Contribution of Osmolyte Accumulation to Abiotic Stress Tolerance in Wild Plants Adapted to Different Stressful Environments

  • Oscar Vicente
  • Mohamad Al Hassan
  • Monica Boscaiu


Abiotic stresses, mostly drought and salinity, are the major environmental factors which limit plant distribution in nature and reduce crop yields worldwide. The biotechnological improvement of crop stress tolerance would significantly contribute to the needed increase in food production, but requires a deep understanding of the mechanisms underlying plant responses to stress. Accumulation of osmolytes is one of those responses, which appears to be essential for tolerance in many species. Their main assumed role is to contribute to osmotic adjustment under conditions causing cellular dehydration, but they also have osmoprotectant functions as low-molecular-weight chaperons and reactive oxygen species (ROS) scavengers. Yet, important aspects of their mechanisms of action remain largely unknown, especially regarding the relevance and relative contribution of specific osmolytes to the stress tolerance of a given species. This gap in our knowledge is partly due to the experimental approaches commonly used to study those mechanisms, which have focused on non-tolerant model species and/or experiments performed under controlled – but artificial – laboratory or greenhouse setups.

In this review, we will summarise the (relatively scarce) data from field studies on the accumulation of different osmolytes in wild plants adapted to distinct stressful environments: saline, arid and gypsum habitats. We propose that more effort and resources should be invested on the study of the stress responses of wild plants in their natural habitats, as a complement to greenhouse experiments. We believe that this approach will significantly enhance our knowledge on this specific topic and could eventually be applied to the genetic improvement of crops.


Salt Marsh Stress Tolerance Wild Plant Proline Content Soluble Carbohydrate 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Adrian-Romero M, Wilson SJ, Blunden G, Yang M, Carabot-Cuervo A, Bashir AK (1998) Betaines in coastal plants. Biochem Syst Ecol 26:535–543CrossRefGoogle Scholar
  2. Ain-Lhout F, Zunzunegui M, Diaz Barradas MC, Tirado R, Clavijo A, Garcia Novo F (2001) Comparison of proline accumulation in two Mediterranean shrubs subjected to natural and experimental water deficit. Plant Soil 230:175–183CrossRefGoogle Scholar
  3. Akashi K, Miyake C, Yokota A (2001) Citrulline, a novel compatible solute in drought-tolerant wild watermelon leaves, is an efficient hydroxyl radical scavenger. FEBS Lett 508:438–442CrossRefPubMedGoogle Scholar
  4. Albert R (1975) Salt regulation in halophytes. Oecologia 21:57–71CrossRefGoogle Scholar
  5. Albert R, Kinzel H (1973) Unterscheidung von Physiotypen bei Halophyten des Neusiedlerseegebietes (Österreich). (Distinction of physiotypes in halophytes from the Neusiedler Lake region, Austria). Z Pflanzenphysiol 70:138–158CrossRefGoogle Scholar
  6. Albert R, Popp M (1977) Chemical composition of halophytes from the Neusiedler Lake region in Austria. Oecologia 27:157–170CrossRefGoogle Scholar
  7. Albert R, Popp M (1978) Zur Rolle der löslichen Kohlenhydrate in Halophyten des Neusiedlersee-Gebietes (Österreich). (On the role of soluble carbohydrates in halophytes from the Neusiedler Lake region, Austria). Oecol Plant 13:27–42Google Scholar
  8. Alvarado JJ, Ruiz JM, López-Cantarero I, Molero J, Romero L (2000) Nitrogen metabolism in five plant species characteristic of gypsiferous soils. Plant Physiol 156:612–616CrossRefGoogle Scholar
  9. Ashraf MY, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216CrossRefGoogle Scholar
  10. Aziz I (2007) Seasonal flux in water potential, chlorophyll and proline content in plants at Ziarat Valley Balochistan, Pakistan. Pak J Bot 39:1995–2002Google Scholar
  11. Aziz I, Khan MA (2003) Proline and water status of some desert shrubs before and after water rains. Pak J Bot 35:902–906Google Scholar
  12. Aziz I, Gul B, Gulzar S, Khan MA (2011) Seasonal variation in plant water status of four desert halophytes from semi-arid region of Karachi. Pak J Bot 43:587–594Google Scholar
  13. Bankaji I, Sleimi N (2012) Polymorphisme biochimique chez quelques halophytes autochtones du nord Tunisien (Chemical polymorphism of some North Tunisian autochthonous halophytes). Rev Écol 67:29–39Google Scholar
  14. Bartels D, Ramanjulu S (2005) Drought and salt tolerance in plants. Plant Sci 24:23–58CrossRefGoogle Scholar
  15. Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58CrossRefGoogle Scholar
  16. Batanouny KH, Ebeid MM (1981) Diurnal changes in proline content of desert plants. Oecologia 51:250–252CrossRefGoogle Scholar
  17. Ben Hamed K, Ellouzi H, Zribi Talbi O, Hessini K, Slama I, Ghnaya T, Munné Bosch S, Savouré A, Abdelly C (2013) Physiological response of halophytes to multiple stresses. Funct Plant Biol 40:883–896Google Scholar
  18. Boscaiu M, Mora E, Fola O, Scrion S, Llinares J, Vicente O (2009) Osmolyte accumulation in xerophytes as a response to environmental stress. Bull UASVM Hort 66:96–102Google Scholar
  19. Boscaiu M, Bautista I, Lidón A, Llinares J, Lull C, Donat P, Mayoral O, Vicente O (2013a) Environmental-dependent proline accumulation in plants living on gypsum soils. Acta Physiol Plant 35:2193–2204CrossRefGoogle Scholar
  20. Boscaiu M, Lull C, Llinares J, Vicente O, Boira H (2013b) Proline as a biochemical marker in relation to the ecology of two halophytic Juncus species. J Plant Ecol 6:177–186CrossRefGoogle Scholar
  21. 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
  22. Burg MB, Kwon ED, Kültz D (1996) Osmotic regulation of gene expression. FASEB J 10:1598–1606PubMedGoogle Scholar
  23. Caballero I, Olano JM, Loidi J, Escudero A (2003) Seed bank structure along a semi-arid gypsum gradient in Central Spain. J Arid Environ 55:287–299CrossRefGoogle Scholar
  24. Chen THH, Murata N (2002) Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr Opin Plant Biol 5:250–257CrossRefPubMedGoogle Scholar
  25. Cushman JC (2001) Osmoregulation in plants: implications for agriculture. Am Zool 41:758–769Google Scholar
  26. DB Climate Change Advisors (2009) Investing in agriculture: far-reaching challenge, significant opportunity. An asset management perspective. (Deutsche Bank report). Whitepaper available online at:
  27. Doddema H, Eddin RS, Mahasneh A (1986) Effects of seasonal changes of soil salinity and soil nitrogen on the N-metabolism of the halophyte Arthrocnemum fruticosum (L.) Moq. Plant Soil 92:279–293CrossRefGoogle Scholar
  28. Duvigneaud P (1968) Essai de classification chimique (éléments minéraux) des plantes gypsicoles du bassin de l’Ebre (Test of chemical classification (mineral elements) of gypsophytes from the Ebro basin). B Soc Roy Bot 101:279–291Google Scholar
  29. Duvigneaud P, Denaeyer-De Smet S (1966) Accumulation du soufre dans quelques espèces gypsophiles d’Espagne (Sulphur accumulation in several species of gypsophytes from Spain). B Soc Roy Bot 99:263–269Google Scholar
  30. Epstein PR, Mills E (eds) (2005) Climate change futures. Health, ecological and economic dimensions. The Center for Health and the Global Environment, Harvard Medical School, HarvardGoogle Scholar
  31. Escudero A, Carnes LF, Pérez García F (1997) Seed germination of gypsophytes and gypsovags in semi-arid central Spain. J Arid Environ 36:487–497CrossRefGoogle Scholar
  32. Escudero A, Somolinos RC, Olano JM, Rubio A (1999) Factors controlling the establishment of Helianthemum squamatum, an endemic gypsophila of semi-arid Spain. J Ecol 87:290–302CrossRefGoogle Scholar
  33. FAO (1990) Management of gypsiferous soils, FAO Soils Bull 62. FAO, Rome: FAO Land and Water Development DivisionGoogle Scholar
  34. Ferriol M, Pérez I, Merle H, Boira H (2006) Ecological germination requirements of the aggregate species Teucrium pumilum (Labiatae) endemic to Spain. Plant Soil 284:205–216CrossRefGoogle Scholar
  35. Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol 179:945–963CrossRefPubMedGoogle Scholar
  36. Flowers TJ, Hajibagheri MA, Clipson NJW (1986) Halophytes. Q Rev Biol 61:313–335CrossRefGoogle Scholar
  37. 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
  38. Forment J, Naranjo MA, Roldán M, Serrano R, Vicente O (2002) Expression of Arabidopsis SR-like splicing proteins confers salt tolerance to yeast and transgenic plants. Plant J 30:511–519CrossRefPubMedGoogle Scholar
  39. Furtana GB, Duman H, Tipirdamaz R (2013) Seasonal changes of inorganic and organic osmolyte content in three endemic Limonium species of Lake Tuz (Turkey). Turk J Bot 37:455–463Google Scholar
  40. Gil R, Lull C, Boscaiu M, Bautista I, Lidón A, Vicente O (2011) Soluble carbohydrates as osmolytes in several halophytes from a Mediterranean salt marsh. Not Bot Horti Agrobo 39:9–17Google Scholar
  41. Gil R, Bautista I, Boscaiu M, Lidón A, Wankhade S, Sánchez H, Llinares J, Vicente O (2014) Responses of five Mediterranean halophytes to seasonal changes in environmental conditions. AoB Plants. doi: 10.1093/aobpla/plu049 PubMedCentralPubMedGoogle Scholar
  42. Gorham J, Hughes L, Wyn Jones RG (1980) Chemical composition of salt-marsh plants from Ynys Môn (Anglesey): the concept of physiotypes. Plant Cell Environ 3:309–318CrossRefGoogle Scholar
  43. Greenway H, Munns R (1980) Mechanisms of salt tolerance in non-halophytes. Annu Rev Plant Physiol 31:149–190CrossRefGoogle Scholar
  44. Hong Z, Lakkineni K, Zhang Z, Verma DPS (2000) Removal of feedback proline accumulation of ∆l-pyrroline-5-carboxylate synthetase results in increased proline accumulation and protection of plants from osmotic stress. Plant Physiol 122:1129–1136PubMedCentralCrossRefPubMedGoogle Scholar
  45. Hussain TM, Chandrasekhar T, Hazara M, Sultan Z, Saleh BK, Gopal GR (2008) Recent advances in salt stress biology – a review. Biotechnol Mol Biol Rev 3:8–13Google Scholar
  46. Inan G, Zhang Q, Li P, Wang Z, Cao Z, Zhang H, Zhang C, Quist TM, Goodwin SM, Zhu J, Shi H, Damsz B, Charbaji T, Gong Q, Ma S, Fredricksen M, Galbraith DW, Jenks MA, Rodees D, Hasegawa PM, Bohnert HJ, Joly RJ, Bressan RA, Zhu JK (2004) Salt stress. A halophyte and cryophyte Arabidopsis relative model system and its applicability to molecular genetic analyses of growth and development of extremophiles. Plant Physiol 135:1718–1737PubMedCentralCrossRefPubMedGoogle Scholar
  47. 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 29:1220–1234CrossRefPubMedGoogle Scholar
  48. Khan MA, Beena N (2002) Seasonal variation in water relations of desert shrubs from Karachi, Pakistan. Pak J Bot 34:329–340Google Scholar
  49. Khan MA, Ungar IA, Showalter AM (2000) The effect of the salinity on the growth, water status, and ion content of a leaf succulent perennial halophyte, Suaeda fruticosa (L) Forssk. J Arid Environ 45:73–84CrossRefGoogle Scholar
  50. Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63:1593–1608PubMedCentralCrossRefPubMedGoogle Scholar
  51. Llinares JV, Bautista I, Donat MP, Lidon A, Lull C, Mayoral O, Shantanu W, Boscaiu M, Vicente O (2015) Responses to environmental stress in plants adapted to Mediterranean gypsum habitats. Not Sci Biol 7:37–44CrossRefGoogle Scholar
  52. Martínez-Duro E, Ferrandis P, Escudero A, Luzuriaga AL, Herranz JM (2010) Secondary old-field succession in an ecosystem with restrictive soils: does time from abandonment matter? Appl Veg Sci 13:234–248CrossRefGoogle Scholar
  53. Merlo ME, Mota JF, Cabello J, Alemán MM (1998) La gipsofilia en plantas: un apasionante edafismo. Investigación y Gestión 3:103–112Google Scholar
  54. Meyer SE (1986) The ecology of gypsophyle endemism in the eastern Mojave desert. Ecology 67:1303–1313CrossRefGoogle Scholar
  55. Meyer SE, García-Moya E (1989) Plant community patterns and soil moisture regime in gypsum grasslands of north central Mexico. J Arid Environ 16:147–155Google Scholar
  56. Meyer SE, García-Moya E, Lagunes-Espinoza LC (1992) Topographic and soil surface effects on gypsophila plant community patterns in central Mexico. J Veg Sci 3:429–438CrossRefGoogle Scholar
  57. Mohammed S, Sen DN (1987) Proline accumulation in arid zones plants. J Arid Environ 13:231–236Google Scholar
  58. Moruno F, Soriano P, Vicente O, Boscaiu M, Estrelles E (2011) Opportunistic germination behaviour of Gypsophila (Caryophyllaceae) in two priority habitats from semi-arid Mediterranean steppes. Not Bot Horti Agrobo 39:18–23Google Scholar
  59. Mota JF, Sola AJ, Jiménez-Sánchez ML, Pérez-García F, Merlo ME (2004) Gypsicolous flora, conservation and restoration of quarries in the southeast of the Iberian Peninsula. Biodivers Conserv 13:1797–1808CrossRefGoogle Scholar
  60. Mouri C, Benhassaini H, Bendimered FZ, Belkhodja M (2012) Variation saisonnière de la teneur en proline et en sucres solubles chez l’oyat (Ammophila arenaria (L.) Link) provenant du milieu naturel de la côte ouest de l’Algérie. Acta Bot Gallica 159:127–135CrossRefGoogle Scholar
  61. Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250CrossRefPubMedGoogle Scholar
  62. Munns R, Greenway H, Kirst GO (1983) Halotolerant eukaryotes. In: Lange OL, Nobel PS, Osmond CB, Ziegler H (eds) Encyclopedia of plant physiology III, vol 12c. Physiological plant ecology. Springer, Berlin, pp 59–135Google Scholar
  63. Murakeözy ÉP, Smirnoff N, Nagy Z, Tuba Z (2002) Seasonal accumulation pattern of pinitol and other carbohydrates in Limonium gmelinii subsp. hungarica. J Plant Physiol 159:485–490CrossRefGoogle Scholar
  64. Murakeözy ÉP, Nagy Z, Duhazé C, Bouchereau A, Tuba Z (2003) Seasonal changes in the levels of compatible osmolytes in three halophytic species of inland saline vegetation in Hungary. J Plant Physiol 160:395–401CrossRefPubMedGoogle Scholar
  65. Palacio S, Escudero A, Montserrat-Martí G, Maestro M, Milla R, Albert M (2007) Plants living on gypsum: beyond the specialist model. Ann Bot 99:333–343PubMedCentralCrossRefPubMedGoogle Scholar
  66. Palacio S, Aitkenhead M, Escudero A, Montserrat-Martí G, Maestro M, Robertson AH (2014) Gypsophila chemistry unveiled: Fourier transform infrared (FTIR) spectroscopy provides new insight into plant adaptations to gypsum soils. PLoS One. doi: 10.1371/journal.pone.0107285 Google Scholar
  67. Pardo-Domènech LL, Tifrea A, Grigore MN, Boscaiu M, Vicente O (2015) Proline and glycine betaine accumulation in two succulent halophytes under natural and experimental conditions. Plant Biosyst. doi: 10.1080/11263504.2014.990943 Google Scholar
  68. Parsons RF (1976) Gypsophily in plants. A review. Am Midl Nat 96:1–20CrossRefGoogle Scholar
  69. Pueyo Y, Alados CL, Maestro M, Komac B (2007) Gypsophila vegetation patterns under a range of soil properties induced by topographical position. Plant Ecol 189:301–311CrossRefGoogle Scholar
  70. Romao RL, Escudero A (2005) Gypsum physical soil crusts and the existence of gypsophytes in semi-arid central Spain. Plant Ecol 181:127–137CrossRefGoogle Scholar
  71. Ruíz JM, López-Cantarero I, Rivero RM, Romero L (2003) Sulphur phytoaccumulation in plant species characteristic of gypsiferous soils. Int J Phytorem 5:203–210CrossRefGoogle Scholar
  72. Sairam RK, Tyagi A (2004) Physiology and molecular biology of salinity stress tolerance in plants. Curr Sci 86:407–421Google Scholar
  73. Sanders D (2000) The salty tale of Arabidopsis. Curr Biol 10:486–488CrossRefGoogle Scholar
  74. Sayed SA, Gadallah MAA, Salama FM (2013) Ecophysiological studies on three desert plants growing in Wadi Natash, Eastern Desert, Egypt. J Biol Earth Sci 3:B135–B143Google Scholar
  75. Serrano R (1996) Salt tolerance in plants and microorganisms: toxicity targets and defence responses. Int Rev Cytol 165:1–52CrossRefPubMedGoogle Scholar
  76. Serrano R, Gaxiola R (1994) Microbial models and salt stress tolerance in plants. Crit Rev Plant Sci 13:121–138CrossRefGoogle Scholar
  77. Shen B, Jensen RG, Bohnert HJ (1997) Mannitol protects against oxidation by hydroxyl radicals. Plant Physiol 115:527–532PubMedCentralPubMedGoogle Scholar
  78. Steudle E (2000) Water uptake by roots: effects of water deficit. J Exp Bot 51:1531–1542CrossRefPubMedGoogle Scholar
  79. Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97CrossRefPubMedGoogle Scholar
  80. Tipirdamaz R, Gagneul D, Duhazé C, Aïnouche A, Monnier C, Özkum 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 57:139–153CrossRefGoogle Scholar
  81. Türkan I, Demiral T (2009) Recent developments in understanding salinity tolerance. Environ Exp Bot 67:2–9CrossRefGoogle Scholar
  82. Valladares F (2003) Light heterogeneity and plants: from ecophysiology to species coexistence and biodiversity. Progress Bot 64:439–471CrossRefGoogle Scholar
  83. Verheye WH, Boyadgiev TG (1997) Evaluating the land use potential of gypsiferous soils from field pedogenic characteristics. Soil Use Manag 13:97–103CrossRefGoogle Scholar
  84. Vicente O, Boscaiu M, Naranjo MA, Estrelles E, Bellés JM, Soriano P (2004) Responses to salt stress in the halophyte Plantago crassifolia (Plantaginaceae). J Arid Environ 58:463–481CrossRefGoogle Scholar
  85. Vinocur B, Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotechnol 16:123–132CrossRefPubMedGoogle Scholar
  86. Yancey PH, Clark ME, Hand SC, Bowlus RD, Somero GN (1982) Living with water stress: evolution of osmolyte systems. Science 217:1214–1222CrossRefPubMedGoogle Scholar
  87. Yanqiong L, Xingliang L, Shaowei Z, Hong C, Yongjie Y, Changlong M, Jun L (2007) Drought-resistant physiological characteristics of four shrub species in arid valley of Minjiang River, China. Acta Ecol Sin 27:870–878CrossRefGoogle Scholar
  88. Yeo A (1998) Molecular biology of salt tolerance in the context of whole-plant physiology. J Exp Bot 49:915–929Google Scholar
  89. Youssef AM (2009) Salt tolerance mechanisms in some halophytes from Saudi Arabia and Egypt. Res J Agric Biol Sci 5:191–206Google Scholar
  90. Zhou H, Tan H, Zhang Z-S, Jia X, Fan H, Yuan J (2010) Physiological responses and adjustment mechanisms of the dominate species of natural vegetation of Eastern Tengger Desert. Sci Cold Arid Reg 2:455–463Google Scholar
  91. Zhu J-K (2000) Genetic analysis of plant salt tolerance using Arabidopsis. Plant Physiol 124:941–948PubMedCentralCrossRefPubMedGoogle Scholar
  92. Zhu J-K (2001) Plant salt tolerance. Trends Plant Sci 6:66–71CrossRefPubMedGoogle Scholar

Copyright information

© Springer India 2016

Authors and Affiliations

  • Oscar Vicente
    • 1
  • Mohamad Al Hassan
    • 1
  • Monica Boscaiu
    • 2
  1. 1.Institute for Plant Molecular and Cellular Biology (IBMCP, UPV-CSIC)Universitat Politècnica de ValènciaValenciaSpain
  2. 2.Mediterranean Agroforestal Institute (IAM, UPV)Universitat Politècnica de ValènciaValenciaSpain

Personalised recommendations