katherine A. Steele C , Rana Munns D E and John Gorham C
+ Author Affiliations
- Author Affiliations
A College of Agriculture, PO Box 79, Dera Ghazi Khan 32200, Pakistan.
B Institute of Soil and Environmental Sciences, University of Agriculture, Faisalabad 38040, Pakistan.
C College of Natural Sciences, Bangor University, Deiniol Road, Bangor, Gwynedd, Wales LL57 2UW, UK.
D School of Plant Biology, University of Western Australia, Crawley, WA 6009, Australia.
E CSIRO Plant Industry, GPO Box 1600, Canberra, ACT 2601, Australia.
F Corresponding author. Email: drtanveer@uaf.edu.pk
Functional Plant Biology 41(4) 379-390 https://doi.org/10.1071/FP13158
Submitted: 23 May 2013 Accepted: 21 October 2013 Published: 3 December 2013
Abstract
Ion accumulation and growth under salt stress was studied in two experiments in a rice mapping population derived from parents CO39 and Moroberekan with 4-fold differences in shoot Na+ accumulation. The 120 recombinant inbred lines (RILs) had differences up to 100-fold in Na+. Measurement of ‘salt tolerance’ (biomass production of the RILs in 100 mM NaCl relative to controls) after 42 days showed a 2-fold variation in ‘salt tolerance’ between parents, with five RILs being more tolerant than the more tolerant parent CO39. The reliability of various traits for selecting salt tolerance in large populations was explored by measuring Na+, K+ and K+/Na+ ratios in leaf blades and sheaths after 7 or 21 days of exposure to 100 mM NaCl, and their correlation with various growth components and with leaf injury. The highest correlations were found for Na+ in the leaf blade on day 21 with injury at day 42 in both experiments (r = 0.7). Earlier measurements of Na+ or of injury had lower correlations. The most sensitive growth components were tiller number plant–1 and shoot water content (g water g–1 dry weight), and these were correlated significantly with Na+ and, to a lesser extent, with K+/Na+. These studies showed that exposure for at least 42 days may be needed to clearly demonstrate the beneficial effect of the trait for Na+ exclusion on growth under salinity.
Additional keywords: criteria, HKT transporter, Oryza sativa, potassium, salinity, screening, sodium, tissue tolerance.
References
Asch F, Dingkuhn M, Dorffling K, Miezan K (2000) Leaf K+/Na+ ratio predicts salinity induced yield loss in irrigated rice. Euphytica 113, 109–118.| Leaf K+/Na+ ratio predicts salinity induced yield loss in irrigated rice.Crossref | GoogleScholarGoogle Scholar |
Ashraf M, Harris PJ (2004) Potential biochemical indicators of salinity tolerance in plants. Plant Science 166, 3–16.
| Potential biochemical indicators of salinity tolerance in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltVOqsA%3D%3D&md5=734f5733abd2ab4427c81c4815052494CAS |
Bhumbla DR, Abrol IP (1978) Saline and sodic soils. I ‘Proceedings of the IRRI Symposium on Soils and Rice’. pp. 719–738. (International Rice Research Institute: Manila, Philippines)
Byrt CS, Platten JD, Spielmeyer W, James RA, Lagudah ES, Dennis ES, Tester M, Munns R (2007) HKT1;5-like cation transporters linked to Na+ exclusion loci in wheat, Nax2 and Kna1. Plant Physiology 143, 1918–1928.
| HKT1;5-like cation transporters linked to Na+ exclusion loci in wheat, Nax2 and Kna1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXksFWjurs%3D&md5=9be0d7fa58f201ec8c2022f412737ef3CAS | 17322337PubMed |
Carden DE, Walker DJ, Flowers TJ, Miller AJ (2003) Single-cell measurements of the contributions of cytosolic Na+ and K+ to salt tolerance. Plant Physiology 131, 676–683.
| Single-cell measurements of the contributions of cytosolic Na+ and K+ to salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtlyjs70%3D&md5=765b844d93057ca5162d3b32f491bea4CAS | 12586891PubMed |
Champoux M, Wang G, Sarkarung S, Mackill D, O’Toole J, Huang N, McCouch SR (1995) Locating genes associated with root morphology and drought avoidance in rice via linkage to molecular markers. Theoretical and Applied Genetics 90, 969–981.
| Locating genes associated with root morphology and drought avoidance in rice via linkage to molecular markers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXnsF2rurg%3D&md5=9552e7ad249d981ef53bf4b408eb2d1dCAS | 24173051PubMed |
Chinnusamy V, Jagendorf A, Zhu JK (2005) Understanding and improving salt tolerance in plants. Crop Science 45, 437–448.
| Understanding and improving salt tolerance in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjtVGjur0%3D&md5=12a988d4df27525d140e36680e29c349CAS |
Cotsaftis O, Plett D, Shirley N, Tester M, Hrmova M (2012) A two-staged model of Na+ exclusion in rice explained by 3D modeling of HKT transporters and alternative splicing. PLoS ONE 7, e39865
| A two-staged model of Na+ exclusion in rice explained by 3D modeling of HKT transporters and alternative splicing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVKrsrvM&md5=69ba86efd120a894346aa07d3f4e9ce7CAS | 22808069PubMed |
Davies WJ, Zhang J (1991) Root signals and the regulation of growth and development of plants in drying soil. Annual Review of Plant Physiology and Plant Molecular Biology 42, 55–76.
| Root signals and the regulation of growth and development of plants in drying soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXltFSmsr8%3D&md5=91a7fd4a63e9eb54599c96211ca9e0d2CAS |
Flowers TJ, Yeo AR (1981) Variability in the resistance of sodium chloride salinity within rice varieties. New Phytologist 88, 363–373.
| Variability in the resistance of sodium chloride salinity within rice varieties.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXlt12ksL8%3D&md5=e989af390a6c8b85dee3e99cc6b5c8dfCAS |
Flowers TJ, Troke PF, Yeo AR (1977) The mechanism of salt tolerance in halophytes. Annual Review of Plant Physiology 28, 89–121.
| The mechanism of salt tolerance in halophytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXksFSisb8%3D&md5=ab0a16957d0ffbee896436c71cd4eb84CAS |
Flowers TJ, Hajibagheri MA, Clipson NJW (1986) Halophytes. Quarterly Review of Biology 61, 313–337.
| Halophytes.Crossref | GoogleScholarGoogle Scholar |
Garciadeblás B, Senn ME, Bañuelos MA, Rodríguez-Navarro A (2003) Sodium transport and HKT transporters: the rice model. The Plant Journal 34, 788–801.
| Sodium transport and HKT transporters: the rice model.Crossref | GoogleScholarGoogle Scholar | 12795699PubMed |
Golldack D, Quigley F, Michalowski CB, Kamasani UR, Bohnert HJ (2003) Salinity stress tolerant and sensitive rice (Oryza sativa L.) regulate AKT1-type potassium channel transcripts differently. Plant Molecular Biology 51, 71–81.
| Salinity stress tolerant and sensitive rice (Oryza sativa L.) regulate AKT1-type potassium channel transcripts differently.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnvFOitL0%3D&md5=3a851abf59481dff30c5f2894e3c8c21CAS | 12602892PubMed |
Gorham J, Bridges J, Dubcovsky J, Dvorak J, Hollington PA, Luo MC, Khan JA (1997) Genetic analysis and physiology of a trait for enhanced K+/Na+ discrimination in wheat. New Phytologist 137, 109–116.
| Genetic analysis and physiology of a trait for enhanced K+/Na+ discrimination in wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXns1ynsbs%3D&md5=323f5ca89190f7052b8a0bd031ba9bd3CAS |
Green RE, Cornell SJ, Scharlemann JPW, Balmford A (2005) Farming and the fate of wild nature. Science 307, 550–555.
| Farming and the fate of wild nature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmslOhtg%3D%3D&md5=66fad8ede61d474c6af3d6e2e8881a23CAS | 15618485PubMed |
Gregorio GB, Senadhira D (1993) Genetic analysis of salinity tolerance in rice (Oryza sativa L.). Theoretical and Applied Genetics 86, 333–338.
Gregorio GB, Senadhira D, Mendoza RD (1997) Screening rice for salinity tolerance. IRRI Discussion Paper Series No. 22. International Rice Research Institute, Manila, Philippines.
Ul Haq T, Akhtar J, Gorham J, Steele KA, Khalid M (2008) Genetic mapping of QTLs, controlling shoot fresh and dry weight under salt stress in rice (Oryza sativa L.) cross between CO39 × Moroberekan. Pakistan Journal of Botany 40, 2369–2381.
Ul Haq T, Gorham J, Akhtar J, Akhtar N, Steele KA (2010) Dynamic QTL for salt stress components on chromosome 1 of rice. Functional Plant Biology 37, 634–645.
| Dynamic QTL for salt stress components on chromosome 1 of rice.Crossref | GoogleScholarGoogle Scholar |
Hoagland DR, Arnon DI (1950) The water culture method for growing plant without soil. California Agriculture Experiment Station Circular 347, 39
Horie T, Karahara I, Katsuhara M (2012) Salinity tolerance mechanisms in glycophytes: an overview with the central focus on rice plants. Rice 5, 11
| Salinity tolerance mechanisms in glycophytes: an overview with the central focus on rice plants.Crossref | GoogleScholarGoogle Scholar |
Huang S, Spielmeyer W, Lagudah ES, James RA, Platten JD, Dennis ES, Munns R (2006) A sodium transporter (HKT7) is a candidate for Nax1, a gene for salt tolerance in durum wheat. Plant Physiology 142, 1718–1727.
| A sodium transporter (HKT7) is a candidate for Nax1, a gene for salt tolerance in durum wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlCns7jE&md5=85fd6e12d4d0dfe6e7a9bcfeafb08a21CAS | 17071645PubMed |
James RA, Davenport R, Munns R (2006) Physiological characterization of two genes for Na+ exclusion in wheat: Nax1 and Nax2. Plant Physiology 142, 1537–1547.
| Physiological characterization of two genes for Na+ exclusion in wheat: Nax1 and Nax2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlCns7vI&md5=b71f2e8faf4ee684a7bfb542a1fa883cCAS | 17028150PubMed |
Koyama ML, Levesley A, Koebner RMD, Flowers TJ, Yeo AR (2001) Quantitative trait loci for component physiological traits determining salt tolerance in rice. Plant Physiology 125, 406–422.
| Quantitative trait loci for component physiological traits determining salt tolerance in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjslyls70%3D&md5=440c7a4fdf871325b7b2383e840d5df4CAS | 11154348PubMed |
Lafitte HR, Ismail A, Bennett J (2004) Abiotic stress tolerance in rice for Asia: progress and the future. In ‘New directions for a diverse planet: proceedings for the 4th International Crop Science Congress, Brisbane, Australia, 26 September – 1 October 2004’. (Eds T Fischer, N Turner, J Angus, L McIntyre, M Robertson, A Borrell, D Lloyd) pp. 1–17. (The Regional Institute Ltd: Gosford, NSW) Available at www.cropscience.org.au/icsc2004
Läuchli A, Epstein E (1990) Plant responses to saline and sodic conditions. In ‘Agricultural salinity assessment and management. ASCE Manuals and Reports on Engineering Practice No. 71’. (Ed. KK Tanji) pp. 113–137 (ASCE: New York)
Lawrence WJC, Newell J (1939) ‘Seed and potting composts.’ (Allen & Unwin: London)
Lee KS, Choi WY, Ko JC, Kim TS, Gregoria GB (2003) Salinity tolerance of japonica and indica rice (Oryza sativa L.) at the seedling stage. Planta 216, 1043–1046.
Lin HX, Zhu MZ, Yano M, Gao JP, Liang ZW, Su WA (2004) QTLs for Na+ and K+ uptake of the shoots and roots controlling rice salt tolerance. Theoretical and Applied Genetics 108, 253–260.
| QTLs for Na+ and K+ uptake of the shoots and roots controlling rice salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjtFCntg%3D%3D&md5=4bc9503db22490d84d375c0042550068CAS | 14513218PubMed |
Lutts S, Guerrir G (1995) Peroxidase activities of two rice cultivars differing in salinity tolerance as affected by proline and NaCl. Biologia Plantarum 37, 577–586.
| Peroxidase activities of two rice cultivars differing in salinity tolerance as affected by proline and NaCl.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xot1Ck&md5=66b4d902aa6e00d147e53e670ccdc114CAS |
Lutts S, Kinet JM, Bouharmont J (1995) Changes in plant response to NaCl during development of rice (Oryza sativa L.) varieties differing in salinity resistance. Journal of Experimental Botany 46, 1843–1852.
| Changes in plant response to NaCl during development of rice (Oryza sativa L.) varieties differing in salinity resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XlsFeguw%3D%3D&md5=e49e9b6d66d5a9a32060ef16941987d8CAS |
Martinez-Atienza J, Jiang XY, Garciadeblas B, Mendoza I, Zhu JK, Pardo JM (2007) Conservation of the salt overly sensitive pathway in rice. Plant Physiology 143, 1001–1012.
| Conservation of the salt overly sensitive pathway in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhvFWnt7s%3D&md5=eba3ff4c6bfd5a997c907aac7ae5dac6CAS | 17142477PubMed |
Møller IS, Gilliham M, Jha D, Mayo GM, Roy SJ, Cotes JC, Haseloff J, Tester M (2009) Shoot Na+ exclusion and increased salinity tolerance engineered by cell type-specific alteration of Na+ transport in Arabidopsis. The Plant Cell
| Shoot Na+ exclusion and increased salinity tolerance engineered by cell type-specific alteration of Na+ transport in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 19584143PubMed |
Moradi M, Ismail AM (2007) Responses of photosynthesis, chlorophyll fluorescence and ROS-scavenging systems to salt stress during seedling and reproductive stages in rice. Annals of Botany 99, 1161–1173.
| Responses of photosynthesis, chlorophyll fluorescence and ROS-scavenging systems to salt stress during seedling and reproductive stages in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXot1agtrs%3D&md5=2867458148fe4c534e6240b9e28b0838CAS |
Munns R (1993) Physiological processes limiting plant growth in saline soil: some dogmas and hypotheses. Plant, Cell & Environment 16, 15–24.
| Physiological processes limiting plant growth in saline soil: some dogmas and hypotheses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXks1yjsr0%3D&md5=a884c868738a00c05e702ebf444e38dbCAS |
Munns R (2002) Comparative physiology of salt and water stress. Plant, Cell & Environment 25, 239–250.
| Comparative physiology of salt and water stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xhslakurw%3D&md5=4b241e0ff1eba2f3fa3d1e323ab7e87aCAS |
Munns R (2005) Genes and salt tolerance: bringing them together. New Phytologist 167, 645–663.
| Genes and salt tolerance: bringing them together.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVGisbfP&md5=a2d23c6d5faa06931cb8a05ae3e289bcCAS | 16101905PubMed |
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annual Review of Plant Biology 59, 651–681.
| Mechanisms of salinity tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFaqtrw%3D&md5=0ce1f7aad22c73fffb329d4603f0e836CAS | 18444910PubMed |
Munns R, Schachtman D, Condon A (1995) The significance of a two-phase growth response to salinity in wheat and barley. Functional Plant Biology 22, 561–569.
Munns R, James RA, Läuchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals. Journal of Experimental Botany 57, 1025–1043.
| Approaches to increasing the salt tolerance of wheat and other cereals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xis1GlsrY%3D&md5=e52874acd87072d96bffb5975e10415bCAS | 16510517PubMed |
Munns R, James RA, Xu B, Athman A, Conn SJ, Jordans C, Byrt CS, Hare RA, Tyerman SD, Tester M, Plett D, Gilliham M (2012) Wheat grain yield on saline soils is improved by an ancestral Na+ transporter gene. Nature Biotechnology 30, 360–364.
| Wheat grain yield on saline soils is improved by an ancestral Na+ transporter gene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjtlOgu7w%3D&md5=7c1aaac749903736cdb6d4cad7aba404CAS | 22407351PubMed |
Negrão S, Almadanim MC, Pires IS, Abreu IA, Maroco J, Courtois B, Gregorio GB, McNally KL, Oliveira MM (2013) New allelic variants found in key rice salt-tolerance genes: an association. Plant Biotechnology Journal 11, 87–100.
| New allelic variants found in key rice salt-tolerance genes: an association.Crossref | GoogleScholarGoogle Scholar | 23116435PubMed |
Peng S, Ismail AM (2004) Physiological basis of yield and environmental adaptation in rice. In ‘Physiology and biochemistry integration for plant breeding’. (Eds HT Nguyen, A Blum) pp. 83–140. (Marcel Dekker Inc.: New York)
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 Biology 13, 32
| Salinity tolerance, Na+ exclusion and allele mining of HKT1;5 in Oryza sativa and O. glaberrima: many sources, many genes, one mechanism?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXosVSntr0%3D&md5=21ec1498c6d11a7cd3705ca7ffa5abffCAS | 23445750PubMed |
Plett D, Safwat G, Gilliham M, Møller IS, Roy S, Shirley N, Jacobs A, Johnson A, Tester M (2010) Improved salinity tolerance of rice through cell type-specific expression of AtHKT1;1. PLoS ONE 5, e12571
| Improved salinity tolerance of rice through cell type-specific expression of AtHKT1;1.Crossref | GoogleScholarGoogle Scholar | 20838445PubMed |
Prasad SR, Bagali PG, Hittalmani S, Shashidhar HE (2000) Molecular mapping of quantitative trait loci associated with seedling tolerance to salt stress in rice (Oryza sativa L.). Current Science 78, 162–164.
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. Nature Genetics 37, 1141–1146.
| A rice quantitative trait locus for salt tolerance encodes a sodium transporter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVCntL%2FJ&md5=a4395cb9d409860c01bd8492efc9d1a4CAS | 16155566PubMed |
Shi HZ, Lee BH, Wu SJ, Zhu JK (2002) Overexpression of a plasmamembrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nature Biotechnology 21, 81–85.
| Overexpression of a plasmamembrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Szabolcs I (1989) ‘Salt affected soils.’ (CRC Press: Boca Raton, FL, USA)
Walia H, Wilson C, Condamine P, Liu X, Ismail AM, Zeng L, Wanamaker SI, Mandal J, Xu J, Cui X, Close TJ (2005) Comparative transcriptional profiling of two contrasting rice genotypes under salinity stress during the vegetative growth stage. Plant Physiology 139, 822–835.
| Comparative transcriptional profiling of two contrasting rice genotypes under salinity stress during the vegetative growth stage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFCgsb7K&md5=7b9758db120e66de15f2d60a9bfdf965CAS | 16183841PubMed |
Witcombe JR, Hollington PA, Howarth CJ, Reader S, Steele KA (2008) Breeding for abiotic stresses for sustainable agriculture. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 363, 703–716.
| Breeding for abiotic stresses for sustainable agriculture.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1c7jtVegsQ%3D%3D&md5=f1482244feb423f9b8bbe0487b98af00CAS | 17761467PubMed |
Yeo AR, Flowers TJ (1982) Accumulation and localization of sodium ions within the shoots of rice (Oryza sativa) varieties differing in salinity resistance. Physiologia Plantarum 56, 343–348.
| Accumulation and localization of sodium ions within the shoots of rice (Oryza sativa) varieties differing in salinity resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXivVyq&md5=cfa3c31928055c68af99b929a9b1869aCAS |
Yeo AR, Flowers TJ (1984) Mechanisms of salinity resistance in rice and their role as physiological criteria in plant breeding. In ‘Salinity tolerance in plants’. (Eds RC Staples, GH Toenniessen) pp. 37–67. (Wiley: New York)
Yeo AR, Flowers TJ (1986) Salinity resistance in rice (Oryza sativa L.) and a pyramiding approach to breeding for saline soils. Australian Journal of Plant Physiology 13, 161–173.
| Salinity resistance in rice (Oryza sativa L.) and a pyramiding approach to breeding for saline soils.Crossref | GoogleScholarGoogle Scholar |
Yeo AR, Yeo ME, Flowers SA, Flowers TJ (1990) Screening of rice (Oryza sativa L.) genotypes for physiological characters contributing to salinity resistance, and their relationship to overall performance. Theoretical and Applied Genetics 79, 377–384.
| Screening of rice (Oryza sativa L.) genotypes for physiological characters contributing to salinity resistance, and their relationship to overall performance.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2c7mt1Whug%3D%3D&md5=982ba0f69fa3409f79ded0792a1f7314CAS | 24226357PubMed |
Yeo AR, Lee KS, Izard P, Boursier PJ, Flowers TJ (1991) Short- and long-term effects of salinity on leaf growth in rice (Oryza sativa L.). Journal of Experimental Botany 42, 881–889.
| Short- and long-term effects of salinity on leaf growth in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXlsl2msr0%3D&md5=cfc015d58165b72da854f451116eee97CAS |
Zeng L, Lesch SM, Grieve CM (2003) Rice growth and yield respond to changes in water depth and salinity stress. Agricultural Water Management 59, 67–75.
| Rice growth and yield respond to changes in water depth and salinity stress.Crossref | GoogleScholarGoogle Scholar |
