Prospects of Halophytes in Understanding and Managing Abiotic Stress Tolerance



Halophytes are a diverse group of plants with tolerance to high salinity. While most of our crops are glycophytes lacking the genetic makeup for salt tolerance, halophytes are endowed with ability to seize NaCl into their cell vacuoles as an osmoticum. The sensitivity of crops to environmental extremities has become a major limitation to worldwide food production. Study of halophytes can be rewarding as the mechanisms by which halophytes survive and maintain productivity on saline water can be understood to define and manage adaptations in glycophytes. The adaptation mechanisms include ion compartmentalization, osmotic adjustment, succulence, ion transport and uptake, antioxidant systems, maintenance of redox and energetic status, and salt inclusion/excretion. Real benefits can be accrued if sustained efforts are in place to investigate the species-­specific regulation during abiotic stresses and extend genetic resource and manipulate stress tolerance mechanisms. Halophytes are also an important plant species with potential for the purposes of desalination and restoration of saline soils, withstand high soil salinity and saline water irrigation, phytoremediation and wetland restoration. It will be invaluable to develop these strategies to ensure sustainability, and future efforts to improve crop performance on marginal and irrigated land.


Halophytes Abiotic stress Compatible solutes Antioxidants Phytoremediation 


  1. Abdelly C, Lachaal M, Grignon C, Soltani A, Hajji M (1995) Association episodique d’halophytes strictes et de glycophytes dans un ecosysteme hydromorphe sale en zone semi-aride. Agronomie 15:557–568Google Scholar
  2. Aken BV (2008) Transgenic plants for phytoremediation: helping nature to clean up environmental pollution. Cell 26:225–227Google Scholar
  3. Almeida CMR, Mucha AP, Vascancelos MTSD (2006) Variability of metal contents in the sea rush Juncus maritimus-estuarine sediment system through one year of plant’s life. Mar Environ Res 61:424–438PubMedGoogle Scholar
  4. Almeida CMR, Dias AC, Mucha AP, Bordalo AA, Vascancelos MTSD (2009) Study of the influence of different organic pollutants on Cu accumulation by Halimione portulacoides. Estuar Coast Shelf Sci 85:627–632Google Scholar
  5. Amtmann A (2009) Learning from evolution: Thellungiella generates new knowledge on essential and critical components of abiotic stress tolerance in Plants. Mol Plant 2:3–12PubMedGoogle Scholar
  6. Apse MP, Blumwald E (2007) Na+ transport in plants. FEBS Lett 581:2247–2254PubMedGoogle Scholar
  7. Aronson JA (1989) HALOPH a data base of salt tolerant plants of the world. Office Arid Land Studies, University of Arizona, TucsonGoogle Scholar
  8. Ashraf M (2009) Biotechnological approach of improving plant salt tolerance using antioxidants as markers. Biotechnol Adv 27:84–93PubMedGoogle Scholar
  9. Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216Google Scholar
  10. Attipali RR, Kolluru VC, Munusamy V (2004) Drought induced responses of photosynthesis and antioxidant metabolism in higher plants. J Plant Physiol 161:1189–1202Google Scholar
  11. Ball MC (1988) Ecophysiology of mangroves. Trees 2:129–143Google Scholar
  12. Bao-Yan AN, Yan L, Jia-Rui L, Wei-Hua Q, Xian-Sheng Z, Xin-Qi Z (2002) Expression of a vacuolar Na+/H+ antiporter gene of alfalfa enhances salinity tolerance in transgenic  Arabidopsis. Acta Agron Sin 34:557–564Google Scholar
  13. Ben Amor N, Ben Hamed K, Debez A, Grignon C, Abdelly C (2005) Physiological and antioxidant responses of the perennial halophyte Crithmum maritimum to salinity. Plant Sci 68:889–899Google Scholar
  14. Blumwald E (2000) Sodium transport and salt tolerance in plants. Curr Opin Cell Biol 12:431–434PubMedGoogle Scholar
  15. Bohnert HJ, Sheveleva E (1998) Plant stress adaptations-making metabolism move. Curr Opin Plant Biol 1:267–274PubMedGoogle Scholar
  16. Bohnert HJ, Gong Q, Li P, Ma S (2006) Unraveling abiotic stress tolerance mechanisms – getting genomics going. Curr Opin Plant Biol 9:180–188PubMedGoogle Scholar
  17. Bor MF, 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 maritime L. Plant Sci 164:77–84Google Scholar
  18. Breckel SW (2002) Salinity, halophytes and salt affected natural ecosystems. In: Lauchli A, Luttge U (eds) Salinity: environment-plants-molecules. Kluwer, Dordrecht, pp 53–77Google Scholar
  19. Breyne P, Zabeau M (2001) Genome-wide expression analysis of plant cell cycle modulated genes. Curr Opin Plant Biol 4:136–142PubMedGoogle Scholar
  20. Briens M, Larher F (1982) Osmoregulation in halophytic higher plants: a comparative study of soluble carbohydrates, polyols, betaines and free proline. Plant Cell Environ 5:287–292Google Scholar
  21. Brockmeyer RE Jr, Rey JR, Virnstein RW, Gilmore RG, Ernest L (1997) Rehabilitation of impounded estuarine wetlands by hydrologic reconnection to the Indian River Lagoon, Florida (USA). Wetland Ecol Manag 4:93–109Google Scholar
  22. Cambrolle J, Redondo-Gomez S, Mateos-Naranjo E, Figueroa ME (2008) Comparison of the role of two Spartina species in terms of phytostabilization and bioaccumulation of metals in the estuarine sediment. Mar Pollut Bull 56:2037–2042PubMedGoogle Scholar
  23. Carias CC, Novais JM, Martins-Dias S (2008) Are Phragmites australis enzymes involved in the degradation of the textile azo dye acid orange 7? Bioresour Technol 99:243–251PubMedGoogle Scholar
  24. Castro R, Pereira S, Lima A, Corticeiro S, Valega M, Pereira E, Duarte A, Figueira E (2009) Accumulation, distribution and cellular partitioning of mercury in several halophytes of a contaminated salt marsh. Chemosphere 76:1348–1355PubMedGoogle Scholar
  25. Chai CL, Li SH, Xu YC (2001) Carbohydrate metabolism in peach leaves during water stress and after stress relief. Plant Physiol Commun 37:495–498Google Scholar
  26. Chen XY, Tsang EPK, Chan ALW (2003) Heavy metal contents in sediments, mangroves and bivalves from Ting Kok, Hong Kong. China Environ Sci 23:480–484Google Scholar
  27. Cherian S, Reddy MP, Pandya JB (1999) Studies on salt tolerance in Avicennia marina (Forsk.) Vierh.: effect of NaCl salinity on growth, ion accumulation and enzyme activity. Indian J Plant Physiol 4:266–270Google Scholar
  28. Cherian S, Reddy MP (2003) Evaluation of NaCl tolerance in the callus cultures of Suaeda nudiflora Moq. Biol Plant 46:193–198Google Scholar
  29. Chiu CY, Hsiu FS, Chen SS, Chou CH (1995) Reduced toxicity of Cu and Zn to mangrove seedlings (Kandelia candel (L.) Druce.) in saline environments. Bot Bull Acad Sin 36:19–24Google Scholar
  30. Coleman J, Hench K, Garbutt K, Sexstone A, Bissonnette G, Skousen J (2001) Treatment of domestic wastewater by three plant species in constructed wetlands. Water Air Soil Pollut 128:283–295Google Scholar
  31. Colmer TD, Flowers TJ (2008) Flooding tolerance in halophytes. New Phytol 179:964–974PubMedGoogle Scholar
  32. Cushman JC (2001) Osmoregulation in plants: implications for agriculture. Am Zool 41:758–769Google Scholar
  33. Cushman JC (2003) Functional genomics of plant abiotic stress tolerance. In: Prade RA, Bohnert HJ (eds) Genomics of plants and fungi. Marcel Dekker, New York, pp 315–357, 18Google Scholar
  34. Cushman JC, Bohnert HJ (2000) Genomic approaches to plant stress tolerance. Curr Opin Plant Biol 3:117–124PubMedGoogle Scholar
  35. Delauney AJ, Verma DPS (1993) Proline biosynthesis and osmoregulation in plants. Plant J 4:215–223Google Scholar
  36. Eid MA, Eisa SS (2010) The use of some halophytic plants to reduce Zn, Cu and Ni in soil. Aust J Basic Appl Sci 4:1590–1596Google Scholar
  37. Epstein E (1980) Response of plants to saline environments. In: Rains DW, Valentine RC, Hollaender A (eds) Genetic engineering of osmoregulation. Plenum, New York, pp 7–21Google Scholar
  38. Fan W, Zhang Z, Zhang Y (2009) Cloning and molecular characterization of fructose-1,6-bisphosphate aldolase gene regulated by high-salinity and drought in Sesuvium portulacastrum. Plant Cell Rep. doi:10.1007/s00299-009-0702-6
  39. Fang ZQ, Yuan LY, Hong PC, Ming LC, Shan WB (2005) NaCl enhances thylakoid-bound SOD activity in the leaves of C3 halophyte Suaeda salsa L. Plant Sci 168:423–430Google Scholar
  40. Fang Q, Xu Z, Song R (2006) Cloning, characterization and genetic engineering of FLC homolog in Thellungiella halophila. Biochem Biophys Res Commun 347:707–714PubMedGoogle Scholar
  41. Fitzgerald EJ, Caffrey JM, Nesaratnam ST, McLoughlin P (2003) Copper and lead concentrations in salt marsh plants on the suir Estuary. Ireland Environ Pollut 123:67–74Google Scholar
  42. Flowers TJ (1985) Physiology of halophytes. Plant Soil 89:41–56Google Scholar
  43. Flowers TJ (2004) Improving crop salt tolerance. J Exp Bot 55:307–319PubMedGoogle Scholar
  44. Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol 179:945–963PubMedGoogle Scholar
  45. Flowers TJ, Troke PF, Yeo AR (1977) The mechanism of salt tolerance in halophytes. Annu Rev Plant Physiol 28:89–121Google Scholar
  46. Flowers TJ, Galal HK, Bromham L (2010) Evolution of halophytes: multiple origins of salt tolerance. Funct Plant Biol 37:604–612Google Scholar
  47. Food and Agricultural Organization (FAO) (2003) New global mangrove estimate. Scholar
  48. Fowler S, Lee K, Onouchi H, Samach A, Richardson K, Morris B, Coupland G, Putterill J (1999) GIGANTEA: a circadian clock-controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane-spanning domains. EMBO J 18:4679–4688PubMedGoogle Scholar
  49. Foyer CH, Noctor G (2005) Oxidant and antioxidant signaling in plants: a re-evaluation of the concept oxidative stress in a physiological context. Plant Cell Environ 28:1056–1071Google Scholar
  50. Fukushima Y, Sasamoto H, Baba S, Ashihara H (1997) The effect of salt stress on the catabolism of sugars in leaves and roots of a mangrove plant Avicennia marina. Z Naturforsch 52:187–192Google Scholar
  51. Gaxiola RA, Palmgren MG, Schumachner K (2007) Plant proton pumps. FEBS Lett 581:2204–2214PubMedGoogle Scholar
  52. Ghnaya T, Slama I, Messedi D, Grignon C, Ghorbel MH, Abdelly C (2007) Effect of Cd2+ on K+, Ca+ and N uptake in two halophytes Sesuvium portulacastrum and Mesembrynathemum crystallinum: consequences on growth. Chemosphere 67:72–79PubMedGoogle Scholar
  53. Glenn EP, Brown JJ (1999) Salt tolerance and crop potential of halophytes. Crit Rev Plant Sci 18(2):227–255Google Scholar
  54. Glenn E, Miyamoto M, Moore D, Brown JJ, Thompson TL, Brown P (1997) Water requirements for cultivating Salicornia bigelovii Torr. with seawater on sand in a coastal desert environment. J Arid Environ 36:711–730Google Scholar
  55. Gonzalez JA, Gallardo M, Hilal M, Rosa M, Prado FE (2009) Physiological responses of quinoa (Chenopodium quinoa Willd.) to drought and water logging stresses: dry matter partitioning. Bot Stud 50:35–42Google Scholar
  56. Goudie AS (1990) Soil salinity-causes and controls. In: Techniques for desert reclamation (ed) J. Wiley and Sons Ltd., Wiley, Chichester, England, pp 110–111Google Scholar
  57. Guo XL, Cao YR, Cao ZY, Zhao YX, Zhang H (2004) Molecular cloning and characterization of a stress-induced peroxiredoxin Q gene in halophyte Suaeda salsa. Plant Sci 167:969–975Google Scholar
  58. Hafsi C, Romero-Puertas MC, Gupta DK, del Riob LA, Sandalio LM, Abdelly C (2010) Moderate salinity enhances the antioxidative response in the halophyte Hordeum maritimum L. under potassium deficiency. Environ Exp Bot 69:129–136Google Scholar
  59. Hare PD, Cress WA (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul 21:79–102Google Scholar
  60. Hollington PA, Hussain Z, Kahlown MA, Abdullah M (2001) Success stories in saline agriculture in Pakistan: from research to production and development. In: BAC saline agriculture conference Dubai, 19–21 Mar 2001Google Scholar
  61. Hong Z, Lakkineni K, Zhang Z, Verma DPS (2000) Removal of feedback inhibition of ∆1-Pyrroline-5-Carboxylate Synthetase results in increased proline accumulation and protection of plants from osmotic stress. Plant Physiol 122:1129–1136PubMedGoogle Scholar
  62. Horie T, Schroeder JI (2004) Sodium transporters in plants. Diverse genes and physiological functions. Plant Physiol 136:2457–2462PubMedGoogle Scholar
  63. Huang J, Reneau RB Jr, Hagedorn C (2000) Nitrogen removal in constructed wetlands employed to treat domestic wastewater. Water Res 34:2582–2588Google Scholar
  64. Hurst AC, Grams TEE, Ratajczak R (2004) Effects of salinity, high irradiance, ozone, and ethylene on mode of photosynthesis, oxidative stress and oxidative damage in the C3/CAM intermediate plant Mesembryanthemum crystallinum L. Plant Cell Environ 27:187–197Google Scholar
  65. Hutchings P, Saenger P (1987) Ecology of mangroves. University of Queensland Press, New YorkGoogle Scholar
  66. Iwasaki K (1987) The effectiveness of salt-accumulating plants in reclaiming salinized soils. Jpn J Trop Agric 31:255–261Google Scholar
  67. Jebara S, Jebara M, Limam F, Aouani ME (2005) Changes in ascorbate peroxidase, catalase, guaiacol peroxidase and superoxide dismutase activities in common bean (Phaseolus vulgaris) nodules under salt stress. J Plant Physiol 162:929–936PubMedGoogle Scholar
  68. Jennings DH (1968) Microelectrode experiments with potato cells: a re-interpretation of the experimental findings. J Exp Bot 19:13Google Scholar
  69. Jitesh MN, Prashanth SR, Sivaprakash KR, Parida AK (2006) Antioxidative response mechanism in halophytes: their role in stress defence. J Genet 85:237–254Google Scholar
  70. Kadukova J, Kalogerakis N (2007) Lead accumulation from non-saline and saline environment by Tamarix smyrnensis Bunge. Eur J Soil Biol 43:216–223Google Scholar
  71. Kadukova J, Manousaki E, Kalogerakis N (2008) Pb and Cd accumulation and phytoexcretion by salt cedar (Tamarix smyrnensis Bunge). Int J Phytoremediation 10:31–46PubMedGoogle Scholar
  72. Kant S, Kant P, Raveh E, Barak S (2006) Evidence that differential gene expression between the halophyte, Thellungiella halophila, and Arabidopsis thaliana is responsible for higher levels of the compatible osmolyte proline and tight control of Na+ uptake in T. halophila. Plant Cell Environ 29:1220–1234PubMedGoogle Scholar
  73. Kavitha K, Venkataraman G, Parida A (2008) An oxidative and salinity stress induced peroxisomal ascorbate peroxidase from Avicennia marina: molecular and functional characterization. Plant Physiol Biochem 46:794–804PubMedGoogle Scholar
  74. Kavitha K, George S, Venkataraman G, Parida A (2010) A salt-inducible chloroplastic monodehydroascorbate reductase from halophyte Avicennia marina confers salt stress tolerance on transgenic plants. Biochimie 92:1321–1329PubMedGoogle Scholar
  75. Ketchum REB, Warren RC, Klima LJ, Lopez-Gutierrez F, Nabors MW (1991) The mechanism and regulation of proline accumulation in suspension cultures of the halophytic grass Distichlis spicata L. J Plant Physiol 137:368–374Google Scholar
  76. Khan MA, Ansari R (2008) Potential use of halophytes with emphasis on fodder production in coastal areas of Pakistan. In: Abdelly C, Ozturk M, Ashraf M, Grignon C (eds) Biosaline agriculture and high salinity tolerance. Birkhauser Verlag, Basel, pp 157–162Google Scholar
  77. Khan MA, Qaiser M (2006) Halophytes of Pakistan: distribution, ecology, and economic importance. In: Khan MA, Barth H-J, Kust GC, Boer B (eds) Sabkha ecosystems: Vol II, The South and Central Asian countries. Springer, Drodrecht, pp 135–160Google Scholar
  78. Kore-eda S, Cushman MA, Akselrod I, Bufford D, Fredrickson M, Clark E, Cushman JC (2004) Transcript profiling of salinity stress responses by large-scale expressed sequence tag analysis in Mesembryanthemum crystallinum. Gene 341:83–92PubMedGoogle Scholar
  79. Kreps JA, Wu Y, Chang HS, Zhu T, Wang X, Harper JF (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 130:2129–2141PubMedGoogle Scholar
  80. Lacerda LD (1997) Trace metals in mangrove plants: why such low concentrations? In: Kjerfve B, Lacerda LD, Diop HS (eds) Mangrove ecosystem studies in Latin America and Africa. UNESCO, Paris, pp 171–178Google Scholar
  81. Lauchli A, Epstein E (1990) Plant responses to saline and sodic conditions. In: Tanji KK (ed) Agricultural salinity assessment and management. American Society of Civil Engineering, New York, pp 113–137Google Scholar
  82. Lefevre I, Marchal G, Meerts P, Correal E, Lutts S (2009) Chloride salinity reduces cadmium accumulation by the Mediterranean halophyte species Atriplex halimus L. Environ Exp Bot 65:142–152Google Scholar
  83. Lewis RR (2005) Ecological engineering for successful management and restoration of mangrove forests. Ecol Eng 24:403–418Google Scholar
  84. Lewis RR, Streever W (2000) Restoration of mangrove habitat. Tech Note ERDC TN-WRP-VN-RS-3. US Army, Corps of Engineers, Waterways Experiment Station, Vicksburg, MSGoogle Scholar
  85. Li TH, Li SH (2005) Leaf responses of micropropagated apple plants to water stress: nonstructural carbohydrate composition and regulatory role of metabolic enzymes. Tree Physiol 25:395–404Google Scholar
  86. Li QL, Liu DW, Gao XR, Su Q, An LJ (2003) Cloning of cDNA encoding choline mono- oxygenase from  Suaeda liaotungensis  and salt tolerance of transgenic tobacco. Acta Bot Sin 45:242–247Google Scholar
  87. Li Q, Yin H, Li D, Zhu H, Zhang Y, Zhu W (2007) Isolation and characterization of  CMO  gene promoter from halophyte  Suaeda liaotungensis  K. J Genet Genom 34:355–361Google Scholar
  88. Lilebo AI, Valega M, Otero M, Pardal MA, Pereira E, Duarte AC (2010) Daily and inter-tidal variations of Fe Mn and Hg in the water column of a contaminated salt marsh: halophytes effect. Estuar Coast Shelf Sci 88:91–98Google Scholar
  89. Lokhande VH, Nikam TD, Suprasanna P (2010a) Biochemical, physiological and growth changes in response to salinity in callus cultures of Sesuvium portulacastrum L. Plant Cell Tissue Organ Cult 102:17–25Google Scholar
  90. Lokhande VH, Nikam TD, Suprasanna P (2010b) Differential osmotic adjustment to iso-osmotic salt and PEG stress in vitro in the halophyte Sesuvium portulacastrum L. J Crop Sci Biotechnol 13:251–256Google Scholar
  91. Lokhande VH, Srivastava AK, Srivastava S, Nikam TD, Suprasanna P (2010c) Regulated alterations in redox and energetic status are the key mediators of salinity tolerance in the halophyte Sesuvium portulacastrum (L.) L. Plant Growth Regul DOI 10.1007/s10725-011-9600-3Google Scholar
  92. Lokhande VH, Nikam TD, Patade VY, Ahire ML, Suprasanna P (2011a) Effects of optimal and supra-optimal salinity stress on antioxidative defence, osmolytes and in vitro growth responses in Sesuvium portulacastrum L. Plant Cell Tissue Organ Cult 104:41–49Google Scholar
  93. Lokhande VH, Srivastava S, Patade VY, Dwivedi S, Tripathi RD, Nikam TD, Suprasanna P (2011b) Investigation of arsenic accumulation and tolerance in Sesuvium portulacastrum (L.). Chemosphere 82:529–534PubMedGoogle Scholar
  94. Lokhande VH, Srivastava AK, Srivastava S, Nikam TD, Suprasanna P (2011c) Regulated alterations in redox and energetic status are the key mediators of salinity tolerance in the halophyte Sesuvium portulacastrum (L.) L. Plant Growth Regul 10.1007/s10725-011-9600-3PubMedGoogle Scholar
  95. Lovelock CE, Ball MC (2002) Influence of salinity on photosynthesis of halophytes. In: Lauchli A, Luttge U (eds) Salinity: environment-plant-molecules. Kluwer, Dordrecht, pp 315–339Google Scholar
  96. M’rah S, Ouerghi Z, Berthomieu C, Havaux M, Jungas C, Hajji M, Grignon C, Lachaal M (2006) Effects of NaCl on the growth, ion accumulation and photosynthetic parameters of Thellungiella halophila. J Plant Physiol 163:1022–1031PubMedGoogle Scholar
  97. MacFarlane GR, Burchett MD (1999) Zinc distribution and excretion in the leaves of the grey mangrove, Avicennia marina (Forsk.) Vierh. Environ Exp Bot 41:167–175Google Scholar
  98. MacFarlane GR, Burchett MD (2000) Cellular distribution of copper, lead and zinc in the grey mangrove, Avicennia marina (Forsk.) Vierh. Aquat Bot 68:45–59Google Scholar
  99. MacFarlane GR, Burchett MD (2002) Toxicity, growth and accumulation relationship of copper, lead and zinc in the grey mangrove, Avicennia marina (Forsk.) Vierh.: biological indication potential. Environ Pollut 123:139–151Google Scholar
  100. MacFarlane GR, Koller CE, Blomberg SP (2007) Accumulation and partitioning of heavy metals in mangroves: a synthesis of field-based studies. Chemosphere 69:1454–1464PubMedGoogle Scholar
  101. Manousaki E, Kalogerakis N (2009) Phytoextraction of Pb and Cd by the Mediterranean saltbush (Atriplex halimus L.): metal uptake in relation to salinity. Environ Sci Pollut Res 16:844–854Google Scholar
  102. Manousaki E, Kadukova J, Papadonatonakis N, Kalogerakis and N (2008) Phytoextraction and Phytoexcretion of Cd by Tamarix smyrnensis growing on contaminated non-saline and saline soils. Environ Res 106:326–332Google Scholar
  103. Martinez JP, Kinet JM, Bajji M, Lutts S (2005) NaCl alleviates polyethylene glycol-induced water stress in the halophyte species Atriplex halimus L. J Exp Bot 56:2421–2431PubMedGoogle Scholar
  104. Masters DG, Benes SE, Norman HC (2007) Biosaline agriculture for forage and livestock production. Agric Ecosyst Environ 119:234–248Google Scholar
  105. Megdichi W, Ben Amor N, Debez A, Hessini K, Ksouri R, Zuily-Fodil Y, Abdelly C (2007) Salt tolerance of the annual halophyte Cakile maritima as affected by the provenance and the developmental stage. Acta Physiol Plant 29:375–384Google Scholar
  106. Menzel U, Lieth H (2003) HALOPHYTE Database V. 2.0 update. In: Lieth H, Mochtchenko M (eds) Cash crop halophytes. Kluwer, Dordrecht, CD-ROMGoogle Scholar
  107. Messedi D, Labidi N, Grignon C, Abdelly C (2004) Limits imposed by salt to the growth of the halophyte Sesuvium portulacastrum. J Plant Nutr Soil Sci 167:720–725Google Scholar
  108. Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signaling during drought and salinity stresses. Plant Cell Environ. 33(4):453–467Google Scholar
  109. Mitsch WJ, Gosselink JG (2007) Wetlands, 4th edn. Wiley, New YorkGoogle Scholar
  110. Mittler M (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410PubMedGoogle Scholar
  111. Mittler R, Vanderauwera S, Gollery M, Breusegem FV (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498PubMedGoogle Scholar
  112. Moghaieb REA, Saneoka H, Fujita K (2004) Effect of salinity on osmotic adjustment, glycine betaine accumulation and the betaine aldehyde dehydrogenase gene expression in two halophytic plants, Salicornia europaea and Suaeda maritime. Plant Sci 166:1345–1349Google Scholar
  113. Moseki B, Buru JC (2010) Ionic and water relations of Sesuvium portulacastrum (L). Sci Res Essay 5:35–40Google Scholar
  114. Mulholland MM, Otte ML (2002) The effects of nitrogen supply and salinity on DMSP, glycine betaine- and proline concentrations in leaves of Spartina anglica. Aquat Bot 72:193–200Google Scholar
  115. Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250PubMedGoogle Scholar
  116. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681PubMedGoogle Scholar
  117. Nah G, Pagliarulo CL, Mohr PG, Luo M, Sisneros N, Yu Y, Collura K, Currie J, Goicoechea JL, Wing RA et al (2009) Comparative sequence analysis of the SALT OVERLY SENSITIVE1 orthologous region in Thellungiella halophila and Arabidopsis thaliana. Genomics 94:196–203PubMedGoogle Scholar
  118. Nedjimi B, Daoud Y (2009) Cadmium accumulation in Atriplex halimus subsp. schweinfurthii and its influence on growth, proline, root hydraulic conductivity and nutrient uptake. Flora 204:316–324Google Scholar
  119. Noctor G, Foyer CH (1998) Ascorbate and glutathione. Keeping active oxygen under control. Ann Rev Plant Physiol Mol Biol 49:249–279Google Scholar
  120. Nouairi I, Ghnaya T, Youssef NB, Zarrouk M, Ghorbel MH (2006) Changes in content and fatty acid profiles of total lipids of two halophytes: Sesuvium portulacastrum and Mesembryanthemum crystallinum under cadmium stress. J Plant Physiol 163:1198–1202Google Scholar
  121. Oh D-H, Leidi E, Zhang Q, Hwang S-M, Li Y, Quintero FJ, Jiang X, D’Urzo MP, Sang Lee Y, Zhao Y, Bahk JD, Bressan RA, Yun D-J, Pardo JM, Bohnert HJ (2009) Loss of halophytism by interference with SOS1 expression. Plant Physiol 15:210–222Google Scholar
  122. Ohta M, Hayashi Y, Nakashima A, Hamada A, Tanaka A, Nakamura T, Hayakawa T (2002) Introduction of a Na+/H+ antiporter gene from Atriplex gmelini confers salt tolerance to rice. FEBS Lett 532:279–282PubMedGoogle Scholar
  123. Ozawa T, Miura M, Fukuda M, Kakuta S (2009) Cadmium tolerance and accumulation in a halophyte Salicornia europaea as a new candidate for phytoremediation of saline soils. Sci Rep Grad Sch Life Environ Sci Osaka Pref Univ 60:1–8Google Scholar
  124. Pagter M, Bragato C, Malagoli M, Brix H (2009) Osmotic and ionic effects of NaCl and Na2SO4 salinity on Phragmites australis. Aquat Bot 90:43–51Google Scholar
  125. Paramonova NV, Shevyakova NI, Kuznetsov VV (2004) Ultrastructure of chloroplasts and their storage inclusions in the primary leaves of Mesembryanthemum crystallinum affected by putrescine and NaCl. Russ J Plant Physiol 1:86–96PubMedGoogle Scholar
  126. Parida AK, Das AB, Mohanty P (2004) Investigations on the antioxidative defense responses to NaCl stress in a mangrove, Bruguirea parviflora: differential, regulations of isoforms of some antioxidant enzymes. Plant Growth Regul 42:213–226Google Scholar
  127. Patra J, Panda BB (1998) A comparison of biochemical responses to oxidative and metal stress in seedlings of barley, Hordeum vulgare L. Environ Pollut 101:99–105PubMedGoogle Scholar
  128. Peters EC, Gassman NJ, Firman JC, Richmond RH, Power EA (1997) Ecotoxicology of tropical marine ecosystems. Environ Toxicol Chem 16:12–40Google Scholar
  129. Pilon-Smits EAH, de Souza MP, Hong G, Amini A, Bravo RC et al (1999) Selenium volatilization and accumulation by twenty aquatic plant species. J Environ Qual 28:1011–1017Google Scholar
  130. Popova OV, Yang O, Dietz KJ, Golldack D (2008) Differential transcript regulation in Arabidopsis thaliana and the halotolerant Lobularia maritima indicates genes with potential function in plant salt adaptation. Gene 423:142–148PubMedGoogle Scholar
  131. Potters G, Horemans N, Jansen MAK (2010) The cellular redox state in plant stress biology – A charging concept. Plant Physiol Biochem 48:292–300PubMedGoogle Scholar
  132. Qadir M, Oster J (2004) Crop and irrigation management strategies for saline–sodic soils and waters aimed at environmentally sustainable agriculture. Sci Total Environ 323:1–19PubMedGoogle Scholar
  133. Qi CH, Chen M, Song J, Wang BS (2009) Increase in aquaporin activity is involved in leaf succulence of the euhalophyte Suaeda salsa, under salinity. Plant Sci 176:200–205Google Scholar
  134. Queval G, Noctor G (2007) A plate-reader method for the measurement of NAD, NADP, glutathione and ascorbate in tissue extracts. Application to redox profiling during Arabidopsis rosette development. Anal Biochem 363:58–69PubMedGoogle Scholar
  135. Rabhi M, Hafsi C, Lakhdar A, Barhoumi Z, Hamrouni MH, Abdelly C, Smauoi A (2009) Evaluation of the capacity of three halophytes to desalinize their rhizosphere as grown on saline soils under nonleaching conditions. Afr J Ecol 47:463–468Google Scholar
  136. Rabhi M, Ferchichi S, Jouini J, Hamrouni MH, Koyro HW, Ranieri A, Abdelly C, Smaoui A (2010) Phytodesalination of a salt-affected soil with the halophyte Sesuvium portulacastrum L. to arrange in advance the requirements for the successful growth of a glycophytic crop. Bioresour Technol 101:6822–6828PubMedGoogle Scholar
  137. Ramadan T (2000) Dynamics of salt secretion by Sporobolus Spicatus (Vahl) kunth from sites of differing salinity. Ann Bot 87:259–266Google Scholar
  138. Rammesmayer G, Pichorner H, Adams P, Jensen RG, Bohnert HJ (1995) Characterization of IMT1, myo-inositol O-methyltrasferase, from Mesembryanthemum crystallinum. Arch Biochem Biophys 322:183–188PubMedGoogle Scholar
  139. Raven JA (1985) Regulation of pH and generation of osmolarity in vascular land plants: costs and benefits in relation to efficiency of use of water, energy and nitrogen. New Phytol 101:25–77Google Scholar
  140. Ravindran KC, Venkatesan K, Balakrishnan V, Cehllappan KP, Balasubramanian T (2007) Restoration of saline land by halophytes for Indian soils. Soil Biol Biochem 39:2661–2664Google Scholar
  141. Reboreda R, Caçador I (2007) Halophyte vegetation influences in salt marsh retention capacity for heavy metals. Environ Pollut 146:147–154PubMedGoogle Scholar
  142. Reboreda R, Caçador I (2008) Enzymatic activity in the rhizosphere of Spartina maritima: potential contribution for phytoremediation of metals. Mar Environ Res 65:77–84PubMedGoogle Scholar
  143. Reda EAM, Saneoka H, Fujita K (2004) Effect of salinity on osmotic adjustment, glycinebetaine accumulation and the betaine aldehyde dehydrogenase gene expression in two halophyte plants, Salicornia europaea and Suaeda maritime. Plant Sci 166:1345–1349Google Scholar
  144. Reddy MP, Shah MT, Patolia JS (2008) Salvadora persica, a potential species for industrial oil production in semiarid saline and alkali soils. Ind Crops Prod 28:273–278Google Scholar
  145. Redondo-Gómez S, Mateos-Naranjo E, Andrades-Moreno L (2010a) Accumulation and tolerance characteristics of cadmium in a halophytic Cd-hyperaccumulator, Arthrocnemum macrostachyum. J Hazard Mater 184:299–307PubMedGoogle Scholar
  146. Redondo-Gómez S, Mateos-Naranjo E, Figueroa ME, Davy AJ (2010b) Salt stimulation of growth and photosynthesis in extreme halophyte, Arthrocnemum macrostachyum. Plant Biol 12:79–87PubMedGoogle Scholar
  147. Rhodes D, Hanson AD (1993) Quaternary ammonium and tertiary sulfonium compounds in higher plants. Ann Rev Plant Physiol Mol Biol 44:357–384Google Scholar
  148. Robinson SP, Jones GP (1986) Accumulation of glycine betaine in chloroplasts provides osmotic adjustment during salt stress. Aust J Plant Physiol 13:659–668Google Scholar
  149. Rozema J (1991) Growth, water and ion relationships of halophytic monocotyledonae and dicotyledonae – a unified concept. Aquat Bot 39:17–33Google Scholar
  150. Russell BL, Rathinasabapathi B, Hanson AD (1998) Osmotic stress induces expression of choline monooxygenase in sugar beet and amaranth. Plant Physiol 116:859–865PubMedGoogle Scholar
  151. Sadiq M, Zaidi TH (1994) Sediment composition and metal concentrations in mangrove leaves from the Saudi coast of the Arabian Gulf. Sci Total Environ 155:1–8Google Scholar
  152. Saenger P (2002) Mangrove ecology, silviculture and conservation. Kluwer, DordrechtGoogle Scholar
  153. Saenger P, Siddiqi NA (1993) Land from the seas: the mangrove afforestration program of Bangladesh. Ocean Coast Manag 20:23–39Google Scholar
  154. Seki M, Ishida J, Narusaka M, Fujita M, Nanjo T, Umezawa T, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-­salinity stresses using a full-length cDNA microarray. Plant J 3:279–292Google Scholar
  155. 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 131:399–411PubMedGoogle Scholar
  156. Seliskar DM, Gallagher JL (2000) Exploiting wild population diversity and somaclonal variation in the salt marsh grass Distichlis spicata (Poaceae) for marsh creation and restoration. Am J Bot 87:141–146PubMedGoogle Scholar
  157. Shahid SA (2002) New technologies for soil reclamation and desert greenery In: Nader MA, Faisal KT (eds) Proceedings of the joint KISR – PEC symposium Yazd, Iran, pp 308–329Google Scholar
  158. Sharma BR, Minhas PS (2005) Strategies for managing saline/alkali waters for sustainable agricultural production in South Asia. Agric Water Manag 78:136–151Google Scholar
  159. Shen YG, Du BX, Zhang JS, Chen SY (2001) Cloning and characterization of CMO gene from  Atriplex hortensis. Chin J Biotechnol 17:1–6Google Scholar
  160. Shi H, Ishitani M, Kim C, Zhu JK (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H  +  antiporter. Proc Natl Acad Sci USA 97:6896–6901PubMedGoogle Scholar
  161. Silveira JAG, Araujo SAM, Lima JPMS, Viegas RA (2009) Roots and leaves display contrasting osmotic adjustment mechanisms in response to NaCl-salinity in Atriplex nummularia. Enviorn Exp Bot 66:1–8Google Scholar
  162. Slama I, Ghnaya T, Savouŕe A, Abdelly C (2008) Combined effects of long-term salinity and soil drying on growth, water relations, nutrient status and proline accumulation of Sesuvium portulacastrum. C R Biol 331:442–451PubMedGoogle Scholar
  163. Slesak I, Miszalski Z (2003) Superoxide dismutase-like protein from roots of the intermediate C3-CAM plant Mesembryanthemum crystallinum L. in in vitro culture. Plant Sci 164:497–505Google Scholar
  164. Slesak I, Miszalski Z, Karpinska B, Niewiadomska E, Ratajczak R, Karpinski S (2002) Redox control of oxidative stress responses in the C3-CAM intermediate plant Mesembryanthemum crystallinum. Plant Physiol Biochem 40:669–677Google Scholar
  165. Slesak I, Slesak H, Libik M, Miszalski Z (2008) Antioxidant response system in the short-term post-wounding effect in Mesembryanthemum crystallinum leaves. J Plant Physiol 165:127–137PubMedGoogle Scholar
  166. Smirnoff N (2005) Ascorbate, tocopherol and carotenoids: metabolism, pathway engineering and functions. In: Smirnoff N (ed) Antioxidants and reactive oxygen species in plants. Blackwell, Oxford, pp 53–86Google Scholar
  167. Sousa AI, Caçador I, Lillebo AI, Pardal MA (2008) Heavy metal accumulation in Halimione portulacoides: intra -and extra-cellular metal binding sites. Chemosphere 70:850–857PubMedGoogle Scholar
  168. Srinivas V, Balasubramanian D (1995) Proline is a protein-compatible hydrotrope. Langmuir 11:2830–2833Google Scholar
  169. Subbarao GV, Levine LH, Wheeler RM, Stutte GW (2001) Glycine betaine accumulation: its role in stress resistance in crop plants. In: Pessarakli M (ed) Handbook of plant and crop physiology. Marcel Dekker, New York, pp 881–907Google Scholar
  170. Sucre B, Suarez N (2010) Effect of salinity and PEG-induced water stress on water status, gas exchange, solute accumulation, and leaf growth in Ipomoea pes-caprae. Environ Exp Bot 70:192–203Google Scholar
  171. Szabados L, Savoure A (2009) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97PubMedGoogle Scholar
  172. Tabuchi T, Kawaguchi Y, Azuma T, Nanmori T, Yasuda T (2005) Similar regulation patterns of choline monooxygenase, phosphoethanolamine N-methyltransferase and S-adenosyl-L-methionine synthetase in leaves of halophyte  Atriplex nummularia  L. Plant Cell Physiol 46:505–513PubMedGoogle Scholar
  173. Taji T, Seki M, Satou M, Sakurai T, Kobayashi M, Ishiyama K, Narusaka Y, Narusaka M, Zhu JK, Shinozaki K (2004) Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis microarray. Plant Physiol 135:1697–1709PubMedGoogle Scholar
  174. 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. Aquat Bot 68:15–28Google Scholar
  175. Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91:503–5027PubMedGoogle Scholar
  176. Tipirdamaz R, Gagneul D, Duhaze C, Ainouche A, Monnier C, Zokum D, Larher F (2006) Clustering of halophytes from an inland salt marsh in Turkey according to their ability to accumulate sodium and nitrogenous osmolytes. Environ Exp Bot 57:139–153Google Scholar
  177. Vicente O, Boscaiu M, Naranjo MA, Estrelles E, Belles JM, Soriano P (2004) Responses to salt stress in the halophyte Plantago crassifolia (Plantaginaceae). J Arid Environ 58:463–481Google Scholar
  178. Waisel Y (1972) Biology of halophytes. Academic, New YorkGoogle Scholar
  179. Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14PubMedGoogle Scholar
  180. Wang B, Luttge U, Ratajczak R (2004a) Specific regulation of SOD isoforms by NaCl and osmotic stress in leaves of the C3 halophyte Suaeda salsa L. J Plant Physiol 161:285–293PubMedGoogle Scholar
  181. Wang LW, Showalter AM (2004b) Cloning and saltinduced, ABA-independent expression of choline mono-oxygenase in Atriplex prostrate. Physiol Plant 120:405–412PubMedGoogle Scholar
  182. Wang B, Davenport RJ, Volkov V, Amtmann A (2006) Low unidirectional sodium influx into root cells restricts net sodium accumulation in Thellungiella halophila, a salt-tolerant relative of Arabidopsis thaliana. J Exp Bot 57:1161–1170PubMedGoogle Scholar
  183. Wang CQ, Xu C, Wei JG, Wang HB, Wang SH (2008a) Enhanced tonoplast H+ -ATPase activity and superoxide dismutase activity in the halophyte Suaeda salsa containing high level of betacyanin. J Plant Growth Regul 27:58–67Google Scholar
  184. Wang KS, Huang LC, Lee HS, Chen PY, Chang SH (2008b) Phytoextraction of cadmium by Ipomoea aquatica (water spinach) in hydroponic solution: effects of cadmium speciation. Chemosphere 72:666–672PubMedGoogle Scholar
  185. Wong CE, Yong L, Aurelie L, David G, Paulo N, Brett W, Claudia D, Brian GG, Gray GR, Weretilnyk EA, Griffith M, Moffatt BA (2006) Transcriptional profiling implicates novel interactions between abiotic stress and hormonal responses in Thellungiella, a close relative of Arabidopsis. Plant Physiol 140:1437–1450PubMedGoogle Scholar
  186. Yadav SK (2010) Heavy metal toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. S Afr J Bot 76:167–179Google Scholar
  187. Yang YL, Shi R, Wei X, Fan Q, An L (2010) Effect of salinity on antioxidant enzymes in calli of the halophyte  Nitraria tangutorum  Bobr. Plant Cell Tissue Organ Cult 102:387–395Google Scholar
  188. Yensen NP (2006) Halophyte uses for the twenty-first century. In: Khan MA, Weber DJ (eds) Ecophysiology of high salinity tolerant plants. Springer, Dordrecht, pp 367–396Google Scholar
  189. 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 13:161–173Google Scholar
  190. Yin X, Zhao Y, Luo D, Zhang H (2002) Isolating the promoter of a stress-induced gene encoding betaine aldehyde dehydrogenase from the halophyte Atriplex centralasiatica Iljin. Biochim Biophys Acta 1577:452–456PubMedGoogle Scholar
  191. Yuanyuan M, Yali Z, Jiang L, Hongbo S (2009) Roles of plant soluble sugars and their responses to plant cold stress. Afr J Plant Biotechnol 8:2004–2010Google Scholar
  192. Zabłudowska E, Kowalska J, Jedynak L, Wojas S, Skłodowska A, Antosiewicz DM (2009) Search for a plant for phytoremediation – What can we learn from field and hydroponic studies? Chemosphere 77:301–307PubMedGoogle Scholar
  193. Zahran MA, Wahid AAA (1982) Halophytes and human welfare. In: Sen DN, Rajpurohit KS (eds) Contributions to the ecology of halophytes. D.W. Junk Publishers, Boston, pp 235–257Google Scholar
  194. Zaier H, Ghnaya T, Lakhdar A, Baioui R, Ghabriche R, Mnasri M, Sghair S, Lutts S, Abdelly C (2010a) Comparative study of Pb-phytoextraction potential in Sesuvium portulacastrum and Brassica juncea: tolerance and accumulation. J Hazard Mat. doi:10.1016/j.jhazmat.2010.07.068
  195. Zaier H, Mudarra A, Kutscher D, Fernandez de la Campa MR, Abdelly C, Sanz-Medel A (2010b) Induced lead binding phytochelatins in Brassica juncea and Sesuvium portulacastrum investigated by orthogonal chromatography inductively coupled plasma-mass spectrometry and matrix assisted laser desorption ionization-time of flight-mass spectrometry. Anal Chim Acta. doi:10.1016/j.aca.2010.04.054
  196. Zhang F, Yang YL, He WL, Zhao X, Zhang LX (2004) Effects of salinity on growth and compatible solutes of callus induced from Populus euphratica. In Vitro Cell Dev Biol Plant 40:491–494Google Scholar
  197. Zhang Y, Lai J, Sun S, Li Y, Liu Y, Liang L, Chen M, Xie Q (2008) Comparison analysis of transcripts from the halophyte Thellungiella halophila. J Integr Plant Biol 50:1327–1335PubMedGoogle Scholar
  198. Zhao KF (1991) Desalinization of saline soils by Suaeda salsa. Plant Soil 135:303–305Google Scholar
  199. Zhao K, Hai F, Ungar IA (2002) Survey of halophytes species in China. Plant Sci 163:491–498Google Scholar
  200. Zhu J-K (2001) Plant salt tolerance. Trends Plant Sci 6:66–71PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  1. 1.Functional Plant Biology Section, Nuclear Agriculture and Biotechnology DivisionBhabha Atomic Research CentreMumbaiIndia

Personalised recommendations