Halophyte Responses and Tolerance to Abiotic Stresses

  • Ganesh Chandrakant Nikalje
  • Kushi Yadav
  • Suprasanna PennaEmail author


Different anthropogenic activities result in the contamination and degradation of the agricultural ecosystem. Improper disposal of industrial waste, use of excess chemical fertilizers, and mining are major sources of soil contamination. These adverse conditions exert a negative effect on crop growth and yield, while a group of plants, known as halophytes, exhibit greater tolerance. These plants are native to such adverse environments and can withstand different abiotic stresses such as salinity, drought, toxic metal stress, and hypoxia. Halophytes grow luxuriantly in saline soils, which make them suitable for saline agriculture. In addition, they are a good source of salt-responsive genes and value-added products. Many halophytes show common biochemical and physiochemical responses to salt stress, whereas under multiple stresses, different mechanisms operate. The accumulation of osmolytes such as proline, selectivity in K:N, the exclusion of sodium and vacuolar compartmentalization, the induction of antioxidant molecules (enzymatic and non-enzymatic) are the most common features of halophytic adaptation to stress. The comparative study of halophytes and glycophytes revealed that the former are well equipped with cross-tolerance mechanism and are well prepared before stress imposition. It is also reported that pretreatment/priming with salinity or other stresses in early developmental stage of halophytes improves their salt tolerance at later stage. This observation suggests that halophytes might have stress memory, which helps them to respond better to stress conditions. In this article, we present a current perspective of the general tolerance mechanism and the responses of halophytes to different abiotic stresses such as salt, drought, toxic metal, and combination of these. Understanding the mechanism of such abiotic stresses alone and in combination will help to identify potential halophytes for re-vegetation or possible breeding for redevelopment of salt-affected agricultural lands.


Halophytes Abiotic stress Multiple stress Salinity Drought Toxic metals 


  1. Adrian-Romeroa M, Wilsona SJ, Blundena G, Yanga MH, Carabot-Cuervoa A, Bashira AK (1998) Betaines in coastal plants. Biochem Syst Ecol 26:535–543CrossRefGoogle Scholar
  2. Amtmann A (2009) Learning from evolution: Thellungiella generates new knowledge on essential and critical components of abiotic stress tolerance in plants. Mol Plant 2:3–12PubMedPubMedCentralCrossRefGoogle Scholar
  3. Armstrong W (1980) Aeration in higher plants. Adv Bot Res 7:225–332CrossRefGoogle Scholar
  4. Atreya A, Vartak V, Bhargava S (2009) Salt priming improves tolerance to desiccation stress and to extreme salt stress in Bruguiera cylindrica. Int J Integr Biol 6:68–73Google Scholar
  5. Baena-González E, Rolland F, Thevelein JM, Sheen JA (2007) Central integrator of transcription networks in plant stress and energy signaling. Nature 448:938–942PubMedCrossRefGoogle Scholar
  6. Bailey-Serres J, Voesenek LACJ (2008) Flooding stress: acclimations and genetic diversity. Annu Rev Plant Biol 59:313–339PubMedCrossRefGoogle Scholar
  7. Barrett-Lennard EG (2003) The interaction between waterlogging and salinity in higher plants: causes, consequences and implications. Plant Soil 253:35–54CrossRefGoogle Scholar
  8. Batty LC, Dolan C (2013) The potential use of phytoremediation for sites with mixed organic and inorganic contamination. Crit Rev Environ Sci Technol 43:217–259CrossRefGoogle Scholar
  9. Bazihizina N, Barrett-Lennard EG, Colmer TD (2012) Plant responses to heterogeneous salinity: growth of the halophyte Atriplex nummularia is determined by the root-weighted mean salinity of the root zone. J Exp Bot 63:6347–6358PubMedPubMedCentralCrossRefGoogle Scholar
  10. Bennett SJ, Barrett-Lennard EG, Colmer TD (2009) Salinity and waterlogging as constraints to salt land pasture production: a review. Agric Ecosyst Environ 129:349–360CrossRefGoogle Scholar
  11. Bose J, Rodrigo-Moreno A, Shabala S (2014) ROS homeostasis in halophytes in the context of salinity stress tolerance. J Exp Bot 65:1241–1257PubMedCrossRefGoogle Scholar
  12. Bose J, Rodrigo-Moreno A, Lai D, Xie Y, Shen W, Shabala S (2015) Rapid regulation of the plasma membrane H+-ATPase activity is essential to salinity tolerance in two halophyte species, Atriplex lentiformis and Chenopodium quinoa. Ann Bot 115:481–494PubMedCrossRefGoogle Scholar
  13. Bradley PM, Morris JT (1990) Influence of oxygen and sulfide concentration on nitrogen uptake kinetics in Spartina alterniflora. Ecology 71:282–287CrossRefGoogle Scholar
  14. Braun-Blanquet J, Conrad HS, Fuller GD (1933) Plant sociology: the study of plant communities. Nature 132:1–472CrossRefGoogle Scholar
  15. Britto DT, Kronzucker HJ (2002) NH4 + toxicity in higher plants: a critical review. J Plant Physiol 159:567–584CrossRefGoogle Scholar
  16. Brown CE, Pezeshki SR (2007) Threshold for recovery in the marsh halophyte Spartina alterniflora grown under the combined effects of salinity and soil drying. J Plant Physiol 164:274–282PubMedCrossRefGoogle Scholar
  17. Bruce TJA, Matthes MC, Napier JA, Pickett JA (2007) Stressful ‘memories’ of plants: evidence and possible mechanisms. Plant Sci 173:603–608CrossRefGoogle Scholar
  18. Brun FG, Olivé I, Malta EJ, Vergara JJ, Hernández I, Pérez-Lloréns JJ (2008) Increased vulnerability of Zostera noltii to stress caused by low light and elevated ammonium levels under phosphate deficiency. Mar Ecol Prog Ser 365:67–75CrossRefGoogle Scholar
  19. Chaturvedi AK, Mishra A, Tiwari V, Jha B (2012) Cloning and transcript analysis of type 2 metallothionein gene (SbMT-2) from extreme halophyte Salicornia brachiata and its heterologous expression in E. coli. Gene 499:280–287PubMedCrossRefGoogle Scholar
  20. Chinnusamy V, Schumaker K, Zhu JK (2004) Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J Exp Bot 55:225–236PubMedCrossRefGoogle Scholar
  21. Cobbett C (2003) Heavy metals and plants – model systems and hyperaccumulators. New Phytol 159:289–293CrossRefGoogle Scholar
  22. Colmer TD (2003) Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots. Plant Cell Environ 26:17–36CrossRefGoogle Scholar
  23. Colmer TD, Pedersen O, Wetson A, Flowers TJ (2013) Oxygen dynamics in a salt-marsh soil and in Suaeda maritima during tidal submergence. Environ Exp Bot 92:73–82CrossRefGoogle Scholar
  24. Cong M, Lv J, Liu X, Zhao J, Wu H (2013) Gene expression responses in Suaeda salsa after cadmium exposure. Springerplus 2:232PubMedPubMedCentralCrossRefGoogle Scholar
  25. Conrath U (2009) Priming of induced plant defense responses. Adv Bot Res 51:361–395CrossRefGoogle Scholar
  26. Cushman JC (2001) Osmoregulation in plants: implications for agriculture. Am Zool 41:758–769Google Scholar
  27. D’Amore JJ, Al-Abed SR, Scheckel K, Ryan J (2005) Methods for speciation of metals in soils. J Environ Qual 34:1707PubMedCrossRefGoogle Scholar
  28. Debez A, Huchzermeyer B, Abdelly C, Koyro HW (2011) Sabkha ecosystems, vol 46, pp 59–77CrossRefGoogle Scholar
  29. Demidchik V (2015) Mechanisms of oxidative stress in plants: from classical chemistry to cell biology. Environ Exp Bot 109:212–228CrossRefGoogle Scholar
  30. Demidchik V, Cuin TA, Svistunenko D, Smith SJ, Miller AJ, Shabala S, Sokolik A, Yurin V (2010) Arabidopsis root K+ efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death. J Cell Sci 123:1468–1479PubMedCrossRefGoogle Scholar
  31. Dhar R, Sägesser R, Weikert C, Wagner A (2013) Yeast adapts to a changing stressful environment by evolving cross-protection and anticipatory gene regulation. Mol Biol Evol 30:573–588PubMedCrossRefGoogle Scholar
  32. Ellouzi H, Ben Hamed K, Cela J, Munné-Bosch S, Abdelly C (2011) Early effects of salt stress on the physiological and oxidative status of Cakile maritima (halophyte) and Arabidopsis thaliana (glycophyte). Physiol Plant 142:128–143PubMedCrossRefGoogle Scholar
  33. Ellouzi H, Ben Hamed K, Asensi-Fabado MA, Müller M, Abdelly C, Munné-Bosch S (2013) Drought and cadmium may be as effective as salinity in conferring subsequent salt stress tolerance in Cakile maritima. Planta 237:1311–1323PubMedCrossRefGoogle Scholar
  34. English JP, Colmer TD (2011) Salinity and waterlogging tolerances in three stem-succulent halophytes (Tecticornia species) from the margins of ephemeral salt lakes. Plant Soil 348:379–396CrossRefGoogle Scholar
  35. English JP, Colmer TD (2013) Tolerance of extreme salinity in two stem-succulent halophytes (Tecticornia species). Funct Plant Biol 40:897–912CrossRefGoogle Scholar
  36. Ernst WH, Nelissen HJM (2000) Life-cycle phases of a zinc- and cadmium-resistant ecotype of Silene vulgaris in risk assessment of polymetallic mine soils. Environ Pollut 107:329–338PubMedCrossRefGoogle Scholar
  37. Flowers TJ (2004) Improving crop salt tolerance. J Exp Bot 55:307–319PubMedCrossRefGoogle Scholar
  38. Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol 179:945–963PubMedCrossRefGoogle Scholar
  39. Flowers TJ, Colmer TD (2015) Plant salt tolerance: adaptations in halophytes. Ann Bot 115:327–331PubMedPubMedCentralCrossRefGoogle Scholar
  40. Flowers TJ, Muscolo A (2015) Halophytes in a changing world. AoB Plants 7:1–12. CrossRefGoogle Scholar
  41. Flowers TJ, Galal HK, Bromham L (2010) Evolution of halophytes: multiple origins of salt tolerance in land plants. Funct Plant Biol 37:604–612CrossRefGoogle Scholar
  42. Flowers TJ, Munns R, Colmer TD (2015) Sodium chloride toxicity and the cellular basis of salt tolerance in halophytes. Ann Bot 115:419–431PubMedCrossRefGoogle Scholar
  43. Ghnaya T, Nouairi I, Slama I, Messedi D, Grignon C, Abdelly C, Ghorbel MH (2005) Cadmium effects on growth and mineral nutrition of two halophytes: Sesuvium portulacastrum and Mesembryanthemum crystallinum. J Plant Physiol 162:1133–1140PubMedCrossRefGoogle Scholar
  44. Ghnaya T, Slama I, Messedi D, Grignon C, Ghorbel MH, Abdelly C (2007) Effects of Cd2+ on K+, Ca2+ and N uptake in two halophytes Sesuvium portulacastrum and Mesembryanthemum crystallinum: consequences on growth. Chemosphere 67:72–79PubMedCrossRefGoogle Scholar
  45. Gibbs J, Greenway H (2003) Mechanisms of anoxia tolerance in plants. I. Growth, survival and anaerobic catabolism. Funct Plant Biol 30:1–47CrossRefGoogle Scholar
  46. Glenn EP, Brown JJ (1998) Effects of soil salt levels on the growth and water use efficiency of Atriplex canescens (Chenopodiaceae) varieties in drying soil. Am J Bot 85:10–16PubMedCrossRefGoogle Scholar
  47. Glenn EP, Nelson SG, Ambrose B, Martinez R, Soliz D, Pabendinskas V, Hultine K (2012) Comparison of salinity tolerance of three Atriplex spp. in well-watered and drying soils. Environ Exp Bot 83:62–72CrossRefGoogle Scholar
  48. Golldack D, Li C, Mohan H, Probst N (2014) Tolerance to drought and salt stress in plants: unraveling the signaling networks. Front Plant Sci 5:151PubMedPubMedCentralCrossRefGoogle Scholar
  49. Gorai M, Ennajeh M, Khemira H, Neffati M (2010) Combined effect of NaCl-salinity and hypoxia on growth, photosynthesis, water relations and solute accumulation in Phragmites australis plants. Flora 205:462–470CrossRefGoogle Scholar
  50. Greenway H, Armstrong W, Colmer TD (2006) Conditions leading to high CO2 in waterlogged-flooded soils and possible effects on root growth and metabolism. Ann Bot 98:9–32PubMedPubMedCentralCrossRefGoogle Scholar
  51. Grigore MN, Ivanescu L, Toma C (2014) Halophytes: an integrative anatomical study. Google Scholar
  52. Hamed KB, Ellouzi H, Talbi OZ, Hessini K, Slama I, Ghnaya T, Bosch SM, Savouré A, Abdelly C (2013) Physiological response of halophytes to multiple stresses. Funct Plant Biol 40:883–896CrossRefGoogle Scholar
  53. Han RM, Lefèvre I, Albacete A, Pérez-Alfocea F, Barba-Espín G, Díaz-Vivancos P, Quinet M, Ruan CJ, Hernández JA, Cantero-Navarro E, Lutts S (2013) Antioxidant enzyme activities and hormonal status in response to Cd stress in the wetland halophyte Kosteletzkya virginica under saline conditions. Physiol Plant 147:352–368PubMedCrossRefGoogle Scholar
  54. Hessini K, Lachaâl M, Cruz C, Soltani A (2009) Role of ammonium to limit nitrate accumulation and to increase water economy in wild swiss chard. J Plant Nutr 32:821–836CrossRefGoogle Scholar
  55. Hessini K, Hamed KB, Gandour M, Mejri M, Abdelly C (2013) Ammonium nutrition in the halophyte Spartina alterniflora under salt stress: evidence for a priming effect of ammonium? Plant Soil 370:163–173CrossRefGoogle Scholar
  56. Hou Q, Bartels D (2015) Comparative study of the aldehyde dehydrogenase (ALDH) gene superfamily in the glycophyte Arabidopsis thaliana and Eutrema halophytes. Ann Bot 115:465–479PubMedCrossRefGoogle Scholar
  57. Huang GY, Wang YS (2009) Expression analysis of type 2 metallothionein gene in mangrove species (Bruguiera gymnorrhiza) under heavy metal stress. Chemosphere 77:1026–1029PubMedCrossRefGoogle Scholar
  58. Huang GY, Wang YS (2010) Expression and characterization analysis of type 2 metallothionein from grey mangrove species (Avicennia marina) in response to metal stress. Aquat Toxicol 99:86–92PubMedCrossRefGoogle Scholar
  59. Huchzermeyer B, Flowers T (2013) Putting halophytes to work genetics, biochemistry and physiology. Funct Plant Biol 40:V–VIIICrossRefGoogle Scholar
  60. Jaskiewicz M, Conrath U, Peterhänsel C (2011) Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response. EMBO Rep 12:50–55PubMedCrossRefGoogle Scholar
  61. Jenkins S, Barrett-Lennard EG, Rengel Z (2010) Impacts of waterlogging and salinity on puccinellia (Puccinellia ciliata) and tall wheatgrass (Thinopyrum ponticum): zonation on saltland with a shallow water-table, plant growth, and Na+ and K+ concentrations in the leaves. Plant Soil 329:91–104CrossRefGoogle Scholar
  62. Jithesh MN, Prashanth SR, Sivaprakash KR, Parida AK (2006) Antioxidative response mechanisms in halophytes: their role in stress defence. J Genet 85:237–254PubMedCrossRefGoogle Scholar
  63. Kholodova VP, Volkov KS, Kuznetsov VV (2005) Adaptation of the common ice plant to high copper and zinc concentrations and their potential using for phytoremediation. Russ J Plant Physiol 52:748–757CrossRefGoogle Scholar
  64. Knight H, Knight MR (2001) Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci 6:262–267PubMedCrossRefGoogle Scholar
  65. Konnerup D, Moir-Barnetson L, Pedersen O, Veneklaas EJ, Colmer TD (2015) Contrasting submergence tolerance in two species of stem-succulent halophytes is not determined by differences in stem internal oxygen dynamics. Ann Bot 115:409–418PubMedCrossRefGoogle Scholar
  66. Kudo N, Fujiyama H (2010) Responses of halophyte Salicornia bigelovii to different forms of nitrogen source. Pedosphere 20:311–317CrossRefGoogle Scholar
  67. Lefèvre I, Marchal G, Meerts P, Corréal E, Lutts S (2009) Chloride salinity reduces cadmium accumulation by the Mediterranean halophyte species Atriplex halimus L. Environ Exp Bot 65:142–152CrossRefGoogle Scholar
  68. Lefèvre I, Marchal G, Edmond GM, Correal E, Lutts S (2010) Cadmium has contrasting effects on polyethylene glycol sensitive and resistant cell lines in the Mediterranean halophyte species Atriplex halimus L. J Plant Physiol 167:365–374PubMedCrossRefGoogle Scholar
  69. Lefèvre I, Vogel-Mikuš K, Jeromel L, Vavpetič P, Planchon S, Arčon I, Van Elteren JT, Lepoint G, Gobert S, Renaut J, Pelicon P, Lutts S (2014) Differential cadmium and zinc distribution in relation to their physiological impact in the leaves of the accumulating Zygophyllum fabago L. Plant Cell Environ 37:1299–1320PubMedCrossRefGoogle Scholar
  70. Leidi EO, Silberbush M, Lips SH (1991) Wheat growth as affected by nitrogen type, PH and salinity. I. Biomass production and mineral composition. J Plant Nutr 14:235–246CrossRefGoogle Scholar
  71. Lewis OAM, Leidi EO, Lips SH (1989) Effect of nitrogen source on growth response to salinity stress in maize and wheat. New Phytol 111:155–160CrossRefGoogle Scholar
  72. Lin WY, Lin SI, Chiou TJ (2009) Molecular regulators of phosphate homeostasis in plants. J Exp Bot 60:1427–1438PubMedCrossRefGoogle Scholar
  73. Liu X, Yang C, Zhang L, Li L, Liu S, Yu J, You L, Zhou D, Xia C, Zhao J, Wu H (2011) Metabolic profiling of cadmium-induced effects in one pioneer intertidal halophyte Suaeda salsa by NMR-based metabolomics. Ecotoxicology 20:1422–1431PubMedCrossRefGoogle Scholar
  74. Liu X, Wu H, Ji C, Wei L, Zhao J, Yu J (2013) An integrated proteomic and metabolomic study on the chronic effects of mercury in Suaeda salsa under an environmentally relevant salinity. PLoS One 8:e64041PubMedPubMedCentralCrossRefGoogle Scholar
  75. Lu YX, Li CJ, Zhang FS (2005) Transpiration, potassium uptake and flow in tobacco as affected by nitrogen forms and nutrient levels. Ann Bot 95:991–998PubMedPubMedCentralCrossRefGoogle Scholar
  76. Lutts S, Lefèvre I (2015) How can we take advantage of halophyte properties to cope with heavy metal toxicity in salt-affected areas? Ann Bot 115:509–528PubMedPubMedCentralCrossRefGoogle Scholar
  77. Lutts S, Lefèvre I, Delpérée C, Kivits S, Dechamps C, Robledo A, Correal E (2004) Heavy metal accumulation by the halophyte species Mediterranean saltbush. J Environ Qual 33:1271PubMedCrossRefGoogle Scholar
  78. Lutts S, Hausman JF, Quinet M, Lefèvre I (2012) Ecophysiology and responses of plants under salt stress, pp 315–353. Google Scholar
  79. Ma Q, Yue LJ, Zhang JL, Wu GQ, Bao AK, Wang SM (2012) Sodium chloride improves photosynthesis and water status in the succulent xerophyte Zygophyllum xanthoxylum. Tree Physiol 32:4–13PubMedCrossRefGoogle Scholar
  80. Mahmood T, Kaiser WM (2003) Growth and solute composition of the salt-tolerant kallar grass [Leptochloa fusca (L.) Kunth] as affected by nitrogen source. Plant Soil 252:359–366CrossRefGoogle Scholar
  81. 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 16:844–854CrossRefGoogle Scholar
  82. Manousaki E, Kalogerakis N (2011) Halophytes-an emerging trend in phytoremediation. Int J Phytoremediation 13:959–969PubMedCrossRefGoogle Scholar
  83. Martínez 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 56:2421–2431PubMedCrossRefGoogle Scholar
  84. Milic D, Lukovic J, Ninkov J, Zeremski-Skoric T, Zoric L, Vasin J, Milic S (2012) Heavy metal content in halophytic plants from inland and maritime saline areas. Cent Eur J Biol 7(2):307–317Google Scholar
  85. Mishra A, Tanna B (2017) Halophytes: potential resources for salt stress tolerance genes and promoters. Front Plant Sci 8:829. CrossRefPubMedPubMedCentralGoogle Scholar
  86. Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19PubMedCrossRefGoogle Scholar
  87. Mittler R, Blumwald E (2010) Genetic engineering for modern agriculture: challenges and perspectives. Annu Rev Plant Biol 61:443–462PubMedCrossRefGoogle Scholar
  88. Mommer L, Pons TL, Wolters-Arts M, Venema JH, Visser EJW (2005) Submergence-induced morphological, anatomical, and biochemical responses in a terrestrial species affect gas diffusion resistance and photosynthetic performance. Plant Physiol 139:497–508PubMedPubMedCentralCrossRefGoogle Scholar
  89. Munne-Bosch S, Queval G, Foyer CH (2013) The impact of global change factors on redox signaling underpinning stress tolerance. Plant Physiol 161:5–19PubMedCrossRefGoogle Scholar
  90. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681PubMedCrossRefGoogle Scholar
  91. Munzarova E, Lorenzen B, Brix H, Vojtiskova L, Votrubova O (2006) Effect of NH4+/NO3- availability on nitrate reductase activity and nitrogen accumulation in wetland helophytes Phragmites australis and Glyceria maxima. Environ Exp Bot 55:49–60CrossRefGoogle Scholar
  92. Nemat Alla MM, Khedr AHA, Serag MM, Abu-Alnaga AZ, Nada RM (2011) Physiological aspects of tolerance in Atriplex halimus L. to NaCl and drought. Acta Physiol Plant 33:547–557CrossRefGoogle Scholar
  93. Nieman RH, Clark R (1976) Interactive effects of salinity and phosphorus nutrition of the concentrations of phosphate and phosphate esters in mature photosynthesizing corn leaves. Plant Physiol 57:157–161PubMedPubMedCentralCrossRefGoogle Scholar
  94. Nikalje GC, Nikam TD, Suprasanna P (2017a) Looking at halophytic adaptation through mechanisms of ROS, redox regulation and signaling, Current Genomics, 18(6): 542–552Google Scholar
  95. Nikalje GC, Variyar PS, Joshi MV, Nikam TD, Suprasanna P (2017b) Ion homeostasis and accumulation of flavanoids and glycolipid in a halophyte Sesuvium portulacastrum (L.) L. Plos One 13(4): e0193394. PubMedPubMedCentralCrossRefGoogle Scholar
  96. Nikalje GC, Srivastava AK, Pandey GK, Suprasanna P (2017c) Halophytes in Biosaline Agriculture: mechanism, utilization and value added products. Land Degradation and Development CrossRefGoogle Scholar
  97. Ozgur R, Uzilday B, Sekmen AH, Turkan I (2013) Reactive oxygen species regulation and antioxidant defence in halophytes. Funct Plant Biol 40:832–847CrossRefGoogle Scholar
  98. Pedersen O, Binzer T, Borum J (2004) Sulphide intrusion in eelgrass (Zostera marina L.). Plant Cell Environ 27:595–602CrossRefGoogle Scholar
  99. Pedersen O, Vos H, Colmer TD (2006) Oxygen dynamics during submergence in the halophytic stem succulent Halosarcia pergranulata. Plant Cell Environ 29:1388–1399PubMedCrossRefGoogle Scholar
  100. Raghothama KG, Karthikeyan AS (2005) Phosphate acquisition. Plant Soil 274:37–49CrossRefGoogle Scholar
  101. Rastgoo L, Alemzadeh A (2011) Biochemical responses of Gouan (Aeluropus littoralis) to heavy metals stress. Aust J Crop Sci 5:375–383Google Scholar
  102. Reboreda R, Caçador I (2007) Halophyte vegetation influences in salt marsh retention capacity for heavy metals. Environ Pollut 146:147–154PubMedCrossRefGoogle Scholar
  103. Redondo-Gómez S (2013) Bioaccumulation of heavy metals in Spartina. Funct Plant Biol 40:913–921CrossRefGoogle Scholar
  104. Reef R, Lovelock CE (2015) Regulation of water balance in mangroves. Ann Bot 115:385–395PubMedCrossRefGoogle Scholar
  105. Rengel Z (1992) The role of calcium in salt toxicity. Plant Cell Environ 5:625–632CrossRefGoogle Scholar
  106. Rodrigo-Moreno A, Poschenrieder C, Shabala S (2013) Transition metals: a double edge sward in ROS generation and signaling. Plant Signal Behav 8:e23425PubMedPubMedCentralCrossRefGoogle Scholar
  107. Ryals JA, Neuenschwander UH, Willits MG, Molina A, Steiner HY, Hunt MD (1996) Systemic acquired resistance. Plant Cell 8:1809–1819PubMedPubMedCentralCrossRefGoogle Scholar
  108. Saslis-Lagoudakis CH, Hua X, Bui E, Moray C, Bromham L (2015) Predicting species’ tolerance to salinity and alkalinity using distribution data and geochemical modelling: a case study using Australian grasses. Ann Bot 115:343–351PubMedCrossRefGoogle Scholar
  109. Shabala S, Mackay A (2011) In: Kader JC, Delseny M (eds) Ion transport in halophytes, Adv Bot Res, vol 57. Academic, Burlington, pp 151–199Google Scholar
  110. Shabala S, Shabala L, Barcelo J, Poschenrieder C (2014) Membrane transporters mediating root signalling and adaptive responses to oxygen deprivation and soil flooding. Plant Cell Environ 37:2216–2233PubMedGoogle Scholar
  111. Sharma SS, Dietz KJ (2006) The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. J Exp Bot 57:711–726PubMedCrossRefGoogle Scholar
  112. Shepherd KA, Wilson PG (2007) Incorporation of the Australian genera Halosarcia, Pachycornia, Sclerostegia and Tegicornia into Tecticornia (Salicornioideae, Chenopodiaceae). Aust Syst Bot 20:319–331CrossRefGoogle Scholar
  113. Sirguey C, Ouvrard S (2013) Contaminated soils salinity, a threat for phytoextraction? Chemosphere 91:269–274PubMedCrossRefGoogle Scholar
  114. Slama I, Ghnaya T, Hessinia K, Messedi D, Savouré A, Abdelly C (2007) Comparative study of the effects of mannitol and PEG osmotic stress on growth and solute accumulation in Sesuvium portulacastrum. Environ Exp Bot 61:10–17CrossRefGoogle Scholar
  115. Slama I, Ghnaya T, Savouré 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 331:442–451PubMedCrossRefGoogle Scholar
  116. Slama I, Abdelly C, Bouchereau A, Flowers T, Savouré A (2015) Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress. Ann Bot 115:433–447PubMedPubMedCentralCrossRefGoogle Scholar
  117. Song J, Ding X, Feng G, Zhang F (2006) Nutritional and osmotic roles of nitrate in a euhalophyte and a xerophyte in saline conditions. New Phytol 171:357–366PubMedCrossRefGoogle Scholar
  118. Song J, Shi G, Xing S, Yin C, Fan H, Wang B (2009) Ecophysiological responses of the euhalophyte Suaeda salsa to the interactive effects of salinity and nitrate availability. Aquat Bot 91:311–317CrossRefGoogle Scholar
  119. Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97PubMedCrossRefGoogle Scholar
  120. 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 135:1697–1709PubMedPubMedCentralCrossRefGoogle Scholar
  121. Teakle NL, Real D, Colmer TD (2006) Growth and ion relations in response to combined salinity and waterlogging in the perennial forage legumes Lotus corniculatus and Lotus tenuis. Plant Soil 289:369–383CrossRefGoogle Scholar
  122. Teakle NL, Bazihizina N, Shabala S, Colmer TD, Barrett-Lennard EG, Rodrigo-Moreno A, Läuchli AE (2013) Differential tolerance to combined salinity and O2 deficiency in the halophytic grasses Puccinellia ciliata and Thinopyrum ponticum: the importance of K+ retention in roots. Environ Exp Bot 87:69–78CrossRefGoogle Scholar
  123. Tennstedt P, Peisker D, Bottcher C, Trampczynska A, Clemens S (2008) Phytochelatin synthesis is essential for the detoxification of excess zinc and contributes significantly to the accumulation of zinc. Plant Physiol 149:938–948PubMedCrossRefGoogle Scholar
  124. Thomas JC, Malick FK, Endreszl C, Davies EC, Murray KS (1998) Distinct responses to copper stress in the halophyte Mesembryanthemum crystallinum. Physiol Plant 102:360–368CrossRefGoogle Scholar
  125. Touchette BW, Burkholder JAM (2000) Review of nitrogen and phosphorus metabolism in seagrasses. J Exp Mar Biol Ecol 250:133–167PubMedCrossRefGoogle Scholar
  126. Usha B, Venkataraman G, Parida A (2009) Heavy metal and abiotic stress inducible metallothionein isoforms from Prosopis juliflora (SW) D.C. show differences in binding to heavy metals in vitro. Mol Genet Genomics 281:99–108PubMedCrossRefGoogle Scholar
  127. Uzilday B, Ozgur R, Sekmen AH, Yildiztugay E, Turkan I (2015) Changes in the alternative electron sinks and antioxidant defence in chloroplasts of the extreme halophyte Eutrema parvulum (Thellungiella parvula) under salinity. Ann Bot 115:449–463PubMedCrossRefGoogle Scholar
  128. Vázquez MD, Poschenriede C, Barcelo J, Baker AJM, Hatton P, Cope GH (1994) Compartmentation of zinc in roots and leaves of the zinc hyperaccumulator Thlaspi caerulescens. J C Presl Bot Acta 107:243–250CrossRefGoogle Scholar
  129. Walter J, Jentsch A, Beierkuhnlein C, Kreyling J (2013) Ecological stress memory and cross stress tolerance in plants in the face of climate extremes. Environ Exp Bot 94:3–8CrossRefGoogle Scholar
  130. Wang HL, Tian CY, Jiang L, Wang L (2014) Remediation of heavy metals contaminated saline soils: a halophyte choice? Environ Sci Technol 48:21–22PubMedCrossRefGoogle Scholar
  131. Wetson AM, Flowers TJ (2010) The effect of saline hypoxia on growth and ion uptake in Suaeda maritima. Funct Plant Biol 37:646–655CrossRefGoogle Scholar
  132. Wetson AM, Zarb C, John EA, Flowers TJ (2012) High phenotypic plasticity of Suaeda maritima observed under hypoxic conditions in relation to its physiological basis. Ann Bot 109:1027–1036PubMedPubMedCentralCrossRefGoogle Scholar
  133. Wilson C, Eller N, Gartner A, Vicente O, Heberle-Bors E (1993) Isolation and characterization of a tobacco cDNA clone encoding a putative MAP kinase. Plant Mol Biol 23:543–551PubMedCrossRefGoogle Scholar
  134. Winkel A, Colmer TD, Ismail AM, Pedersen O (2013) Internal aeration of paddy field rice Oryza sativa during complete submergence importance of light and floodwater O2. New Phytol 197:1193–1203PubMedCrossRefGoogle Scholar
  135. Wu H, Liu X, Zhao J, Yu J (2013) Regulation of metabolites, gene expression, and antioxidant enzymes to environmentally relevant lead and zinc in the halophyte Suaeda salsa. J Plant Growth Regul 32:353–361CrossRefGoogle Scholar
  136. Xu C, Tang X, Shao H, Wang H (2016) Salinity tolerance mechanism of economic halophytes from physiological to molecular hierarchy for improving food quality. Curr Genomics 17:207–214PubMedPubMedCentralCrossRefGoogle Scholar
  137. Yang XE, Long XX, Ye HB, He ZL, Calvert DV, Stoffella PJ (2004) Cadmium tolerance and hyperaccumulation in a new Zn-hyperaccumulating plant species (Sedum alfredii Hance). Plant Soil 259:181–189CrossRefGoogle Scholar
  138. Zaier H, Ghnaya T, Lakhdar A, Baioui R, Ghabriche R, Mnasri M, Sghair S, Lutts S, Abdelly C (2010) Comparative study of Pb-phytoextraction potential in Sesuvium portulacastrum and Brassica juncea: tolerance and accumulation. J Hazard Mater 183:609–615PubMedCrossRefGoogle Scholar
  139. Zepeda-Jazo I, Velarde-Buendía AM, Enríquez-Figueroa R, Bose J, Shabala S, Muñiz-Murguía J, Pottosin II (2011) Polyamines interact with hydroxyl radicals in activating Ca2+ and K+ transport across the root epidermal plasma membranes. Plant Physiol 157:2167–2180PubMedPubMedCentralCrossRefGoogle Scholar
  140. Zhu J, Meinzer FC (1999) Efficiency of C4 photosynthesis in Atriplex lentiformis under salinity stress. Aust J Plant Physiol 26:79Google Scholar
  141. Zribi OT, Labidi N, Slama I, Debez A, Ksouri R, Rabhi M, Smaoui, Abdelly C (2012) Alleviation of phosphorus deficiency stress by moderate salinity in the halophyte Hordeum maritimum L. Plant Growth Regul 66:75–85CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Ganesh Chandrakant Nikalje
    • 1
  • Kushi Yadav
    • 2
  • Suprasanna Penna
    • 3
    Email author
  1. 1.Department of Botany, R. K. Talreja College of Arts, Science and CommerceAffiliated to University of MumbaiThaneIndia
  2. 2.Dr. B. Lal Institute of BiotechnologyRajasthan UniversityJaipurIndia
  3. 3.Nuclear Agriculture and Biotechnology DivisionBhabha Atomic Research CentreMumbaiIndia

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