Abstract
There is large area of saline abandoned and low-yielding land distributed in coastal zone in the world. Soil salinity which inhibits plant growth and decreases crop yield is a serious and chronic problem for agricultural production. Improving plant salt tolerance is a feasible way to solve this problem. Plant physiological and biochemical responses under salinity stress become a hot issue at present, because it can provide insights into how plants may be modified to become more tolerant. It is generally known that the negative effects of soil salinity on plants are ascribed to ion toxicity, oxidative stress and osmotic stress, and great progress has been made in the study on molecular and physiological mechanisms of plant salinity tolerance in recent years. However, the present knowledge is not easily applied in the agronomy research under field environment. In this review, we simplified the physiological adaptive mechanisms in plants grown in saline soil and put forward a practical procedure for discerning physiological status and responses. In our opinion, this procedure consists of two steps. First, negative effects of salt stress are evaluated by the changes in biomass, crop yield and photosynthesis. Second, the underlying reasons are analyzed from osmotic regulation, antioxidant response and ion homeostasis. Photosynthesis is a good indicator of the harmful effects of saline soil on plants because of its close relation with crop yield and high sensitivity to environmental stress. Particularly, chlorophyll a fluorescence transient has been accepted as a reliable, sensitive and convenient tool in photosynthesis research in recent years, and it can facilitate and enrich photosynthetic research under field environment.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- ABA:
-
Abscisic acid
- AsA:
-
Ascorbate
- APX:
-
Ascorbate peroxidase
- CAT:
-
Catalase
- DHAR:
-
Dehydroascorbate reductase
- GPXs:
-
Glutathione peroxidases
- GR:
-
Glutathione reductase
- GSH:
-
Glutathione
- H2O2 :
-
Hydrogen peroxide
- MDA:
-
Malondialdehyde
- MDAR:
-
Monoascorbate reductase
- O2 − :
-
Superoxide anion radical
- –OH:
-
Hydroxyl radical
- PSI:
-
Photosystem I
- PSII:
-
Photosystem II
- ROS:
-
Reactive oxygen species
- SOD:
-
Superoxide dismutase
References
Abrol E, Vyas D, Koul S (2012) Metabolic shift from secondary metabolite production to induction of anti-oxidative enzymes during NaCl stress in Swertia chirata Buch.-Ham. Acta Physiol Plant 34:541–546. doi:10.1007/s11738-011-0851-4
Akram MS, Ashraf M (2011) Exogenous application of potassium dihydrogen phosphate can alleviate the adverse effects of salt stress on sunflower. J Plant Nutr 34:1041–1057. doi:10.1080/01904167.2011.555585
Almodares A, Hadi MR, Ahmadpour H (2008) Sorghum stem yield and soluble carbohydrates under different salinity levels. Afr J Biotechnol 7:4051–4055
Amzallag GN, Lerner HR, Poljakoffmayber A (1990) Induction of increased salt tolerance in sorghum-bicolor by NaCl pretreatment. J Exp Bot 41:29–34. doi:10.1093/Jxb/41.1.29
Apse MP, Blumwald E (2007) Na+ transport in plants. FEBS Lett 581:2247–2254. doi:10.1016/j.febslet.2007.04.014
Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216. doi:10.1016/j.envexpbot.2005.12.006
Athar HUR, Khan A, Ashraf M (2008) Exogenously applied ascorbic acid alleviates salt-induced oxidative stress in wheat. Environ Exp Bot 63:224–231. doi:10.1016/j.envexpbot.2007.10.018
Ausubel F, Benfey P (2002) Arabidopsis functional genomics. Plant Physiol 129:393–393. doi:10.1104/Pp.900036
Babiychuk E, Kushnir S, Belles-Boix E, Van Montagu M, Inzé D (1995) Arabidopsis thaliana NADPH oxidoreductase homologs confer tolerance of yeasts toward the thiol-oxidizing drug diamide. J Biol Chem 270:26224–26231. doi:10.1074/jbc.270.44.26224
Badawi GH, Yamauchi Y, Shimada E, Sasaki R, Kawano N, Tanaka K, Tanaka K (2004) Enhanced tolerance to salt stress and water deficit by overexpressing superoxide dismutase in tobacco (Nicotiana tabacum) chloroplasts. Plant Sci 166:919–928. doi:10.1016/j.plantsci.2003.12.007
Begcy K, Mariano ED, Mattiello L, Nunes AV, Mazzafera P, Maia IG, Menossi M (2011) An Arabidopsis mitochondrial uncoupling protein confers tolerance to drought and salt stress in transgenic tobacco plants. PLoS ONE 6:1–9. doi:10.1371/journal.pone.0023776
Belkhodja R, Morales F, Abadia A, Gomezaparisi J, Abadia J (1994) Chlorophyll fluorescence as a possible tool for salinity tolerance screening in barley (Hordeum vulgare L). Plant Physiol 104:667–673. doi:10.1104/pp.104.2.667
Benzarti M, Rejeb KB, Debez A, Messedi D, Abdelly C (2012) Photosynthetic activity and leaf antioxidative responses of Atriplex portulacoides subjected to extreme salinity. Acta Physiol Plant 34:1679–1688. doi:10.1007/s11738-012-0963-5
Bor M, Ozdemir F, Turkan I (2003) The effect of salt stress on lipid peroxidation and antioxidants in leaves of sugar beet Beta vulgaris L. and wild beet Beta maritima L. Plant Sci 164:77–84. doi:10.1016/S0168-9452(02)00338-2
Brugnoli E, Bjorkman O (1992) Growth of cotton under continuous salinity stress—influence on allocation pattern, stomatal and nonstomatal components of photosynthesis and dissipation of excess light energy. Planta 187:335–347
Chakraborty K, Sairam RK, Bhattacharya RC (2012) Salinity-induced expression of pyrrolline-5-carboxylate synthetase determines salinity tolerance in Brassica spp. Acta Physiol Plant 34:1935–1941. doi:10.1007/s11738-012-0994-y
Chang CS, Wang BL, Shi L, Li YX, Duo LA, Zhang WH (2010) Alleviation of salt stress-induced inhibition of seed germination in cucumber (Cucumis sativus L.) by ethylene and glutamate. J Plant Physiol 167:1152–1156. doi:10.1016/j.jplph.2010.03.018
Chattopadhayay MK, Tiwari BS, Chattopadhyay G, Bose A, Sengupta DN, Ghosh B (2002) Protective role of exogenous polyamines on salinity-stressed rice (Oryza sativa) plants. Physiol Plant 116:192–199. doi:10.1034/j.1399-3054.2002.1160208.x
Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Annu Bot 103:551–560. doi:10.1093/Aob/Mcn125
Chen S, Polle A (2010) Salinity tolerance of Populus. Plant Biol 12:317–333. doi:10.1111/j.1438-8677.2009.00301.x
Chen HX, Li WJ, An SZ, Gao HY (2004) Characterization of PSII photochemistry and thermostability in salt-treated Rumex leaves. J Plant Physiol 161:257–264. doi:10.1078/0176-1617-01231
Chen HX, Li PM, Gao HY (2007) Alleviation of photoinhibition by calcium supplement in salt-treated Rumex leaves. Physiol Plant 129:386–396. doi:10.1111/j.1399-3054.2006.00830.x
Chen LS, Li P, Cheng L (2008) Effects of high temperature coupled with high light on the balance between photooxidation and photoprotection in the sun-exposed peel of apple. Planta 228:745–756. doi:10.1007/s00425-008-0776-3
Chen Q, Zhang M, Shen S (2010) Effect of salt on malondialdehyde and antioxidant enzymes in seedling roots of Jerusalem artichoke (Helianthus tuberosus L.). Acta Physiol Plant 32:27–36. doi:10.1007/s11738-009-0371-7
Cimrin KM, Turkmen O, Turan M, Tuncer B (2010) Phosphorus and humic acid application alleviate salinity stress of pepper seedling. Afr J Biotech 9:5845–5851. doi:10.5897/AJB10.384
Colmer TD, Flowers TJ, Munns R (2006) Use of wild relatives to improve salt tolerance in wheat. J Exp Bot 57:1059–1078. doi:10.1093/Jxb/Erj124
Cuin TA, Miller AJ, Laurie SA, Leigh RA (2003) Potassium activities in cell compartments of salt-grown barley leaves. J Exp Bot 54:657–661. doi:10.1093/Jxb/Erg072
D’Souza MR, Devaraj VR (2010) Biochemical responses of Hyacinth bean (Lablab purpureus) to salinity stress. Acta Physiol Plant 32:341–353. doi:10.1007/s11738-009-0412-2
Dasgupta N, Nandy P, Das S (2011) Photosynthesis and antioxidative enzyme activities in five Indian mangroves with respect to their adaptability. Acta Physiol Plant 33:803–810. doi:10.1007/s11738-010-0605-8
Demiral T, Turkan I (2004) Does exogenous glycinebetaine affect antioxidative system of rice seedlings under NaCl treatment? J Plant Physiol 161:1089–1100. doi:10.1016/j.jplph.2004.03.009
Demiral T, Turkan I (2005) Comparative lipid peroxidation, antioxidant defense systems and proline content in roots of two rice cultivars differing in salt tolerance. Environ Exp Bot 53:247–257. doi:10.1016/j.envexpbot.2004.03.017
Demiral T, Turkan I (2006) Exogenous glycinebetaine affects growth and proline accumulation and retards senescence in two rice cultivars under NaCl stress. Environ Exp Bot 56:72–79. doi:10.1016/j.envexpbot.2005.01.005
Dionisio-Sese ML, Tobita S (1998) Antioxidant responses of rice seedlings to salinity stress. Plant Sci 135:1–9. doi:10.1016/S0168-9452(98)00025-9
Dixon RA (2005) Plant biotechnology kicks off into the 21st century. Trends Plant Sci 10:560–561. doi:10.1016/j.tplants.2005.10.011
Downton WJS, Grant WJR, Robinson SP (1985) Photosynthetic and stomatal responses of spinach leaves to salt stress. Plant Physiol 78:85–88. doi:10.1104/Pp.78.1.85
Dufty AM, Clobert J, Moller AP (2002) Hormones, developmental plasticity and adaptation. Trends Ecol Evol 17:190–196. doi:10.1016/S0169-5347(02)02498-9
Dvorak J, Noaman MM, Goyal S, Gorham J (1994) Enhancement of the salt tolerance of Triticum turgidum L. by the kna1 locus transferred from the Triticum aestivum L. chromosome 4d by homoeologous recombination. Theor Appl Genet 87:872–877. doi:10.1007/Bf00221141
Everard JD, Gucci R, Kann SC, Flore JA, Loescher WH (1994) Gas-exchange and carbon partitioning in the leaves of celery (Apium graveolens L.) at various levels of root-zone salinity. Plant Physiol 106:281–292. doi:10.1104/pp.106.1.281
Fallon KM, Phillips R (1989) Responses to water-stress in adapted and unadapted carrot cell-suspension cultures. J Exp Bot 40:681–687. doi:10.1093/Jxb/40.6.681
Fan ML, Bie ZL, Krumbein A, Schwarz D (2011) Salinity stress in tomatoes can be alleviated by grafting and potassium depending on the rootstock and K-concentration employed. Sci Hortic 130:615–623. doi:10.1016/j.scienta.2011.08.018
FAO (2008) FAO land and plant nutrition management service. Available at http://www.fao.org/ag/agl/agll/spush
Flexas J, Bota J, Loreto F, Cornic G, Sharkey TD (2004) Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants. Plant Biol 6:269–279. doi:10.1055/s-2004-820867
Flowers TJ (2004) Improving crop salt tolerance. J Exp Bot 55:307–319. doi:10.1093/Jxb/Erh003
Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol 179:945–963. doi:10.1111/j.1469-8137.2008.02531.x
Flowers TJ, Troke PF, Yeo AR (1977) Mechanism of salt tolerance in halophytes. Annu Rev Plant Physiol 28:89–121. doi:10.1146/annurev.pp.28.060177.000513
Foyer CH, Souriau N, Perret S, Lelandais M, Kunert KJ, Pruvost C, Jouanin L (1995) Overexpression of glutathione-reductase but not glutathione synthetase leads to increases in antioxidant capacity and resistance to photoinhibition in poplar trees. Plant Physiol 109:1047–1057. doi:10.1104/pp.109.3.1047
Fricke W, Akhiyarova G, Veselov D, Kudoyarova G (2004) Rapid and tissue-specific changes in ABA and in growth rate in response to salinity in barley leaves. J Exp Bot 55:1115–1123. doi:10.1093/Jxb/Erh117
Fricke W, Akhiyarova G, Wei WX, Alexandersson E, Miller A, Kjellbom PO, Richardson A, Wojciechowski T, Schreiber L, Veselov D, Kudoyarova G, Volkov V (2006) The short-term growth response to salt of the developing barley leaf. J Exp Bot 57:1079–1095. doi:10.1093/Jxb/Erj095
Gaxiola R, Delarrinoa IF, Villalba JM, Serrano R (1992) A novel and conserved salt-induced protein is an important determinant of salt tolerance in yeast. EMBO J 11:3157–3164
Glombitza S, Dubuis PH, Thulke O, Welzl G, Bovet L, Gotz M, Affenzeller M, Geist B, Hehn A, Asnaghi C, Ernst D, Seidlitz HK, Gundlach H, Mayer KF, Martinoia E, Werck-Reichhart D, Mauch F, Schaffner AR (2004) Crosstalk and differential response to abiotic and biotic stressors reflected at the transcriptional level of effector genes from secondary metabolism. Plant Mol Biol 54:817–835. doi:10.1007/s11103-004-0274-3
Gorai M, Ennajeh M, Khemira H, Neffati M (2011) Influence of NaCl-salinity on growth, photosynthesis, water relations and solute accumulation in Phragmites australis. Acta Physiol Plant 33:963–971. doi:10.1007/s11738-010-0628-1
Gorham J, Bristol A, Young EM, Jones RGW (1991) The presence of the enhanced K/Na discrimination trait in diploid Triticum species. Theor Appl Genet 82:729–736
Gossett DR, Millhollon EP, Lucas MC (1994) Antioxidant response to Nacl stress in salt-tolerant and salt-sensitive cultivars of cotton. Crop Sci 34:706–714
Greenway H, Munns R (1980) Mechanisms of salt tolerance in non-halophytes. Annu Rev Plant Physiol 31:149–190. doi:10.1146/annurev.pp.31.060180.001053
GuetaDahan Y, Yaniv Z, Zilinskas BA, BenHayyim G (1997) Salt and oxidative stress: similar and specific responses and their relation to salt tolerance in Citrus. Planta 203:460–469. doi:10.1007/s004250050215
Hao YJ, Wei W, Song QX, Chen HW, Zhang YQ, Wang F, Zou HF, Lei G, Tian AG, Zhang WK, Ma B, Zhang JS, Chen SY (2011) Soybean NAC transcription factors promote abiotic stress tolerance and lateral root formation in transgenic plants. Plant J. 68:302–313. doi:10.1111/j.1365-313X.2011.04687.x
Hare PD, Cress WA (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul 21:79–102. doi:10.1023/A:1005703923347
Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol 51:463–499. doi:10.1146/annurev.arplant.51.1.463
He ZX, Ruan CJ, Qin P, Seliskar DM, Gallagher JL (2003) Kosteletzkya virginica, a halophytic species with potential for agroecotechnology in Jiangsu Province. China Ecol Eng 21:271–276. doi:10.1016/j.ecoleng.2004.01.001
Hernandez JA, Olmos E, Corpas FJ, Sevilla F, Delrio LA (1995) Salt-induced oxidative stress in chloroplasts of pea plants. Plant Sci 105:151–167. doi:10.1016/0168-9452(94)04047-8
Hernandez JA, Jimenez A, Mullineaux P, Sevilla F (2000) Tolerance of pea (Pisum sativum L.) to long-term salt stress is associated with induction of antioxidant defences. Plant Cell Environ 23:853–862. doi:10.1046/j.1365-3040.2000.00602.x
Hsu SY, Kao CH (2003) Differential effect of sorbitol and polyethylene glycol on antioxidant enzymes in rice leaves. Plant Growth Regul 39:83–90. doi:10.1023/A:1021830926902
Idrees M, Naeem M, Aftab T, Khan MAM, Moinuddin (2011) Salicylic acid mitigates salinity stress by improving antioxidant defence system and enhances vincristine and vinblastine alkaloids production in periwinkle [Catharanthus roseus (L.) G. Don]. Acta Physiol Plant 33:987–999. doi:10.1007/s11738-010-0631-6
Islam S, Malik AI, Islam AKMR, Colmer TD (2007) Salt tolerance in a Hordeum marinum-Triticum aestivum amphiploid, and its parents. J Exp Bot 58:1219–1229. doi:10.1093/Jxb/Erl293
Jacobs A, Ford K, Kretschmer J, Tester M (2011) Rice plants expressing the moss sodium pumping Atpase PpENA1 maintain greater biomass production under salt stress. Plant Biotech J 9:838–847. doi:10.1111/j.1467-7652.2011.00594.x
Jaleel CA, Riadh K, Gopi R, Manivannan P, Ines J, Al-Juburi HJ, Zhao CX, Shao HB, Panneerselvam R (2009) Antioxidant defense responses: physiological plasticity in higher plants under abiotic constraints. Acta Physiol Plant 31:427–436. doi:10.1007/s11738-009-0275-6
Jedmowski C, Ashoub A, Bruggemann W (2013) Reactions of Egyptian landraces of Hordeum vulgare and Sorghum bicolor to drought stress, evaluated by the OJIP fluorescence transient analysis. Acta Physiol Plant 35:345–354. doi:10.1007/s11738-012-1077-9
Kaya C, Tuna AL, Ashraf M, Altunlu H (2007) Improved salt tolerance of melon (Cucumis melo L.) by the addition of proline and potassium nitrate. Environ Exp Bot 60:397–403. doi:10.1016/j.envexpbot.2006.12.008
Khan N, Syeed S, Masood A, Nazar R, Iqbal N (2010) Application of salicylic acid increases contents of nutrients and antioxidative metabolism in mungbean and alleviates adverse effects of salinity stress. Inter J Plant Biol 1:1–8. doi:10.4081/pb.2010.e1
Koca H, Ozdemir F, Turkan I (2006) Effect of salt stress on lipid peroxidation and superoxide dismutase and peroxidase activities of Lycopersicon esculentum and L. pennellii. Biol Plant 50:745–748. doi:10.1007/s10535-006-0121-2
Koca H, Bor M, Ozdemir F, Turkan I (2007) The effect of salt stress on lipid peroxidation, antioxidative enzymes and proline content of sesame cultivars. Environ Exp Bot 60:344–351. doi:10.1016/j.envexpbot.2006.12.005
Koskeroglu S, Tuna AL (2010) The investigation on accumulation levels of proline and stress parameters of the maize (Zea mays L.) plants under salt and water stress. Acta Physiol Plant 32:541–549. doi:10.1007/s11738-009-0431-z
Ksouri R, Megdiche W, Debez A, Falleh H, Grignon C, Abdelly C (2007) Salinity effects on polyphenol content and antioxidant activities in leaves of the halophyte Cakile maritima. Plant Physiol Biochem 45:244–249. doi:10.1016/j.plaphy.2007.02.001
Li PM, Cheng LL, Gao HY, Jiang CD, Peng T (2009) Heterogeneous behavior of PSII in soybean (Glycine max) leaves with identical PSII photochemistry efficiency under different high temperature treatments. J Plant Physiol 166:1607–1615. doi:10.1016/j.jplph.2009.04.013
Li ZR, Li G, Qin P (2010) The prediction of ecological potential for developing salt-tolerant oil plants on coastal saline land in Sheyang Saltern. China Ecol Eng 36:27–35. doi:10.1016/j.ecoleng.2009.09.006
Lin SH, Liu ZJ, Xu PL, Fang YY, Bai JG (2011) Paraquat pre-treatment increases activities of antioxidant enzymes and reduces lipid peroxidation in salt-stressed cucumber leaves. Acta Physiol Plant 33:295–304. doi:10.1007/s11738-010-0547-1
Long XH, Mehta SK, Liu ZP (2008) Effect of NO3–N enrichment on seawater stress tolerance of Jerusalem artichoke (Helianthus tuberosus). Pedosphere 18:113–123
Long XH, Chi JH, Liu L, Li Q, Liu ZP (2009) Effect of seawater stress on physiological and biochemical responses of five Jerusalem artichoke ecotypes. Pedosphere 19:208–216
Loreto F, Centritto M, Chartzoulakis K (2003) Photosynthetic limitations in olive cultivars with different sensitivity to salt stress. Plant Cell Environ 26:595–601. doi:10.1046/j.1365-3040.2003.00994.x
Lu CM, Qiu NW, Lu QT, Wang BS, Kuang TY (2002) Does salt stress lead to increased susceptibility of photosystem II to photoinhibition and changes in photosynthetic pigment composition in halophyte Suaeda salsa grown outdoors? Plant Sci 163:1063–1068. doi:10.1016/S0168-9452(02)00281-9
Lu CM, Jiang GM, Wang BS, Kuang TY (2003a) Photosystem II photochemistry and photosynthetic pigment composition in salt-adapted halophyte Artimisia anethifolia grown under outdoor conditions. J Plant Physiol 160:403–408. doi:10.1078/0176-1617-00839
Lu CM, Qiu NW, Wang BS, Zhang JH (2003b) Salinity treatment shows no effects on photosystem II photochemistry, but increases the resistance of photosystem II to heat stress in halophyte Suaeda salsa. J Exp Bot 54:851–860. doi:10.1093/Jxb/Erg080
Luo QY, Yu BJ, Liu YL (2005) Differential sensitivity to chloride and sodium ions in seedlings of Glycine max and G. soja under NaCl stress. J Plant Physiol 162:1003–1012. doi:10.1016/j.jplph.2004.11.008
Maathuis FJM, Amtmann A (1999) K+ nutrition and Na+ toxicity: the basis of cellular K+/Na+ ratios. Annu Bot 84:123–133. doi:10.1006/anbo.1999.0912
Mansour MMF (2000) Nitrogen containing compounds and adaptation of plants to salinity stress. Biol Plant 43:491–500. doi:10.1023/A:1002873531707
Mehta P, Jajoo A, Mathur S, Bharti S (2010) Chlorophyll a fluorescence study revealing effects of high salt stress on Photosystem II in wheat leaves. Plant Physiol Biochem 48:16–20. doi:10.1016/j.plaphy.2009.10.006
Meneguzzo S, Navari-Izzo F, Izzo R (1999) Antioxidative responses of shoots and roots of wheat to increasing NaCl concentrations. J Plant Physiol 155:274–280
Meyerowitz EM (2002) Comparative genomics—plants compared to animals: the broadest comparative study of development. Science 295:1482–1485. doi:10.1126/science.1066609
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410. doi:10.1016/S1360-1385(02)02312-9
Mittova V, Tal M, Volokita M, Guy M (2003) Up-regulation of the leaf mitochondrial and peroxisomal antioxidative systems in response to salt-induced oxidative stress in the wild salt-tolerant tomato species Lycopersicon pennellii. Plant Cell Environ 26:845–856. doi:10.1046/j.1365-3040.2003.01016.x
Mohanty A, Kathuria H, Ferjani A, Sakamoto A, Mohanty P, Murata N, Tyagi AK (2002) Transgenics of an elite indica rice variety pusa basmati 1 harbouring the coda gene are highly tolerant to salt stress. Theor Appl Genet 106:51–57. doi:10.1007/s00122-002-1063-5
Morales F, Abadia A, Gomezaparisi J, Abadia J (1992) Effects of combined NaCl and CaCl2 salinity on photosynthetic parameters of barley grown in nutrient solution. Physiol Plant 86:419–426. doi:10.1034/j.1399-3054.1992.860311.x
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681. doi:10.1146/annurev.arplant.59.032607.092911
Nazar R, Iqbal N, Syeed S, Khan NA (2011) Salicylic acid alleviates decreases in photosynthesis under salt stress by enhancing nitrogen and sulfur assimilation and antioxidant metabolism differentially in two mungbean cultivars. J Plant Physiol 168:807–815. doi:10.1016/j.jplph.2010.11.001
Netondo GW, Onyango JC, Beck E (2004) Sorghum and salinity: II. Gas exchange and chlorophyll fluorescence of sorghum under salt stress. Crop Sci 44:806–811
Pokorny R, Tomaskova I, Marek MV (2011) The effects of elevated atmospheric [CO2] on Norway spruce needle parameters. Acta Physiol Plant 33:2269–2277. doi:10.1007/s11738-011-0766-0
Rahnama H, Vakilian H, Fahimi H, Ghareyazie B (2011) Enhanced salt stress tolerance in transgenic potato plants (Solanum tuberosum L.) expressing a bacterial mtID gene. Acta Physiol Plant 33:1521–1532. doi:10.1007/s11738-010-0690-8
Rapacz M, Tyrka M, Kaczmarek W, Gut M, Wolanin B, Mikulski W (2008) Photosynthetic acclimation to cold as a potential physiological marker of winter barley freezing tolerance assessed under variable winter environment. J Agron Crop Sci 194:61–71. doi:10.1111/j.1439-037X.2007.00292.x
Rapacz M, Koscieiniak J, Jurczyk B, Adamska A, Wojcik M (2010) Different patterns of physiological and molecular response to drought in seedlings of malt- and feed-type barleys (Hordeum vulgare). J Agron Crop Sci 196:9–19. doi:10.1111/j.1439-037X.2009.00389.x
Reezi S, Babalar M, Kalantari S (2009) Silicon alleviates salt stress, decreases malondialdehyde content and affects petal color of salt-stressed cut rose (Rosa xhybrida L.) ‘Hot Lady’. Afr J Biotech 8:1502–1508. doi:10.5897/AJB09.180
Renault S (2012) Salinity tolerance of Cornus sericea seedlings from three provenances. Acta Physiol Plant 34:1735–1746. doi:10.1007/s11738-012-0970-6
Ruan CJ, Li H, Guo YQ, Qin P, Gallagher JL, Seliskar DM, Lutts S, Mahy G (2008) Kosteletzkya virginica, an agroecoengineering halophytic species for alternative agricultural production in China’s east coast: ecological adaptation and benefits, seed yield, oil content, fatty acid and biodiesel properties. Ecol Eng 32:320–328. doi:10.1016/j.ecoleng.2007.12.010
Sakr MT, El-Sarkassy NM, Fuller MP (2012) Osmoregulators proline and glycine betaine counteract salinity stress in canola. Agron Sustain Dev 32:747–754. doi:10.1007/s13593-011-0076-3
Salvucci ME, Crafts-Brandner SJ (2004) Inhibition of photosynthesis by heat stress: the activation state of Rubisco as a limiting factor in photosynthesis. Physiol Plant 120:179–186. doi:10.1111/j.0031-9317.2004.0173.x
Sekmen AH, Turkan I, Takio S (2007) Differential responses of antioxidative enzymes and lipid peroxidation to salt stress in salt-tolerant Plantago maritima and salt-sensitive Plantago media. Physiol Plant 131:399–411. doi:10.1111/j.1399-3054.2007.00970.x
Shabala S, Cuin TA (2008) Potassium transport and plant salt tolerance. Physiol Plant 133:651–669. doi:10.1111/j.1399-3054.2007.01008.x
Shabala S, Demidchik V, Shabala L, Cuin TA, Smith SJ, Miller AJ, Davies JM, Newman IA (2006) Extracellular Ca2+ ameliorates NaCl-induced K+ loss from Arabidopsis root and leaf cells by controlling plasma membrane K+-permeable channels. Plant Physiol 141:1653–1665. doi:10.1104/pp.106.082388
Shalata A, Mittova V, Volokita M, Guy M, Tal M (2001) Response of the cultivated tomato and its wild salt-tolerant relative Lycopersicon pennellii to salt-dependent oxidative stress: the root antioxidative system. Physiol Plant 112:487–494. doi:10.1080/10715760290006402
Shao HB, Liang ZS, Shao MA (2006) Osmotic regulation of 10 wheat (Triticum aestivum L.) genotypes at soil water deficits. Colloids Surf B Biointerfaces 47:132–139. doi:10.1016/j.colsurfb.2005.11.028
Shao HB, Chu LY, Lu ZH, Kang CM (2008) Primary antioxidant free radical scavenging and redox signaling pathways in higher plant cells. Int J Biol Sci 4:8–14
Shao HB, Jaleel CA, Shao MA (2009) Understanding water deficit stress-induced changes in basic metabolisms of higher plants for biotechnologically and sustainably improving agriculture and ecoenvironment in arid regions on the globe. Crit Rev Biotech 29:131–151. doi:10.1080/07388550902869792
Shao HB, Chu LY, Xu G, Yan K, Zhang LH, Guo DG (2010) Understanding molecular mechanisms for improving phytoremediation of heavy metal-contaminated soils. Crit Rev Biotech 30:23–30. doi:10.3109/07388550903208057
Sreenivasulu N, Grimm B, Wobus U, Weschke W (2000) Differential response of antioxidant compounds to salinity stress in salt-tolerant and salt-sensitive seedlings of foxtail millet (Setaria italica). Physiol Plant 109:435–442. doi:10.1034/j.1399-3054.2000.100410.x
Stewart CN (2005) Plant functional genomics: beyond the parts list. Trends Plant Sci 10:561–562. doi:10.1016/j.tplants.2005.10.010
Strasser RJ, Tsimilli-Micheal M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis. Advances in photosynthesis and respiration, vol 19. Springer, Berlin, pp 321–362
Strauss AJ, Kruger GHJ, Strasser RJ, van Heerden PDR (2007) The role of low soil temperature in the inhibition of growth and PSII function during dark chilling in soybean genotypes of contrasting tolerance. Physiol Plant 131:89–105. doi:10.1111/j.1399-3054.2007.00930.x
Tarchoune I, Degl’Innocenti E, Kaddour R, Guidi L, Lachaal M, Navari-Izzo F, Ouerghi Z (2012) Effects of NaCl or Na2SO4 salinity on plant growth, ion content and photosynthetic activity in Ocimum basilicum L. Acta Physiol Plant 34:607–615. doi:10.1007/s11738-011-0861-2
Tausz M, Grulke NE, Wieser G (2007) Defense and avoidance of ozone under global change. Environ Pollut 147:525–531. doi:10.1016/j.envpol.2006.08.042
Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Annu Bot 91:503–527. doi:10.1093/Aob/Mcg058
Tholen D, Ethier G, Genty B, Pepin S, Zhu XG (2012) Variable mesophyll conductance revisited: theoretical background and experimental implications. Plant Cell Environ 35:2087–2103. doi:10.1111/j.1365-3040.2012.02538.x
Toth SZ, Schansker G, Garab G, Strasser RJ (2007) Photosynthetic electron transport activity in heat-treated barley leaves: the role of internal alternative electron donors to photosystem II. Biochim Biophys Acta 1767:295–305. doi:10.1016/j.bbabio.2007.02.019
Treutter D (2006) Significance of flavonoids in plant resistance: a review. Environ Chem Lett 4:147–157. doi:10.1007/s10311-006-0068-8
Tseng MJ, Liu CW, Yiu JC (2007) Enhanced tolerance to sulfur dioxide and salt stress of transgenic Chinese cabbage plants expressing both superoxide dismutase and catalase in chloroplasts. Plant Physiol Biochem 45:822–833. doi:10.1016/j.plaphy.2007.07.011
Turkan I, Demiral T (2009) Recent developments in understanding salinity tolerance. Environ Exp Bot 67:2–9. doi:10.1016/j.envexpbot.2009.05.008
Turkan I, Bor M, Ozdemir F, Koca H (2005) Differential responses of lipid peroxidation and antioxidants in the leaves of drought-tolerant P. acutifolius gray and drought-sensitive P. vulgaris L. Subjected to polyethylene glycol mediated water stress. Plant Sci 168:223–231. doi:10.1016/j.plantsci.2004.07.032
Umezawa T, Shimizu K, Kato M, Ueda T (2000) Enhancement of salt tolerance in soybean with NaCl pretreatment. Physiol Plant 110:59–63. doi:10.1034/j.1399-3054.2000.110108.x
Van Montagu M (2005) Technological milestones from plant science to agricultural biotechnology. Trends Plant Sci 10:559–560. doi:10.1016/j.tplants.2005.10.013
Venkatesan A, Chellappan KP (1998) Accumulation of proline and glycine betaine in Ipomoea pes-caprae induced by NaCl. Biol Plant 41:271–276. doi:10.1023/A:1001839302627
Voncaemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153:376–387. doi:10.1007/BF00384257
Wahid A, Ghazanfar A (2006) Possible involvement of some secondary metabolites in salt tolerance of sugarcane. J Plant Physiol 163:723–730. doi:10.1016/j.jplph.2005.07.007
Wahid A, Perveen M, Gelani S, Basra SMA (2007) Pretreatment of seed with H2O2 improves salt tolerance of wheat seedlings by alleviation of oxidative damage and expression of stress proteins. J Plant Physiol 164:283–294. doi:10.1016/j.jplph.2006.01.005
Wang J, Zhang H, Allen RD (1999) Overexpression of an Arabidopsis peroxisomal ascorbate peroxidase gene in tobacco increases protection against oxidative stress. Plant Cell Physiol 40:725–732
Wei Q, Guo YJ, Cao HM, Kuai BK (2011) Cloning and characterization of an AtNEX2-like Na+/H+ antiporter gene from Ammopiptanthus mongolicus (Leguminosae) and its ectopic expression enhanced drought and salt tolerance in Arabidopsis thaliana. Plant Cell Tissue Organ Cult 105:309–316. doi:10.1007/s11240-010-9869-3
Weimberg R, Lerner HR, Poljakoffmayber A (1984) Changes in growth and water soluble solute concentrations in sorghum bicolor stressed with sodium and potassium salts. Physiol Plant 62:472–480. doi:10.1111/j.1399-3054.1984.tb04605.x
Wen XG, Qiu NW, Lu QT, Lu CM (2005) Enhanced thermotolerance of photosystem II in salt-adapted plants of the halophyte Artemisia anethifolia. Planta 220:486–497. doi:10.1007/s00425-004-1382-7
Wu XH, Zhang HS, Li G, Liu XC, Qin P (2012) Ameliorative effect of castor bean (Ricinus communis L.) planting on physico-chemical and biological properties of seashore saline soil. Ecol Eng 38:97–100. doi:10.1016/j.ecoleng.2011.10.016
Xu S, Lou T, Zhao N, Gao Y, Dong L, Jiang D, Shen W, Huang L, Wang R (2011) Presoaking with hemin improves salinity tolerance during wheat seed germination. Acta Physiol Plant 33:1173–1183. doi:10.1007/s11738-010-0645-0
Yan K, Chen N, Qu YY, Dong XC, Meng QW, Zhao SJ (2008) Overexpression of sweet pepper Glycerol-3-Phosphate acyltransferase gene enhanced thermotolerance of photosynthetic apparatus in transgenic tobacco. J Integr Plant Biol 50:613–621. doi:10.1111/j.1744-7909.2008.00652.x
Yan K, Chen P, Shao H, Zhang L, Xu G (2011) Effects of short-term high temperature on photosynthesis and photosystem II performance in sorghum. J Agron Crop Sci 197:400–408. doi:10.1111/j.1439-037X.2011.00469.x
Yan K, Chen P, Shao HB, Zhao SJ, Zhang LH, Zhang LW, Xu G, Sun JN (2012) Photosynthetic characterization of Jerusalem artichoke during leaf expansion. Acta Physiol Plant 34:353–360. doi:10.1007/s11738-011-0834-5
Yang XH, Lu CM (2005) Photosynthesis is improved by exogenous glycinebetaine in salt-stressed maize plants. Physiol Plant 124:343–352. doi:10.1111/j.1399-3054.2005.00518.x
Yang WJ, Rich PJ, Axtell JD, Wood KV, Bonham CC, Ejeta G, Mickelbart MV, Rhodes D (2003) Genotypic variation for glycinebetaine in sorghum. Crop Sci 43:162–169
Yang XH, Wen XG, Gong HM, Lu QT, Yang ZP, Tang YL, Liang Z, Lu CM (2007) Genetic engineering of the biosynthesis of glycinebetaine enhances thermotolerance of photosystem II in tobacco plants. Planta 225:719–733. doi:10.1007/s00425-006-0380-3
Yang XH, Liang Z, Wen XG, Lu CM (2008) Genetic engineering of the biosynthesis of glycinebetaine leads to increased tolerance of photosynthesis to salt stress in transgenic tobacco plants. Plant Mol Biol 66:73–86. doi:10.1007/s11103-007-9253-9
Yazici I, Tuerkan I, Sekmen AH, Demiral T (2007) Salinity tolerance of purslane (Portulaca oleracea L.) is achieved by enhanced antioxidative system, lower level of lipid peroxidation and proline accumulation. Environ Exp Bot 61:49–57. doi:10.1016/j.envexpbot.2007.02.010
Zhang ZS, Jia YJ, Gao HY, Zhang LT, Li HD, Meng QW (2011) Characterization of PSI recovery after chilling-induced photoinhibition in cucumber (Cucumis sativus L.) leaves. Planta 234:883–889. doi:10.1007/s00425-011-1447-3
Zheng YH, Jia AJ, Ning TY, Xu JL, Li ZJ, Jiang GM (2008) Potassium nitrate application alleviates sodium chloride stress in winter wheat cultivars differing in salt tolerance. J Plant Physiol 165:1455–1465. doi:10.1016/j.jplph.2008.01.001
Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445. doi:10.1016/S1369-5266(03)00085-2
Acknowledgments
This work was jointly supported by National Natural Science Foundation of China (No. 41201292; 41171216; 41001137; 31100313), One Hundred-Talent Plan of Chinese Academy of Sciences (CAS), the Opening Foundation of the State Key Laboratory of Crop Biology, Shandong Agriculture University (2011KF02), the Project of Shandong Provincial Technology Development plan (2010GSF10208), the CAS/SAFEA International Partnership Program for Creative Research Teams, the Science and Technology Development Plan of Yantai City (2011016), CAS VISITING PROFESSORSHIP (2012T1Z0010), The Strategic Priority Research Program of the Chinese Academy of Sciences (XDA01020304), Yantai Double hundred High-end Talent Plan (XY-003-02) and 135 Development Plan of YIC-CAS.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by A. K. Kononowicz.
Rights and permissions
About this article
Cite this article
Yan, K., Shao, H., Shao, C. et al. Physiological adaptive mechanisms of plants grown in saline soil and implications for sustainable saline agriculture in coastal zone. Acta Physiol Plant 35, 2867–2878 (2013). https://doi.org/10.1007/s11738-013-1325-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11738-013-1325-7