Journal of Plant Research

, Volume 131, Issue 6, pp 1029–1046 | Cite as

Salt tolerance mechanisms in three Irano-Turanian Brassicaceae halophytes relatives of Arabidopsis thaliana

  • Roghieh HajibolandEmail author
  • Sara Bahrami-Rad
  • Hossein Akhani
  • Charlotte Poschenrieder
Regular Paper


Salt tolerance mechanisms were studied in three Irano-Turanian halophytic species from the Brassicaceae ‎‎(Lepidium latifolium, L. perfoliatum and Schrenkiella parvula) and compared with the glycophyte Arabidopsis thaliana. According to seed germination under salt stress, L. perfoliatum was the most tolerant species, while L. latifolium and S. parvula were rather susceptible. Contrastingly, based on biomass production L. perfoliatum was more salt sensitive than the other two species. In S. parvula biomass was increased up to 2.8-fold by 100 mM NaCl; no significant growth reduction was observed even when exposed to 400 mM NaCl. Stable activities of antioxidative defense enzymes, nil or negligible accumulation of superoxide anion and hydrogen peroxide, as well as stable membrane integrity in the three halophytes revealed that no oxidative stress occurred in these tolerant species under salt stress. Proline levels increased in response to salt treatment. However, it contributed only by 0.3‒2.0% to the total osmolyte concentration in the three halophytes (at 400 mM NaCl) and even less (0.04%) in the glycophyte, A. thaliana (at 100 mM NaCl). Soluble sugars in all three halophytes and free amino acids pool in S. parvula decreased under salt treatment in contrast to the glycophyte, A. thaliana. The contribution of organic osmolytes to the total osmolyte pool increased by salt treatment in the roots, while decreased in halophyte and glycophyte, A. thaliana leaves. Interestingly, this reduction was compensated by a higher relative contribution of K in the leaves of the halophytes, but of Na in A. thaliana. Taken together, biomass data and biochemical indicators show that S. parvula is more salt tolerant than the two Lepidium species. Our data indicate that L. latifolium, as a perennial halophyte with a large biomass, is highly suitable for both restoration of saline habitats and saline agriculture.


Antioxidative defense system Brassicaceae Lepidium latifolium L. Lepidium perfoliatum L. Organic osmolytes Schrenkiella parvula 



R.H. and S. B.-R. thank Research Deputy Office, University of Tabriz, Iran for providing a postdoctoral fellowship for S. B.-R.


This work has been supported by the Center for International Scientific Studies & Collaboration (CISSC), Iran. C.P. thanks support from project SAL-CAL-MED from Spanish MICINN BFU2016-75176-R.

Compliance with ethical standards

Conflict of interest

The authors declare that there is no conflict of interest regarding the publication of this paper.

Supplementary material

10265_2018_1053_MOESM1_ESM.pdf (1 mb)
Supplementary material 1 (PDF 1052 KB)


  1. Akhani H (1988) Plant records from Kavire-Meyghan (Arak), new to Iran. Iranian J Bot 4:105–107Google Scholar
  2. Akhani H (2006) Biodiversity of halophytic and sabkha ecosystems in Iran. In: Khan MA, Böer B, Kust GS, Barth H-J (eds) Sabkha ecosystems. Springer, Dordrecht, pp 71–88CrossRefGoogle Scholar
  3. Akhani H (2016) Plant diversity of saline wetlands and salt marshes of Iran. In: U.S.-Iran Symposium on Wetlands. University of Arizone, Irvine, pp 38–45Google Scholar
  4. Alemán F, Nieves-Cordones M, Martínez V, Rubio F (2009) Potassium/sodium steady-state homeostasis in Thellungiella halophila and Arabidopsis thaliana under long-term salinity conditions. Plant Sci 176:768–774CrossRefGoogle Scholar
  5. Amor NB, Jiménez A, Megdiche W, Lundqvist M, Sevilla F, Abdelly C (2007) Kinetics of the anti-oxidant response to salinity in the halophyte Cakile maritima. J Integr Plant Biol 49:982–992CrossRefGoogle Scholar
  6. Aronson JA (1989) HALOPH, a database of salt tolerant plants of the world. Office of Arid Lands Studies, University of Arizona, TucsonGoogle Scholar
  7. Bahrami-Rad S, Hajiboland R (2017) Effect of potassium application in drought-stressed tobacco (Nicotiana rustica L.) plants: Comparison of root with foliar application. Ann Agric Sci 62:121–130CrossRefGoogle Scholar
  8. Barcelo J, Poschenrieder C, Gunsé B (1986) Water relations of chromium VI treated bush bean plants (Phaseous vulgaris L. cv Contender) under both normal and water stress conditions. J Exp Bot 37:178–187CrossRefGoogle Scholar
  9. Benton Jones J Jr (1999) Soil analysis: handbook of reference methods. CRC Press, Boca RatonGoogle Scholar
  10. Bose J, Rodrigo-Moreno A, Shabala S (2014) ROS homeostasis in halophytes in the context of salinity stress tolerance. J Exp Bot 65:1241–1257CrossRefGoogle Scholar
  11. Bressan RA, Zhang C, Zhang H, Hasegawa PM, Bohnert HJ, Zhu JK (2001) Learning from the Arabidopsis experience. The next gene search paradigm. Plant Physiol 127:1354–1360CrossRefGoogle Scholar
  12. Cabot C, Sibole JV, Poschenrieder C (2014) Lessons from crops struggling with salinity. Plant Sci 226:2–13CrossRefGoogle Scholar
  13. Caldwell MM (1974) Physiology of desert halophytes. In: Reimold RJ, Queen WH (eds) Ecology of halophytes. Academic Press, New York, pp 355–378CrossRefGoogle Scholar
  14. Chaitanya KK, Naithani SC (1994) Role of superoxide, lipid peroxidation and superoxide dismutase in membrane perturbation during loss of viability in seeds of Shorea robusta Gaertn. f. New Phytol 126:623–627CrossRefGoogle Scholar
  15. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743CrossRefGoogle Scholar
  16. Conn SJ, Hocking B, Dayod M, Xu B, Athman A, Henderson S, Aukett L, Conn V, Shearer MK, Fuentes S, Tyerman SD (2013) Protocol: optimising hydroponic growth systems for nutritional and physiological analysis of Arabidopsis thaliana and other plants. Plant Methods 9:4CrossRefGoogle Scholar
  17. Dassanayake M, Oh DH, Haas JS, Hernandez A, Hong H, Ali S, Yun DJ, Bressan RA, Zhu JK, Bohnert HJ, Cheeseman JM (2011) The genome of the extremophile crucifer Thellungiella parvula. Nat Genet 43:913CrossRefGoogle Scholar
  18. de Vos AC, Broekman R, de Almeida Guerra CC, van Rijsselberghe M, Rozema J (2013) Developing and testing new halophyte crops: a case study of salt tolerance of two species of the Brassicaceae, Diplotaxis tenuifolia and Cochlearia officinalis. Environ Exp Bot 92:154–164CrossRefGoogle Scholar
  19. Debez A, Hamed KB, Grignon C, Abdelly C (2004) Salinity effects on germination, growth, and seed production of the halophyte Cakile maritima. Plant Soil 262:179–189CrossRefGoogle Scholar
  20. Demidchik V (2018) ROS-activated ion channels in plants: biophysical characteristics, physiological functions and molecular nature. Int J Mol Sci 19:1263CrossRefGoogle Scholar
  21. Djamali M, Akhani H, Khoshravesh R, Andrieu-Ponel V, Ponel P, Brewer S (2011) Application of the global bioclimatic classification to Iran: implications for understanding the modern vegetation and biogeography. Ecol Medit 37:91–114Google Scholar
  22. Ellouzi H, Hamed KB, Hernández I, Cela J, Müller M, Magné C, Abdelly C, Munné-Bosch S (2014) A comparative study of the early osmotic, ionic, redox and hormonal signaling response in leaves and roots of two halophytes and a glycophyte to salinity. Planta 240:1299–1317CrossRefGoogle Scholar
  23. FAO (2000) Global network on integrated soil management for sustainable use of salt-affected soils. Rome. Accessed 5 March 2018
  24. Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol 179:945–963CrossRefGoogle Scholar
  25. 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
  26. Foyer CH, Noctor G (2003) Redox sensing and signaling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant 119:355–364CrossRefGoogle Scholar
  27. FrancisA,WarwickSI(2007) The biology of invasive alien plants in Canada. 8. Lepidium latifolium L. Can J Plant Sci 87:639–658CrossRefGoogle Scholar
  28. Ghars MA, Parre E, Debez A, Bordenave M, Richard L, Leport L, Bouchereau A, Savouré A, Abdelly C (2008) Comparative salt tolerance analysis between Arabidopsis thaliana and Thellungiella halophila, with special emphasis on K+/Na+ selectivity and proline accumulation. J Plant Physiol 165:588–599CrossRefGoogle Scholar
  29. Glenn EP, Brown JJ, Blumwald E (1999) Salt tolerance and crop potential of halophytes. Crit Rev Plant Sci 18:227–255CrossRefGoogle Scholar
  30. Gong Q, Li P, Ma S, Indu Rupassara S, Bohnert HJ (2005) Salinity stress adaptation competence in the extremophile Thellungiella halophila in comparison with its relative Arabidopsis thaliana. Plant J 44:826–839CrossRefGoogle Scholar
  31. Gul B, Ansari R, Flowers TJ, Khan MA (2013) Germination strategies of halophyte seeds under salinity. Environ Exp Bot 92:4–18CrossRefGoogle Scholar
  32. Hajiboland R, Aliasgharzadeh N, Laiegh SF, Poschenrieder C (2010) Colonization with arbuscular mycorrhizal fungi improves salinity tolerance of tomato (Solanum lycopersicum L.) plants. Plant Soil 331:313–327CrossRefGoogle Scholar
  33. Hajiboland R, Dashtebani F, Aliasgharzad N (2015) Physiological responses of halophytic C4 grass Aeluropus littoralis to salinity and arbuscular mycorrhizal fungi colonization. Photosynthetica 53:572–584CrossRefGoogle Scholar
  34. Hedge IC (1968) Cruciferae (Lepidium and Arabidopsis). In: Rechinger KH (ed) Flora Iranica, vol 57. Akademische Druck u. Verlagsanstalt, Graz, pp 65–72 , 328–334Google Scholar
  35. Huang CH, Sun RR, Hu Y, Zeng LP, Zhang N, Cai LM, Zhang Q, Koch MA, Al-Shehbaz I, Edger PP, Pires JC, Tan DY, Zhong Y, Ma H (2016) Resolution of Brassicaceae phylogeny using nuclear genes uncovers nested radiations and supports convergent morphological evolution. Mol Biol Evol 33:394–412CrossRefGoogle Scholar
  36. Inan G, Zhang Q, Li P, Wang Z, Cao Z, Zhang H, Zhang C, Quist TM, Goodwin SM, Zhu J, Shi H (2004) Salt cress. A halophyte and cryophyte Arabidopsis relative model system and its applicability to molecular genetic analyses of growth and development of extremophiles. Plant Physiol 135:1718–1737CrossRefGoogle Scholar
  37. Jithesh MN, Prashanth SR, Sivaprakash KR, Parida AK (2006) Antioxidative response mechanisms in halophytes: their role in stress defence. J Genetics 85:237CrossRefGoogle Scholar
  38. Joshi AJ (1981) Amino acids and mineral constituents in Sesuvium portulacastrum L., a salt marsh halophyte. Aquat Bot 10:69–74CrossRefGoogle Scholar
  39. Kawano T (2003) Roles of the reactive oxygen species-generating peroxidase reactions in plant defense and growth induction. Plant Cell Rep 21:829–837PubMedGoogle Scholar
  40. Khan MA, Gul B (2006) Halophyte seed germination. In: Khan MA, Weber DJ (eds) Eco-physiology of high salinity tolerant plants. Springer, Dordrecht, pp 11–30CrossRefGoogle Scholar
  41. Koornneef M, Meinke D (2010) The development of Arabidopsis as a model plant. Plant J 61:909–921CrossRefGoogle Scholar
  42. Kosová K, Vítámvás P, Urban MO, Prášil IT (2013) Plant proteome responses to salinity stress–comparison of glycophytes and halophytes. Funct Plant Biol 40:775–786CrossRefGoogle Scholar
  43. Lugan R, Niogret MF, Leport L, Guégan JP, Larher FR, Savouré A, Kopka J, Bouchereau A (2010) Metabolome and water homeostasis analysis of Thellungiella salsuginea suggests that dehydration tolerance is a key response to osmotic stress in this halophyte. Plant J 64:215–229CrossRefGoogle Scholar
  44. M’rah S, Ouerghi Z, Berthomieu C, Havaux M, Jungas C, Hajji M, Grignon C, Lachaâl M (2006) Effects of NaCl on the growth, ion accumulation and photosynthetic parameters of Thellungiella halophila. J Plant Physiol 163:1022–1031CrossRefGoogle Scholar
  45. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681CrossRefGoogle Scholar
  46. Oh DH, Hong H, Lee SY, Yun DJ, Bohnert HJ, Dassanayake M (2014) Genome structures and transcriptomes signify niche adaptation for the multiple-ion-tolerant extremophyte Schrenkiella parvula. Plant Physiol 164:2123–2138CrossRefGoogle Scholar
  47. Orsini F, D’urzo MP, Inan G, Serra S, Oh DH, Mickelbart MV, Consiglio F, Li X, Jeong JC, Yun DJ, Bohnert HJ (2010) A comparative study of salt tolerance parameters in 11 wild relatives of Arabidopsis thaliana. J Exp Bot 61:3787–3798CrossRefGoogle Scholar
  48. 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
  49. Pottosin I, Velarde-Buendía AM, Bose J, Zepeda-Jazo I, Shabala S, Dobrovinskaya O (2014) Cross-talk between reactive oxygen species and polyamines in regulation of ion transport across the plasma membrane: implications for plant adaptive responses. J Exp Bot 65:1271–1283CrossRefGoogle Scholar
  50. Raven JA (1985) Regulation of pH and generation of osmolarity in vascular plants—a cost-benefit analysis in relation to efficiency of use of energy, nitrogen and water. New Phytol 101:25–77CrossRefGoogle Scholar
  51. Renz MJ, Blank RR (2004) Influence of perennial pepperweed (Lepidium latifolium) biology and plant–soil relationships on management and restoration. Weed Technol 18:1359–1363CrossRefGoogle Scholar
  52. Richards SL, Laohavisit A, Mortimer JC, Shabala L, Swarbreck SM, Shabala S, Davies JM (2014) Annexin 1 regulates the H2O2-induced calcium signature in Arabidopsis thaliana roots. Plant J 77:136–145CrossRefGoogle Scholar
  53. Rozema J, Schat H (2013) Salt tolerance of halophytes, research questions reviewed in the perspective of saline agriculture. Environ Exp Bot 92:83–95CrossRefGoogle Scholar
  54. Scott SJ, Jones RA, Williams WA (1984) Review of data analysis methods for seed germination. J Crop Sci 24:1192–1199CrossRefGoogle Scholar
  55. Shabala S, Mackay A (2011) Ion transport in halophytes. In: Turkan I (ed) Plant responses to drought and salinity stress, developments in a post-genomic era. Advances in Botanical Research, Vol. 57. Elsevier, Amsterdam, pp 151–199CrossRefGoogle Scholar
  56. Sibole JV, Cabot C, Michalke W, Poschenrieder C, Barceló J (2005) Relationship between expression of the PM H+-ATPase, growth and ion partitioning in the leaves of salt-treated Medicago species. Planta 221:557–566CrossRefGoogle Scholar
  57. 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 115:433–447CrossRefGoogle Scholar
  58. Szabados L, Savoure A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97CrossRefGoogle Scholar
  59. 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 135:1697–1709CrossRefGoogle Scholar
  60. Tran D, El-Maarouf-Bouteau H, Rossi M, Biligui B, Briand J, Kawano T, Mancuso S, Bouteau F (2013) Post-transcriptional regulation of GORK channels by superoxide anion contributes to increases in outward-rectifying K + currents. New Phytol 198:1039–1048CrossRefGoogle Scholar
  61. 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 115:449–463CrossRefGoogle Scholar
  62. 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 57:1161–1170CrossRefGoogle Scholar
  63. 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 157:2167–2180CrossRefGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan KK, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Plant ScienceUniversity of TabrizTabrizIran
  2. 2.Halophytes and C4 Plants Research Laboratory, Department of Plant Science, School of BiologyUniversity of TehranTehranIran
  3. 3.Plant Physiology Laboratory, Bioscience FacultyUniversidad Autónoma de BarcelonaBellaterraSpain

Personalised recommendations