Physiological Responses and Clustering of Four Aromatic Rice Cultivars to NaCl Salt Stress
Abstract
Salt affected soil is a member of abiotic stresses to play as major barrier in rice production, which has been reported as salt susceptible. The objective of this research was to investigate the physiological responsesto salt stress in rice cultivars including Riceberry, Suphan Buri 1, Pathum Thani 1 and Khao Dawk Mali 105. Rice seedlings were subjected to NaCl salt stress treatment at 2, 4, 6, 8 or 10 dS m-1. Growth parameters, photosynthetic pigment contents, relative water content and free proline content were investigated. After 14 days of NaCl treatment with 8 dSm-1, the shoot fresh weight, shoot dry weight, leaf length and relative water content of Riceberry seedlings were enhanced in comparison with the control (without salt stress treatment). Moreover, four rice cultivars were classified into 2 groups based on growth parameters and photosynthetic pigment contents. For the first group, all growth parameters in Riceberry were maintained, while the second group (Suphan Buri 1, Pathum Thani 1 and Khao Dawk Mali 105 cultivars) the growth performances under salt stress conditions were declined. It was noted that only Riceberry had dramatically responded to salt tress by elevating its proline content, suggesting that the Riceberry might be a salt-tolerant rice cultivar via proline accumulation mechanism as an osmoregulation under salt stress.References
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New Phytologist, 82, 671-678.
Amirjani, M.R. (2010). Effect of NaCl on some physiological parameters of rice. European Journal of Biomedical and Pharmaceutical Sciences, 3(1), 6-16.
Bates, L.S., Waldren, R.P., & Teare, I.D. (1973). Rapid determination of free proline for water stress studies. Plant and Soil, 39, 205–207.
Botia, P., Navarro, J.M., & Cerda A, V.M. (2005). Yield and fruit quality of two melon cultivars irrigated with saline water at different stages of development. European Journal of Agronomy, 23, 243–253.
Bray, E.A. (1993). Molecular responses to water deficit. Plant Physiology, 103, 1035-1040.Bureau of Rice
Research and Development, Rice Department. (2009). Research salt-tolerant rice in the Central
Thailand. Retrieved April 17, 2017, from
http://www.brrd.in.th/library/document/E-book/brrd5201011c1. pdf, (in Thai).
Chaves, M.M., Flexas, J., & Pinheiro, C. (2009). Photosynthesis under drought and salt stress: Regulation mechanisms from whole plant to cell. Annals of Botany, 103, 551-560.
Cha-um, S., Vejchasarn, P., & Kirdmanee, C. (2007). An effective defensive response in Thai aromatic rice varities (Oryza sativa L. spp. indica) to salinity. Journal of Crop Science and Biotechnology, 10(4), 257-264.
Chen, C.T., & KaO, C.H. (1993). Osmotic stress and water stress have opposite effects on putrescence and proline production in excise rice leaves. Plant Growth Regulation, 13, 197-202.
Chunthaburee, S., Dongsansuk, A., Sanitchon, J., Pattanagul, W., & Theerakulpisut, P. (2016). Physiological and biochemical parameters for evaluation and clustering of rice cultivars differing in salt tolerance at seedling stage. Saudi Journal of Biological Sciences, 23, 467-477.
Chutimanukul, P., Chaidee, A., Buaboocha, T., Siangliw, M., Toojinda, T., Chadchawan, S., & Kositsup, B. (2013). Effect of salt stress on photosynthesis and growth in salt-tolerant rice lines obtained from CSSL population. Thai Journal of Genetics, S(1), 276-279, (in Thai).
Chutippaijit, S., Chu-um, S., & Sompornpailin, K. (2009). Differential accumulations of proline and flavonoids in indica rice varieties against salinity. Pakistan Journal of Botany, 41(5), 2497-2506.
Daiponmak, W., Theerakulpisut, P., Thanonkao, P., Vanavichit, A., & Prathepha, P. (2010). Changes of anthocyanin cyanidin-3-glucoside content and antioxidant activity in Thai rice varieties under salinity stress. ScienceAsia, 36, 286-291.
Dierickx, W. R. (2009). The salinity and alkalinity status of arid and semi-arid lands. In Willy H. Verheye (Ed.), Encyclopedia of Land Use, Land Cover and Soil Sciences - Volume V: Dry Lands and Desertification (pp. 163-189). United Kingdom: Eoless Publisher.
Gadallah, M. A. A. (1999). Effects of proline and glycinebetaines on Vicia faba responses to salt stress. Biologia Plantarum, 42(2), 249-257.
Gashaw, A., Theerawitaya, C., Samphumphuang, T., Cha-um, S., & Supaibulwatana, K. (2014). CPPU elevates photosynthetic abilities, growth performances and yield traits in salt stressed rice (Oryza sativa L. spp. indica) via free proline and sugar accumulation. Pesticide Biochemistry and Physiology, 108, 27-33.
Greenway, H., & Munns, R. (1980). Mechanisms of salt tolerance in non-halophytes. Annual Review of
Plant Physiology, 31, 149-190.
Hoang, T.M.L., Tran, T. N., Nguyen, T.K.T., Williams, B., & Wurm, P. (2016). Improvement of salinity stress tolerance in rice: Challenges and opportunities. Agronomy, 6(4), 54; doi:10.3390/agronomy6040054.
Huang, Z., Long, X., Wang, L., Kang, J., Zhang, Z., Zed, R., & Liu, Z. (2012). Growth, photosynthesis and
H+-ATPase activity in two Jerusalem artichoke varieties under NaCl- induced stress. Process Biochemistry, 47, 591–596.
Iyer, S., & Caplan, A. (1998). Products of proline catabolism can induce osmotically regulated genes in rice. Plant Physiology, 116, 203-211.
Kennedy, B.F., & Fillippis, D.L. (1999). Physiological and oxidative response to NaCl of the salt tolerant Grevillea ilicifolia and the salt sensitive Grevillea arenaria. Journal of Plant Physiology, 155,
746–754.
Kurotani, K., Yamanaka, K., Toda, Y., Ogawa, D., Tanaka, M., Kozawa, H., & Takeda, S. (2015). Stress tolerance profiling of a collection of extant salt-tolerant rice varieties and transgenic plants overexpressing abiotic stress tolerance genes. Plant Cell Physiology, 56(10), 1867-1876.
Lee, D.G., Park, K.W., An, Y.J., Sohn, Y.G., Ha, J.K., Kim, H.Y., Bae, D.W., Lee, K.H., Kang, N.J., Lee, B.H., Kang, K.Y., & Lee, J.J. (2011). Proteomics analysis of salt-induced leaf proteins in two rice germplasms with different salt sensitivity Can. Journal of Plant Sciences, 91, 337-349.
Li, X., Bua, N., Li, Y., Maa, L., Xin, S., & Zhang, L. (2012). Growth, photosynthesis and antioxidant responses of endophyte infected and non-infected rice under lead stress conditions. Journal of Hazardous Materials, 213, 55–61.
Lichtenthaler, H.K. (1987). Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. Methods in Enzymology, 148, 350-382.
Lutts, S., Kinet, J.M., & Bouharmont, J. (1996a). Effect of salt stress on growth, mineral nutrition and proline accumulation in relation to osmotic adjustment in rice (Oryza sativa L.) cultivars differing in salinity resistance. Plant Growth Regulation, 19, 207-218.
Lutts, S., Kinet, J.M., & Bouharmont, J. (1996b). NaCl-induced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance. Annals of Botany, 78, 389-398.
Lutts, S., Majerus, V., & Kinet, J.M. (1999). NaCl effects on proline metabolism in rice (Oryza sativa L.) seedlings. Physiologia Plantarum, 105, 1399-3054.
Maas, E.V., Poss, J.A., & Hoffman, G.J. (1986). Salinity sensitivity of sorghum at three growth stages.
Irrigation Science, 7, 1-11.
Maas, E.V., & Poss, J.A. (1989). Salt sensitivity of cowpea at various growth stages. Irrigation Science, 10, 313-320.
Maksup, S., Roytrakul, S., & Supaibulwatana, K. (2014). Physiological and comparative proteomic analyses of Thai jasmine rice and two check cultivars in response to drought stress. Journal of Plant Interactions, 9(1), 43-55.
Meloni, D.A., Oliva, M.A., Ruiz, H.A., & Martinez, C.A. (2001). Contribution of proline and inorganic solutes to
osmotic adjustment in cotton under salt stress. Journal of Plant Nutrition, 24, 599 - 612.
Nguyen, H.T., Babu, R.C., & Blum, A. (1997). Breeding for drought resistance in rice: Physiology and
molecular genetics considerations. Crop Science, 37, 1426-1443.
Parida, A.K., & Das, A.B. (2005). Salt tolerance and salinity effects on plants: a review. Ecotoxicology and Environmental Safety, 60, 324–349.
Pongprayoon, W., Chu-um, S., Pichakum, A. & Kirdmanee, C. (2008). Proline profiles in aromatic cultivars
photoautotrophically grown in responses to salt stress. International Journal of Botany, 4 (3),
276-282.
Saeed, A.I., Sharov, V., White, J., Li, J., Liang, W., Bhagabati, N., Braisted, J., Klapa, M., Currier, T.,
Thiagarajan, M., Sturn, A., Snuffin, M., Rezantsev, A., Popov, D., Ryltsov, A., Kostukovich, E.,
Borisovsky, I., Liu, Z., Vinsavich, A., Trush, V., & Quackenbush, J. (2003). TM4: a free, open-source
system for microarray data management and analysis. Biotechniques, 34, 374-378.
Sakamoto, A., & Murata, N. (2002). The role of glycine betaine in the protection of plants from stress: clues from transgenic plants. Plant, Cell & Environment, 25, 163-171.
Schonfeld, M.A., Johnson, R.C., Carwer, B.F., & Mornhinweg, D.W. (1988). Water relations in winter wheat as drought resistance indicators. Crop Science, 28, 526-531.
Shabala, S.N., Shabala, S.I., Martynenko, A.I., Babourina, O., & Newman, I.A. (1998). Salinity effect on bioelectric activity, growth, Na+ accumulation and chlorophyll fluorescence of maize leaves: a comparative survey and prospects for screening. Australian Journal of Plant Physiology, 25,
609-616.
Strizhov, N., Ábrahám, E., Ökrész, L., Blickling, S., Zilberstein, A., Schell, J., Koncz, C., & Szabados, L. (1997). Differential expression of two P5CS genes controlling proline accumulation during salt-stress requires ABA and is regulated by ABA1, ABI1 and AXR2 in Arabidopsis. The Plant Journal, 12, 557-569.
Sultana, N., Ikeda T., and Itoh, R. (1999). Effect of NaCl salinity on photosynthesis and dry matter
accumulation in developing rice grains. Environmental and Experimental Botany, 42, 211–220.
Taiz, L., & Zeiger, E. (2006). Plant Physiology (4th ed.). Massachusetts: Sinaure Associate.
Takemura, T., Hanagata, N., Sugihara, K., Baba, S., Karube, I., & Dubinsky, Z. (2000). Physiological and
biochemical responses to salt stress in the mangrove, Bruguiera gymnorrhiza. Aquatic Botany, 68,
15-28.
Tarczynski, M.C., Jensen, R.G., & Bohnert, H.J. (1993). Stress protection of transgenic tobacco by production of the osmolyte mannitol. Science, 259, 508-510.
Vajrabhaya, M., & Vajrabhaya, T. (1991). Somaclonal variation of salt tolerance in rice. In
Y.P.S Bajaj (Ed), Biotechnology in Agriculture and Forestry 14 (pp. 368-382). Berlin Heidelberg: Springer-Verlag.
Wilson, C., Lesch, S.M., & Grieve, C.M. (2000). Growth stage modulates salinity tolerance of
New Zealand spinach (Tetragonia tetragonioides, Pall) and Red Orach (Atriplex hortensis L.). Annals of Botany, 85, 501-509.
Zheng, C., Jiang, D., Liu, F., Dai, T., Jing, Q., & Cao, W. (2009). Effects of salt and water logging stresses and their combination on leaf photosynthesis, chloroplast ATP synthesis, and antioxidant capacity in wheat. Plant Science, 176, 575-582.
New Phytologist, 82, 671-678.
Amirjani, M.R. (2010). Effect of NaCl on some physiological parameters of rice. European Journal of Biomedical and Pharmaceutical Sciences, 3(1), 6-16.
Bates, L.S., Waldren, R.P., & Teare, I.D. (1973). Rapid determination of free proline for water stress studies. Plant and Soil, 39, 205–207.
Botia, P., Navarro, J.M., & Cerda A, V.M. (2005). Yield and fruit quality of two melon cultivars irrigated with saline water at different stages of development. European Journal of Agronomy, 23, 243–253.
Bray, E.A. (1993). Molecular responses to water deficit. Plant Physiology, 103, 1035-1040.Bureau of Rice
Research and Development, Rice Department. (2009). Research salt-tolerant rice in the Central
Thailand. Retrieved April 17, 2017, from
http://www.brrd.in.th/library/document/E-book/brrd5201011c1. pdf, (in Thai).
Chaves, M.M., Flexas, J., & Pinheiro, C. (2009). Photosynthesis under drought and salt stress: Regulation mechanisms from whole plant to cell. Annals of Botany, 103, 551-560.
Cha-um, S., Vejchasarn, P., & Kirdmanee, C. (2007). An effective defensive response in Thai aromatic rice varities (Oryza sativa L. spp. indica) to salinity. Journal of Crop Science and Biotechnology, 10(4), 257-264.
Chen, C.T., & KaO, C.H. (1993). Osmotic stress and water stress have opposite effects on putrescence and proline production in excise rice leaves. Plant Growth Regulation, 13, 197-202.
Chunthaburee, S., Dongsansuk, A., Sanitchon, J., Pattanagul, W., & Theerakulpisut, P. (2016). Physiological and biochemical parameters for evaluation and clustering of rice cultivars differing in salt tolerance at seedling stage. Saudi Journal of Biological Sciences, 23, 467-477.
Chutimanukul, P., Chaidee, A., Buaboocha, T., Siangliw, M., Toojinda, T., Chadchawan, S., & Kositsup, B. (2013). Effect of salt stress on photosynthesis and growth in salt-tolerant rice lines obtained from CSSL population. Thai Journal of Genetics, S(1), 276-279, (in Thai).
Chutippaijit, S., Chu-um, S., & Sompornpailin, K. (2009). Differential accumulations of proline and flavonoids in indica rice varieties against salinity. Pakistan Journal of Botany, 41(5), 2497-2506.
Daiponmak, W., Theerakulpisut, P., Thanonkao, P., Vanavichit, A., & Prathepha, P. (2010). Changes of anthocyanin cyanidin-3-glucoside content and antioxidant activity in Thai rice varieties under salinity stress. ScienceAsia, 36, 286-291.
Dierickx, W. R. (2009). The salinity and alkalinity status of arid and semi-arid lands. In Willy H. Verheye (Ed.), Encyclopedia of Land Use, Land Cover and Soil Sciences - Volume V: Dry Lands and Desertification (pp. 163-189). United Kingdom: Eoless Publisher.
Gadallah, M. A. A. (1999). Effects of proline and glycinebetaines on Vicia faba responses to salt stress. Biologia Plantarum, 42(2), 249-257.
Gashaw, A., Theerawitaya, C., Samphumphuang, T., Cha-um, S., & Supaibulwatana, K. (2014). CPPU elevates photosynthetic abilities, growth performances and yield traits in salt stressed rice (Oryza sativa L. spp. indica) via free proline and sugar accumulation. Pesticide Biochemistry and Physiology, 108, 27-33.
Greenway, H., & Munns, R. (1980). Mechanisms of salt tolerance in non-halophytes. Annual Review of
Plant Physiology, 31, 149-190.
Hoang, T.M.L., Tran, T. N., Nguyen, T.K.T., Williams, B., & Wurm, P. (2016). Improvement of salinity stress tolerance in rice: Challenges and opportunities. Agronomy, 6(4), 54; doi:10.3390/agronomy6040054.
Huang, Z., Long, X., Wang, L., Kang, J., Zhang, Z., Zed, R., & Liu, Z. (2012). Growth, photosynthesis and
H+-ATPase activity in two Jerusalem artichoke varieties under NaCl- induced stress. Process Biochemistry, 47, 591–596.
Iyer, S., & Caplan, A. (1998). Products of proline catabolism can induce osmotically regulated genes in rice. Plant Physiology, 116, 203-211.
Kennedy, B.F., & Fillippis, D.L. (1999). Physiological and oxidative response to NaCl of the salt tolerant Grevillea ilicifolia and the salt sensitive Grevillea arenaria. Journal of Plant Physiology, 155,
746–754.
Kurotani, K., Yamanaka, K., Toda, Y., Ogawa, D., Tanaka, M., Kozawa, H., & Takeda, S. (2015). Stress tolerance profiling of a collection of extant salt-tolerant rice varieties and transgenic plants overexpressing abiotic stress tolerance genes. Plant Cell Physiology, 56(10), 1867-1876.
Lee, D.G., Park, K.W., An, Y.J., Sohn, Y.G., Ha, J.K., Kim, H.Y., Bae, D.W., Lee, K.H., Kang, N.J., Lee, B.H., Kang, K.Y., & Lee, J.J. (2011). Proteomics analysis of salt-induced leaf proteins in two rice germplasms with different salt sensitivity Can. Journal of Plant Sciences, 91, 337-349.
Li, X., Bua, N., Li, Y., Maa, L., Xin, S., & Zhang, L. (2012). Growth, photosynthesis and antioxidant responses of endophyte infected and non-infected rice under lead stress conditions. Journal of Hazardous Materials, 213, 55–61.
Lichtenthaler, H.K. (1987). Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. Methods in Enzymology, 148, 350-382.
Lutts, S., Kinet, J.M., & Bouharmont, J. (1996a). Effect of salt stress on growth, mineral nutrition and proline accumulation in relation to osmotic adjustment in rice (Oryza sativa L.) cultivars differing in salinity resistance. Plant Growth Regulation, 19, 207-218.
Lutts, S., Kinet, J.M., & Bouharmont, J. (1996b). NaCl-induced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance. Annals of Botany, 78, 389-398.
Lutts, S., Majerus, V., & Kinet, J.M. (1999). NaCl effects on proline metabolism in rice (Oryza sativa L.) seedlings. Physiologia Plantarum, 105, 1399-3054.
Maas, E.V., Poss, J.A., & Hoffman, G.J. (1986). Salinity sensitivity of sorghum at three growth stages.
Irrigation Science, 7, 1-11.
Maas, E.V., & Poss, J.A. (1989). Salt sensitivity of cowpea at various growth stages. Irrigation Science, 10, 313-320.
Maksup, S., Roytrakul, S., & Supaibulwatana, K. (2014). Physiological and comparative proteomic analyses of Thai jasmine rice and two check cultivars in response to drought stress. Journal of Plant Interactions, 9(1), 43-55.
Meloni, D.A., Oliva, M.A., Ruiz, H.A., & Martinez, C.A. (2001). Contribution of proline and inorganic solutes to
osmotic adjustment in cotton under salt stress. Journal of Plant Nutrition, 24, 599 - 612.
Nguyen, H.T., Babu, R.C., & Blum, A. (1997). Breeding for drought resistance in rice: Physiology and
molecular genetics considerations. Crop Science, 37, 1426-1443.
Parida, A.K., & Das, A.B. (2005). Salt tolerance and salinity effects on plants: a review. Ecotoxicology and Environmental Safety, 60, 324–349.
Pongprayoon, W., Chu-um, S., Pichakum, A. & Kirdmanee, C. (2008). Proline profiles in aromatic cultivars
photoautotrophically grown in responses to salt stress. International Journal of Botany, 4 (3),
276-282.
Saeed, A.I., Sharov, V., White, J., Li, J., Liang, W., Bhagabati, N., Braisted, J., Klapa, M., Currier, T.,
Thiagarajan, M., Sturn, A., Snuffin, M., Rezantsev, A., Popov, D., Ryltsov, A., Kostukovich, E.,
Borisovsky, I., Liu, Z., Vinsavich, A., Trush, V., & Quackenbush, J. (2003). TM4: a free, open-source
system for microarray data management and analysis. Biotechniques, 34, 374-378.
Sakamoto, A., & Murata, N. (2002). The role of glycine betaine in the protection of plants from stress: clues from transgenic plants. Plant, Cell & Environment, 25, 163-171.
Schonfeld, M.A., Johnson, R.C., Carwer, B.F., & Mornhinweg, D.W. (1988). Water relations in winter wheat as drought resistance indicators. Crop Science, 28, 526-531.
Shabala, S.N., Shabala, S.I., Martynenko, A.I., Babourina, O., & Newman, I.A. (1998). Salinity effect on bioelectric activity, growth, Na+ accumulation and chlorophyll fluorescence of maize leaves: a comparative survey and prospects for screening. Australian Journal of Plant Physiology, 25,
609-616.
Strizhov, N., Ábrahám, E., Ökrész, L., Blickling, S., Zilberstein, A., Schell, J., Koncz, C., & Szabados, L. (1997). Differential expression of two P5CS genes controlling proline accumulation during salt-stress requires ABA and is regulated by ABA1, ABI1 and AXR2 in Arabidopsis. The Plant Journal, 12, 557-569.
Sultana, N., Ikeda T., and Itoh, R. (1999). Effect of NaCl salinity on photosynthesis and dry matter
accumulation in developing rice grains. Environmental and Experimental Botany, 42, 211–220.
Taiz, L., & Zeiger, E. (2006). Plant Physiology (4th ed.). Massachusetts: Sinaure Associate.
Takemura, T., Hanagata, N., Sugihara, K., Baba, S., Karube, I., & Dubinsky, Z. (2000). Physiological and
biochemical responses to salt stress in the mangrove, Bruguiera gymnorrhiza. Aquatic Botany, 68,
15-28.
Tarczynski, M.C., Jensen, R.G., & Bohnert, H.J. (1993). Stress protection of transgenic tobacco by production of the osmolyte mannitol. Science, 259, 508-510.
Vajrabhaya, M., & Vajrabhaya, T. (1991). Somaclonal variation of salt tolerance in rice. In
Y.P.S Bajaj (Ed), Biotechnology in Agriculture and Forestry 14 (pp. 368-382). Berlin Heidelberg: Springer-Verlag.
Wilson, C., Lesch, S.M., & Grieve, C.M. (2000). Growth stage modulates salinity tolerance of
New Zealand spinach (Tetragonia tetragonioides, Pall) and Red Orach (Atriplex hortensis L.). Annals of Botany, 85, 501-509.
Zheng, C., Jiang, D., Liu, F., Dai, T., Jing, Q., & Cao, W. (2009). Effects of salt and water logging stresses and their combination on leaf photosynthesis, chloroplast ATP synthesis, and antioxidant capacity in wheat. Plant Science, 176, 575-582.
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