Plant Soil Environ., 2025, 71(5):320-337 | DOI: 10.17221/73/2025-PSE

Halophytic resilience in extreme environments: adaptive strategies of Suaeda schimperi in the Red Sea’s hyper-arid salt marshesOriginal Paper

Farag Ibraheem ORCID...1, Mohammed Albaqami2, Eman M. Elghareeb ORCID...3
1 Umm Al-Qura University, Al-Qunfodah University College, Biology and Chemistry Department, Al-Qunfodah, Saudi Arabia
2 Botany and Microbiology Department, College of Science, King Saud University, Riyadh, Saudi Arabia
3 Botany Department, Faculty of Science, Mansoura University, Mansoura, Egypt

Suaeda schimperi, a halophyte native to the Red Sea’s hyper-arid salt marshes, thrives in its extreme conditions (high salinity, minimal rainfall, and elevated temperatures). However, its adaptive tolerance mechanisms to these harsh conditions remain unclear. Herein, we investigated its growth responses and physiological mechanisms after short (5 days after treatment; DAT) and long-term (15 DAT) exposure to 0, 100, 200, and 400 mmol NaCl. Moderate salinity (200 mmol NaCl) enhanced growth, inducing 103.2% (5 DAT) and 40% (15 DAT) higher leaf biomass and 43.33% and 59.6% higher root biomass, respectively, compared to non-saline conditions. Deviation from moderate salinity reduced growth and disrupted ion balance, lowering K+, raising Na+, and increasing the Na+/K+ ratio, particularly under high salinity. The moderate salinity-enhanced growth was associated with increased chlorophyll, glycine betaine, glutathione, betacyanin, and betaxanthin, as well as higher antioxidant enzyme activity (polyphenol oxidase, peroxidase, catalase, ascorbate, and peroxidase) at 5 DAT. At 15 DAT, sugar accumulation and unsaturated fatty acids increased, while malondialdehyde and saturated fatty acids decreased. These findings reveal multiple adaptive strategies that support S. schimperi’s physiological stability under extreme environments and highlight its significance in ecological restoration and breeding salt-tolerant crops under escalating soil salinisation and climate change.

Keywords: osmotic stress; saline habitat; adaptation; salt tolerance

Received: February 23, 2025; Revised: April 28, 2025; Accepted: May 5, 2025; Prepublished online: May 23, 2025; Published: May 29, 2025  Show citation

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Ibraheem F, Albaqami M, Elghareeb EM. Halophytic resilience in extreme environments: adaptive strategies of Suaeda schimperi in the Red Sea’s hyper-arid salt marshes. Plant Soil Environ. 2025;71(5):320-337. doi: 10.17221/73/2025-PSE.
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References

  1. Agarwal S., Shaheen R. (2007): Stimulation of antioxidant system and lipid peroxidation by abiotic stresses in leaves of Momordica charantia. Brazilian Journal of Plant Physiology, 19: 149-161. Go to original source...
  2. Ahmed M., Tóth Z., Decsi K. (2024): The impact of salinity on crop yields and the confrontational behaviour of transcriptional regulators, nanoparticles, and antioxidant defensive mechanisms under stressful conditions: a review. International Journal of Molecular Sciences, 25: 2654. Go to original source...
  3. Alexieva V., Sergiev I., Mapelli S., Karanov E. (2001): The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant, Cell and Environment, 24: 1337-1344. Go to original source...
  4. Al-Shamsi N., Hussain M.I., El-Keblawy A. (2020): Physiological responses of the xerohalophyte Suaeda vermiculata to salinity in its hyper-arid environment. Flora, 273: 151705. Go to original source...
  5. Ayub M.A., Rehman M.Z.U., Umar W., Farooqi Z.U.R., Sarfraz M., Ahmad H.R., Ahmad Z., Aslam M.Z. (2022): Role of glycine betaine in stress management in plants. Emerging Plant Growth Regulators in Agriculture: Roles in Stress Tolerance, 2022: 335-356. Go to original source...
  6. Bates L.S., Waldren R.P., Teare I.D. (1973): Rapid determination of free proline for water-stress studies. Plant and Soil, 39: 205-207. Go to original source...
  7. Behr J.H., Bouchereau A., Berardocco S., Seal C.E., Flowers T.J., Zörb C. (2017): Metabolic and physiological adjustment of Suaeda maritima to combined salinity and hypoxia. Annals of Botany, 119: 965-976. Go to original source...
  8. 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 Science, 168: 889-899. Go to original source...
  9. Ben Hamed K., Castagna A., Salem E., Ranieri A., Abdelly C. (2007): Sea fennel (Crithmum maritimum L.) under salinity conditions: a comparison of leaf and root antioxidant responses. Plant Growth Regulation, 53: 185-194. Go to original source...
  10. Boughalleb F., Abdellaoui R., Mahmoudi M., Bakhshandeh E. (2020): Changes in phenolic profile, soluble sugar, proline, and antioxidant enzyme activities of Polygonum equisetiforme in response to salinity. Turkish Journal of Botany, 44: 25-35. Go to original source...
  11. Boulos L. (1999): Flora of Egypt. Cairo, Al Hadara Publishing, 419.
  12. Bueno M., Lendínez M.L., Calero J., del Pilar Cordovilla M. (2020): Salinity responses of three halophytes from inland saltmarshes of Jaén (southern Spain). Flora, 266: 151589. Go to original source...
  13. Cai L.Y., Li M., Shen Y.F., Jiang R.T., Wang J.W., Ma S.Z., Wu M.Q., He P.M. (2025): Betacyanin accumulation mediates photosynthetic protection in Suaeda salsa (L.) Pall. under salt stress. Planta, 261: 100. Go to original source... Go to PubMed...
  14. Castillo J.M., Mancilla-Leytón J.M., Martins-Noguerol R., Moreira X., Moreno-Pérez A.J., Muñoz-Vallés S., Pedroche J.J., Figueroa M.E., García-González A., Salas J.J., Cambrollé J. (2022): Interactive effects between salinity and nutrient deficiency on biomass production and bio-active compounds accumulation in the halophyte Crithmum maritimum. Scientia Horticulturae, 301: 111136. Go to original source...
  15. Collenette S. (1985): Illustrated Guide to the Flowers of Saudi Arabia. London, Scorpion.
  16. Darbyshire I., Pickering H., Kordofani M., Farag I., Candiga R. (2015): The plants of Sudan and South Sudan: An Annotated Checklist. Kew, Royal Botanic Gardens, 400.
  17. Devi P. (2002): Principles and Methods in Plant Molecular, Biology, Biochemistry and Genetics. Jodhpur, Agrobios. ISBN-10: 8188826286
  18. Diao F., Dang Z., Xu J., Ding S., Hao B., Zhang Z., Zhang J., Wang L., Guo W. (2021): Effect of arbuscular mycorrhizal symbiosis on ion homeostasis and salt tolerance-related gene expression in halophyte Suaeda salsa under salt treatments. Microbiological Research, 245: 126688. Go to original source... Go to PubMed...
  19. Edwards S., Tadesse M., Demissew S., Hedberg I. (2000): Flora of Ethiopia and Eritrea, 2, The National Herbarium, Addis Ababa University, Department of Systematic Botany, Upps, 532.
  20. Flowers T.J., Colmer T.D. (2015): Plant salt tolerance: adaptations in halophytes. Annals of Botany, 115: 327-331. Go to original source... Go to PubMed...
  21. Gil R., Boscaiu M., Lull C., Bautista I., Lidón A., Vicente O. (2013): Are soluble carbohydrates ecologically relevant for salt tolerance in halophytes? Functional Plant Biology, 40: 805-818. Go to original source... Go to PubMed...
  22. Gliszczyńska-¦wigło A., Szymusiak H., Malinowska P. (2006): Betanin, the main pigment of red beet: molecular origin of its exceptionally high free radical-scavenging activity. Food Additives and Contaminants, 23: 1079-1087. Go to original source... Go to PubMed...
  23. Grieve C.M., Grattan S.R. (1983): Rapid assay for determination of water soluble quaternary ammonium compounds. Plant and Soil, 70: 303-307. Go to original source...
  24. Gul B., Hameed A., Ahmed M., Hussain T., Rasool S., Nielsen B. (2024): Thriving under salinity: growth, ecophysiology and proteomic insights into the tolerance mechanisms of obligate halophyte Suaeda fruticosa. Plants, 13: 1529. Go to original source... Go to PubMed...
  25. Guo J., Dong X., Han G., Wang B. (2019): Salt-enhanced reproductive development of Suaeda salsa L. coincided with ion transporter gene upregulation in flowers and increased pollen K+ content. Frontiers in Plant Science, 10: 1-17. Go to original source... Go to PubMed...
  26. Guo J., Du M., Lu C., Wang B. (2020): NaCl improves reproduction by enhancing starch accumulation in the ovules of the euhalophyte Suaeda salsa. BMC Plant Biology, 20: 1-16. Go to original source... Go to PubMed...
  27. Hameed A., Hussain T., Gulzar S., Aziz I., Gul B., Khan M.A. (2012): Salt tolerance of a cash crop halophyte Suaeda fruticosa: biochemical responses to salt and exogenous chemical treatments. Acta Physiologiae Plantarum, 34: 2331-2340. Go to original source...
  28. Hansen J., Møller I. (1975): Percolation of starch and soluble carbohydrates from plant tissue for quantitative determination with anthrone. Analytical Biochemistry, 68: 87-94. Go to original source... Go to PubMed...
  29. Hayakawa K., Agarie S. (2010): Physiological roles of betacyanin in a halophyte, Suaeda japonica Makino. Plant Production Science, 13: 351-359. Go to original source...
  30. Huang Z., Zhao L., Chen D., Liang M., Liu Z., Shao H., Long X. (2013): Salt stress encourages proline accumulation by regulating proline biosynthesis and degradation in Jerusalem artichoke plantlets. Plos One, 8: e62085. Go to original source... Go to PubMed...
  31. Hussain T., Khan M. (2022): Empirical values of halophytes in agro-ecology and sustainability. Earth Systems Protection and Sustainability, 1: 57-78. Go to original source...
  32. Hussain T., Li J., Feng X., Asrar H., Gul B., Liu X. (2021): Salinity induced alterations in photosynthetic and oxidative regulation are ameliorated as a function of salt secretion. Journal of Plant Research, 134: 779-796. Go to original source... Go to PubMed...
  33. Ibraheem F., Al-Zahrani A., Mosa A. (2022): Physiological adaptation of three wild halophytic Suaeda species: salt tolerance strategies and metal accumulation capacity. Plants, 11: 537. Go to original source... Go to PubMed...
  34. Jain G., Gould K.S. (2015): Functional significance of betalain biosynthesis in leaves of Disphyma australe under salinity stress. Environmental and Experimental Botany, 109: 131-140. Go to original source...
  35. Joshi A., Rajput V.D., Verma K.K., Minkina T., Ghazaryan K., Arora J. (2023): Potential of Suaeda nudiflora and Suaeda fruticosa to adapt to high salinity conditions. Horticulturae, 9: 1-18. Go to original source...
  36. Kumar A., Mann A., Kumar A., Kumar N., Meena B.L. (2021): Physiological response of diverse halophytes to high salinity through ionic accumulation and ROS scavenging. International Journal of Phytoremediation, 23: 1041-1051. Go to original source... Go to PubMed...
  37. Li H., Wang H., Wen W., Yang G. (2020): The antioxidant system in Suaeda salsa under salt stress. Plant Signaling and Behavior, 15: 1771939. Go to original source...
  38. Li J., Wang Y., Bao J., Ding Z., Yisilam G., Chu Z., Su Y., Wang Q., Tian X. (2023): Morphological and physiological responses of Suaeda salsa under drought and salt stress. Research Square. doi.org/10.21203/rs.3.rs-3255941/v1 Go to original source...
  39. Li Q., Liu R., Li Z., Fan H., Song J. (2022): Positive effects of NaCl on the photoreaction and carbon assimilation efficiency in Suaeda salsa. Plant Physiology and Biochemistry, 177: 32-37. Go to original source... Go to PubMed...
  40. Li Q., Song J. (2019): Analysis of widely targeted metabolites of the euhalophyte Suaeda salsa under saline conditions provides new insights into salt tolerance and nutritional value in halophytic species. BMC Plant Biology, 19: 1-11. Go to original source... Go to PubMed...
  41. Lichtenthaler H.K., Wellburn A.R. (1983): Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochemical Society Transactions, 11: 591-592. Go to original source...
  42. López-Pérez L., Martínez-Ballesta M. del C., Maurel C., Carvajal M. (2009): Changes in plasma membrane lipids, aquaporins and proton pump of broccoli roots, as an adaptation mechanism to salinity. Phytochemistry, 70: 492-500. Go to original source... Go to PubMed...
  43. Megdiche W., Amor N. Ben, 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 Physiologiae Plantarum, 29: 375-384. Go to original source...
  44. Mohammadi H., Kardan J. (2016): Morphological and physiological responses of some halophytes to salinity stress. Annales Universitatis Mariae Curie-Sklodowska, Sectio C - Biologia, 70: 31. Go to original source...
  45. Mujeeb A., Aziz I., Ahmed M.Z., Shafiq S., Fatima S., Alvi S.K. (2021): Spatial and seasonal metal variation, bioaccumulation and biomonitoring potential of halophytes from littoral zones of the Karachi Coast. Science of The Total Environment, 781: 146715. Go to original source...
  46. Murata N., Mohanty P.S., Hayashi H., Papageorgiou G.C. (1992): Glycine betaine stabilizes the association of extrinsic proteins with the photosynthetic oxygen-evolving complex. FEBS Letters, 296: 187-189. Go to original source... Go to PubMed...
  47. Ouyang S.Q., Liu Y.F., Liu P., Lei G., He S.J., Ma B., Zhang W.K., Zhang J.S., Chen S.Y. (2010): Receptor-like kinase OsSIK1 improves drought and salt stress tolerance in rice (Oryza sativa): plants. The Plant Journal, 62: 316-329. Go to original source... Go to PubMed...
  48. Panda A., Rangani J., Parida A.K. (2021): Unravelling salt responsive metabolites and metabolic pathways using non-targeted metabolomics approach and elucidation of salt tolerance mechanisms in the xero-halophyte Haloxylon salicornicum. Plant Physiology and Biochemistry, 158: 284-296. Go to original source... Go to PubMed...
  49. Park J., Okita T.W., Edwards G.E. (2009): Salt tolerant mechanisms in single-cell C4 species Bienertia sinuspersici and Suaeda aralocaspica Chenopodiaceae. Plant Science, 176: 616-626. Go to original source...
  50. Patel M.K., Mishra A., Jha B. (2016): Untargeted metabolomics of halophytes. In: Kim S.-K. (ed.): Marine Omics. Boca Raton, CRC Press, 307-325. ISBN: 9781315372303 Go to original source...
  51. Pirasteh-Anosheh H., Samadi M., Kazemeini S.A., Ozturk M., Ludwiczak A., Piernik A. (2023): ROS homeostasis and antioxidants in the halophytic plants and seeds. Plants, 12: 3023. Go to original source... Go to PubMed...
  52. Podar D., Macalik K., Réti K.O., Martonos I., Török E., Carpa R., Weindorf D.C., Csiszár J., Székely G. (2019): Morphological, physiological and biochemical aspects of salt tolerance of halophyte Petrosimonia triandra grown in natural habitat. Physiology and Molecular Biology of Plants, 25: 1335-1347. Go to original source... Go to PubMed...
  53. Pungin A., Lartseva L., Loskutnikova V., Shakhov V., Popova E., Skrypnik L., Krol O. (2023): Effect of salinity stress on phenolic compounds and antioxidant activity in halophytes Spergularia marina (L.): Griseb. and Glaux maritima L. cultured in vitro. Plants, 12: 1905. Go to original source...
  54. Qu Y., Wang J., Qu C., Mo X., Zhang X. (2024): Genome-wide identification of WRKY in Suaeda australis against salt stress. Forests, 15: 1297. Go to original source...
  55. Raymond J., Rakariyatham N., Azanza J. (1993): Purification and some properties of polyphenoloxidase from sunflower seeds. Phytochemistry, 34: 927-931. Go to original source...
  56. Sadasivam S. (1996): Biochemical Methods. New Delhi, New Age International Publishers.
  57. Shabala S., Mackay A. (2011): Ion transport in halophytes. Advances in Botanical Research, 57: 151-199. Go to original source...
  58. Sinha A.K. (1972): Colorimetric assay of catalase. Analytical Biochemistry, 47: 389-394. Go to original source... Go to PubMed...
  59. Skalicky M., Kubes J., Shokoofeh H., Tahjib-Ul-Arif M., Vachova P., Hejnak V. (2020): Betacyanins and betaxanthins in cultivated varieties of Beta vulgaris L. compared to weed beets. Molecules, 25: 1-15. Go to original source... Go to PubMed...
  60. Sogoni A., Jimoh M.O., Kambizi L., Laubscher C.P. (2021): The impact of salt stress on plant growth, mineral composition, and antioxidant activity in Tetragonia decumbens Mill.: an underutilized edible halophyte in South Africa. Horticulturae, 7: 140. Go to original source...
  61. Souid A., Gabriele M., Longo V., Pucci L., Bellani L., Smaoui A., Abdelly C., Ben Hamed K. (2016): Salt tolerance of the halophyte Limonium delicatulum is more associated with antioxidant enzyme activities than phenolic compounds. Functional Plant Biology, 43: 607-619. Go to original source... Go to PubMed...
  62. Thulin M., Beier B.A., Razafimandimbison S.G., Banks H.I. (2008): Ambilobea, a new genus from Madagascar, the position of aucoumea, and comments on the tribal classification of the frankincense and myrrh family (Burseraceae). Nordic Journal of Botany, 26: 218-229. Go to original source...
  63. Tian F., Hou M., Qiu Y., Zhang T., Yuan Y. (2020): Salinity stress effects on transpiration and plant growth under different salinity soil levels based on thermal infrared remote (TIR): technique. Geoderma, 357: 113961. Go to original source...
  64. Wang C.Q., Chen M., Wang B.S. (2007): Betacyanin accumulation in the leaves of C3 halophyte Suaeda salsa L. is induced by watering roots with H2O2. Plant Science, 172: 1-7. Go to original source...
  65. Wang N., Zhao Z., Zhang X., Liu S., Zhang K., Hu M. (2023): Plant growth, salt removal capacity, and forage nutritive value of the annual euhalophyte Suaeda salsa irrigated with saline water. Frontiers in Plant Science, 13: 1-13. Go to original source... Go to PubMed...
  66. Wang Y., Nii N. (2000): Changes in chlorophyll, ribulose bisphosphate carboxylase-oxygenase, glycine betaine content, photosynthesis and transpiration in Amaranthus tricolor leaves during salt stress. The Journal of Horticultural Science and Biotechnology, 75: 623-627. Go to original source...
  67. Wu H.F., Liu X.L., You L.P., Zhang L.B., Zhou D., Feng J.H., Zhao J., Yu J.B. (2012): Effects of salinity on metabolic profiles, gene expressions, and antioxidant enzymes in halophyte Suaeda salsa. Journal of Plant Growth Regulation, 31: 332-341. Go to original source...
  68. Wungrampha S., Rawat N., Lata Singla-Pareek S., Pareek A. (2020): Survival strategies in halophytes: adaptation and regulation. In: Grigore M.-N. (ed.): Handbook of Halophytes. From Molecules to Ecosystems towards Biosaline Agriculture. Cham, Springer International Publishing, 1-22. Go to original source...
  69. Yamaguchi T., Hamamoto S., Uozumi N. (2013): Sodium transport system in plant cells. Frontiers in Plant Science, 4: 65912. Go to original source... Go to PubMed...
  70. Zahran H.A., Tawfeuk H.Z. (2019): Physicochemical properties of new peanut (Arachis hypogaea L.) varieties. OCL, 26: 19. Go to original source...
  71. Zang W., Miao R., Zhang Y., Yuan Y., Pang Q., Zhou Z. (2021): Metabolic and molecular basis for the salt and alkali responses of Suaeda corniculata. Environmental and Experimental Botany, 192: 104643. Go to original source...
  72. Zhang J.L., Bai R., Flowers T.J., Wang C.M., Wetson A.M., Duan H.R., He A.L., Gurmani A.R., Wang S.M. (2021): Dynamic responses of the halophyte Suaeda maritima to various levels of external NaCl concentration. In: Grigore M.-N. (ed.): Handbook of Halophytes. From Molecules to Ecosystems towards Biosaline Agriculture. Cham, Springer International Publishing, 1637-1657. Go to original source...
  73. Zhao L., Yang Z., Guo Q., Mao S., Li S., Sun F., Wang H., Yang C. (2017): Transcriptomic profiling and physiological responses of halophyte Kochia sieversiana provide insights into salt tolerance. Frontiers in Plant Science, 8: 1-13. Go to original source... Go to PubMed...

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