Abstract
Aims
The objectives of this study were to evaluate salt tolerance level of rice genotypes using the well-established screening criteria; the salt injury score, survival percentage and ratio between Na+ and K+, as well as the contents of proline and chlorophyll, and to identify the relationship between salt tolerance and physiological characters.
Methods
One hundred and six rice genotypes were grown in hydroponic solutions subjected to salt stress and evaluated for salt tolerance ability and the physiological parameters. Multivariate cluster analysis was performed based on salinity tolerance scores (ST scores; score 1 being the most tolerant, score 9 the most sensitive), survival percentage and Na+/K+ ratio.
Results
ST scores based on salt injury symptoms were negatively correlated with survival percentage and chlorophyll concentration in the stressed seedlings but positively correlated with Na+/K+ ratio and proline content. Rice genotypes were classified into five salt tolerance groups: tolerant (T), moderately tolerant (MT), moderately sensitive (MS), sensitive (S) and highly sensitive (HS). The means of ST scores were significantly different among the five tolerance groups indicating that the ST score was the most reliable index for identifying salt tolerance. The means of Na+/K+ ratio and proline content in stressed seedlings were distinctively different between the extreme T and HS groups, but the means among the intermediate groups (MT, MS and S) were not significantly different. Chlorophyll content, on the other hand, was not related to the levels of salt tolerance.
Conclusions
In addition to the commonly used Na+/K+ ratio, proline content is suggested to be another useful criterion to differentiate salt-tolerant from salt-sensitive rice. This study also identified several Thai improved and local cultivars with the level of salt tolerance and physiological characters comparable to Pokkali, the standard salt-tolerant donor and may be utilized as alternative sources of salt tolerance alleles.
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Abbreviations
- CaC:
-
Chlorophyll a in the control
- CaS:
-
Chlorophyll a in the stressed treatment
- CbC:
-
Chlorophyll b in the control
- CbS:
-
Chlorophyll b in the stressed treatment
- CI:
-
Chlorophyll index
- CS:
-
Chlorophyll content in the stressed treatment
- DMRT:
-
Duncan’s multiple range test
- HS:
-
Highly sensitive
- MT:
-
Moderately tolerant
- MS:
-
Moderately sensitive
- PC:
-
Proline content
- PI:
-
Proline index
- PS:
-
Proline in the stressed treatment
- RCB:
-
Randomized complete block
- ROS:
-
Reactive oxygen species
- RWC:
-
Relative water content
- S:
-
Sensitive
- ST:
-
Salinity tolerant
- T:
-
Tolerant
- TC:
-
Total chlorophyll in the control
- TS:
-
Total chlorophyll in the stressed treatment
References
Akbar M (1986) Breeding for salinity tolerance in rice. In: IRRI (ed) Salt-affected soils of Pakistan, India and Thailnad. Intl. Rice Res. Institute, Manila, Philippines, pp 39–63
Ali Y, Aslam Z, Awan AR, Hussain F, Cheema AA (2004) Screening rice (Oryza sativa L.) lines/cultivars against salinity in relation to morphological and physiological traits and yield components. Int J Agri Biol 6(3):572–575
Arnon DI (1949) Copper enzymes in isolated chlorophasts. Polyphenoloxidase in Beta vulgaria. Plant Physiol 24(1):1–15. doi:10.1104/pp.24.1.1
Ashraf M, Wu L (1994) Breeding for salinity tolerance in plants. Crit Rev Plant Sci 13:17–42. doi:10.1080/07352689409701906
Aslam M, Qureshi RH, Ahmed N (1993) A rapid screening technique for salt tolerance in rice (Oryza sativa L.). Plant Soil 150:99–107. doi:10.1007/BF00779180
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207. doi:10.1007/BF00018060
Chen Z, Cuin TA, Zhou M, Twomey A, Naidu BP, Shabala S (2007) Compatible solute accumulation and stress-mitigating effects in barley genotypes contrasting in their salt tolerance. J Exp Bot 58(15/16):4245–4255. doi:10.1093/jxb/erm284
Chinnusamy V, Jagendorf A, Zhu J-K (2005) Understanding and improving salt tolerance in plants. Crop Sci 45:437–448. doi:10.2135/cropsci2005.0437
Chowdhury MAM, Moseki B, Bowling DJF (1995) A method for screening rice plants for salt tolerance. Plant Soil 171(2):317–322. doi:10.1007/BF00010287
Cuin TA, Shabala S (2005) Exogenously supplied compatible solutes rapidly ameliorate NaCl-induced potassium efflux from barley roots. Plant Cell Physiol 46(12):1924–1933. doi:10.1093/pcp/pci205, available online at www.pcp.oupjournals.org
Delauney AJ, Verma DPS (1993) Proline biosynthesis and osmoregulation in plants. Plant J 4(2):215–223. doi:10.1046/j.1365-313X.1993.04020215.x
Demiral T, Türkan İ (2005) Comparative lipid peroxidation, antioxidant defense systems and proline content in roots of two rice cultivars differing in salt tolerance. Envi Exp Bot 53(3):247–257. doi:10.1016/j.envexpbot.2004.03.017
Farooq S, Azam F (2006) The use of cell membrane stability (CMS) technique to screen for salt tolerant wheat varieties. J Plant Physiol 163(6):629–637. doi:10.1016/j.jplph.2005.06.006
Flowers TJ, Yeo AR (1981) Variability in the resistance of sodium chloride salinity within rice (Oryza sativa L.) varieties. New Phytol 88:363–373. doi:10.1111/j.1469-8137.1981.tb01731.x
Gregorio GB, Dharmawansa S, Mendoza RD (1997) Screening rice for salinity tolerance. IRRI. Discussion Paper Series No. 22. International Rice Research Institute, Manila, the Philippines, pp 1–30
Gregorio GB, Senadhira D, Mendoza RD, Manigbas NL, Roxas JP, Guerta CQ (2002) Progress in breeding for salinity tolerance and associated abiotic stresses in rice. Field Crop Res 76(2–3):91–101. doi:10.1016/S0378-4290(02)00031-X
Haq TU, Akhtar J, Nawaz S, Ahmad R (2009) Morpho-physiological response of rice (Oryza sativa L.) varieties to salinity stress. Pak J Bot 41(6):2943–2956
Hare PD, Cress WA (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul 21(2):79–102. doi:10.1023/A:1005703923347
Heenan DP, Lewin LG, McCaffery DW (1988) Salinity tolerance in rice varieties at different growth stages. Aust J Exp Agric 28(3):343–349. doi:10.1071/EA9880343
Hellmann H, Funk D, Rentsch D, Frommer WB (2000) Hypersensitivity of an Arabidopsis sugar signaling mutant towards exogenous proline application. Plant Physiol 122(2):357–368. doi:10.1104/pp. 122.2.357
Hien DT, Jacobs M, Angenon G, Hermans C, Thu TT, Van Son L, Roosens NH (2003) Proline accumulation and ∆1-pyrroline-5-carboxylate synthase gene properties in three rice cultivars differing in salinity and drought tolerance. Plant Sci 165(5):1059–1068. doi:10.1016/S0168-9452(03)00301-7
Igarashi Y, Yoshiba Y, Sanada Y, Yamaguchi-Shinozaki K, Wada K, Shinozaki K (1997) Characterization of the gene for ∆1-pyrroline-5-carboxylate synthethase and correlation between the expression of the gene and the salt tolerance in Oryza sativa L. Plant Mol Biol 33(5):857–865. doi:10.1023/A:1005702408601
Kavi Kishor PB, Hong Z, Miao G-H, Hu C-AA, Verma DPS (1995) Overexpression of Δ1-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiol 108(4):1387–1394. doi:10.1104/pp. 108.4.1387
Khedr AHA, Abbas MA, Wahid AAA, Quick WP, Abogadallah GM (2003) Proline induces the expression of salt-stress-responsive proteins and may improve the adaptation of Pancratium maritimum L. to salt-stress. J Exp Bot 54(392):2553–2562. doi:10.1093/jxb/erg277
Khush GS, Virk PS (2005) IR varieties and their impact. International Rice Research Institute, Philippines, Los Baños (Philippines)
Lattin JM, Carroll JD, Green PE (2003) Analyzing multivariate data. Thomson Brooks/Cole, Pacific Grove, CA
Lee K-S, Choi W-Y, Ko J-C, Kim T-S, Gregorio GB (2003) Salinity tolerance of japonica and indica rice (Oryza sativa L.) at the seedling stage. Planta 216(6):1043–1046. doi:10.1007/s00425-002-0958-3
Li N, Chen S, Zhou X, Li C, Shao J, Wang R, Fritz E, Hüttermann A, Polle A (2008) Effect of NaCl on Photosynthesis, salt accumulation and ion compartmentation in two mangrove species, Kandelia candel and Bruguiera gymnorhiza. Aquat Bot 88:303–310. doi:10.1016/j.aquabot.2007.12.003
Lutts S, Kinet JM, Bouharmont J (1996) NaCl-induced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance. Ann Bot 78(3):389-398. doi:10.1006/anbo.1996.0134
Lutts S, Majerus V, Kinet J-M (1999) NaCl effects on proline metabolism in rice (Oryza sativa) seedlings. Physiol Plant 105(3):450–458. doi:10.1034/j.1399-3054.1999.105309.x
Maggio A, Miyazaki S, Veronese P, Fujita T, Ibeas JI, Damsz B, Narasimhan M, Hasegawa PM, Joly RJ, Bressan RA (2002) Does proline accumulation play an active role in stress-induced growth reduction? Plant J 31(6):699–712. doi:10.1046/j.1365-313X.2002.01389.x
Misra AN, Sahu SM, Misra M, Singh P, Meera I, Das N, Kar M, Sahu P (1997) Sodium chloride induced changes in leaf growth, and pigment and protein contents in two rice cultivars. Biol Plantarum 39(2):257–262. doi:10.1023/A:1000357323205
Moftah AE, Michel BE (1987) The effect of sodium chloride on solute potential and proline accumulation in soybean leaves. Plant Physiol 83:238–240. doi:10.1104/pp. 83.2.238
Mohammadi-Nejad G, Arzani A, Rezai AM, Singh RK, Gregorio GB (2008) Assessment of rice genotypes for salt tolerance using microsatellite markers associated with the saltol QTL. Afr J Biotechnol 7(6):730–736
Molazem D, Qurbanov EM, Dunyamaliyev SA (2010) Role of proline, Na and chylrophyll content in salt tolerance of corn (Zea mays L.). American-Eurasian J Agr Environ Sci 9(3):319–324
Moradi F, Ismail AM (2007) Responses of photosynthesis, chlorophyll fluorescence and ROS-scavenging systems to salt stress during seedling and reproductive stages in rice. Ann Bot 99(6):1161–1173. doi:10.1093/aob/mcm052
Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25(2):239–250. doi:10.1046/j.0016-8025.2001.00808.x
Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Safety 60(3):324–349. doi:10.1016/j.ecoenv.2004.06.010
Pitman MG (1976) Ion uptake by plant root. In: Lüttge U, Pitman MG (eds) Encyclopedia of plant physiology, vol 2, Springer-Verlag. Berlinpp, Heidelberg, New York, pp 95–128
Poustini K, Siosemardeh A, Ranjbar M (2007) Proline accumulation as a response to salt stress in 30 wheat (Triticum aestivum L.) cultivars differing in salt tolerance. Genet Resour Crop Evol 54(5):925–934. doi:10.1007/s10722-006-9165-6
Renuka Devi PS, Sabu A, Sheeja TE, Nambisan P (1996) Proline accumulation and salt tolerance in rice. In: Ravishankar GA, Venkataraman L (eds) Recent advances in biotechnological applications of plant tissue and cell culture. Oxford and IBH publishing co, New Delhi, India, pp 410–414
Sanchez DH, Siahpoosh MR, Roessner U, Udvardi M, Kopka J (2008) Plant metabolomics reveals conserved and divergent metabolic responses to salinity. Physiol Plant 132(2):209–219. doi:10.1111/j.1399-3054.2007.00993.x
Shabala S, Cuin TA (2007) Potassium transport and plant salt tolerance. Physiol Plant 133:651–669. doi:10.1111/j.1399-3054.2007.01008.x
Smirnoff N, Cumbes QJ (1989) Hydroxyl radical scavenging activity of compatible solutes. Phytochem 28(4):1057–1060. doi:10.1016/0031-9422(89)80182-7
Suriya-arunroj D, Supapoj N, Toojinda T, Vanavichit A (2004) Relative leaf water content as an efficient method for evaluating rice cultivars for tolerance to salt stress. Sci Asia 30:411–415. doi:10.2306/scienceasia1513-1874.2004.30.411
Szabados L, Savouré A (2009) Proline: a multifunctional amino acid. Trends Plant Sci 15(2):89–97. doi:10.1016/j.tplants.2009.11.009
Székely G, Ábrahám E, Cséplo Á, Rigo G, Zsigmond L, Csiszár J, Ayaydin F, Strizhov N, Jásik J, Schmelzer E, Koncz C, Szabados L (2008) Duplicated P5CS genes of Arabidopsis play distinct roles in stress regulation and developmental control of proline biosynthesis. Plant J 53(1):11–28. doi:10.1111/j.1365-313X.2007.03318.x
Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91:503–527. doi:10.1093/aob/mcg058
Theerakulpisut P, Bunnag S, Kong-ngern K (2005) Genetic diversity, salinity tolerance and physiology responses to NaCl of Six rice (Oryza sativa L.) cultivars. Asian J Plant Sci 4(6):562–573. doi:10.3923/ajps.2005.562.573
Trovato M, Mattioli R, Costantino P (2008) Multiple roles of proline in plant stress tolerance and development. Rend Lincei 19(4):325–346. doi:10.1007/s12210-008-0022-8
Wanichananan P, Kirdmanee C, Vutiyano C (2003) Effect of salinity on biochemical and physiological characteristics in correlation to selection of salt-tolerance in aromatic rice (Oryza sativa L.). Sci Asia 29:333–339. doi:10.2306/scienceasia1513-1874.2003.29.333
Yeo AR, Flowers TJ (1982) Accumulation and localization of sodium ions within the shoots of rice (Oryza sativa L.) varieties differing in salinity resistance. Physiol Plant 56(3):343–348. doi:10.1111/j.1399-3054.1982.tb00350.x
Yeo AR, Flowers TJ (1983) Varietal differences in the toxicity of sodium ions in rice leaves. Physiol Plant 59(2):189–195. doi:10.1111/j.1399-3054.1983.tb00756.x
Yeo AR, Flowers TJ (1986) Salinity resistance in rice (Oryza sativa L.) and a pyramiding approach to breeding varieties for saline soils. Aust J Plant Physiol 13(1):161–173. doi:10.1071/PP9860161
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. Theor Appl Genet 79(3):377–384. doi:10.1007/BF01186082
Yoshida S (1976) Routine procedure for growing rice plants in culture solution. In: Yoshida S, Forno DA, Cook JH, Gomez KA (eds) Laboratory manual for physiological studies of rice. I.R.R.I, Manilla, Philippines, pp 61–66
Zeng L (2005) Exploration of relationships between physiological parameters and growth performance of rice (Oryza sativa L.) seedlings under salinity stress using multivariate analysis. Plant Soil 268(1):51–59. doi:10.1007/s11104-004-0180-0
Acknowledgements
The authors wish to thank Dr. Teerayut Toojinda of Biotec and Dr. Suwat Jearakongman of Rice Department, Thailand for kindly providing rice seeds for this study. We are grateful for Dr. Phan Tuan Nghia for kindly reviewing the manuscript. This work was financially supported by the Ph.D. scholarship awarded to the first author from the Office of the Higher Education Commission, Ministry of Education, Thailand, and research funding from Khon Kaen University to the corresponding author and the Genomics and Proteomics Research Group for Improvement of Salt-tolerant Rice.
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Kanawapee, N., Sanitchon, J., Lontom, W. et al. Evaluation of salt tolerance at the seedling stage in rice genotypes by growth performance, ion accumulation, proline and chlorophyll content. Plant Soil 358, 235–249 (2012). https://doi.org/10.1007/s11104-012-1179-6
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DOI: https://doi.org/10.1007/s11104-012-1179-6