Abdul HAMEED, Muhameed Zaheer AHMED, Bilquees GUL, Sarwat Ghulam RASOOL

Altered water relations, selective nutrient uptake, and reduced Na+ flux make Halopeplis perfoliata an obligate halophyte

Halopeplis perfoliata, a succulent halophyte of coastal marshy habitats, was grown in a greenhouse to study its adaptive responses in terms of growth, osmoregulation, and N-metabolism following one-month exposure to salinity (0, 150, 300, and 600 mmol $L^{–1}$ NaCl). Biomass was optimal in 150 mmol $L^{–1}$ NaCl with unaltered malondialdehyde (MDA) levels. On the other hand, biomass remained comparable to non-saline control with some increase in MDA in 300 and 600 mmol $L^{–1}$ NaCl. Osmotic potential $(ψ_S)$ was maintained up to 300 mmol $L^{–1}$ NaCl that correlated with an increase in succulence (SC) and lower water deficit (WD), whereas sap $ψ_S$ was lowest in 600 mmol $L^{–1}$ NaCl along with lower SC and high WD. Sodium level gradually increased in shoot and was higher than the root. Potassium deficiency was not observed up to high salinity. Both soluble sugars and nitrogen isotope $(δ^{15}N)$ increased transiently in 300 mmol $L^{–1}$ NaCl. Hence, modulations in water relation, selective nutrient uptake, and controlled $Na^{+}$ flux appear important for salinity tolerance of H. perfoliata.

PDF

___

Ahmed HAI, Shabala L, Shabala S (2021). Understanding the mechanistic basis of adaptation of perennial Sarcocornia quinqueflora species to soil salinity. Physiologia Plantarum 172 (4):1997-2010. doi.org/10.1111/ppl.13413
Ahmed MZ, Shimazaki T, Gulzar S, Kikuchi A, Gul B et al. (2013). The influence of genes regulating transmembrane transport of Na+ on the salt resistance of Aeluropus lagopoides. Functional Plant Biology 40 (9):860-871. doi: 10.1071/FP12346
Alfarhan AH, Al-Turki TA, Basahy AY (2005). Flora of Jizan region. Final Report Supported by King Abdulaziz City for Science and Technology 1 545.
Almeida DM, Oliveira MM, Saibo NJ (2017). Regulation of Na+ and K+ homeostasis in plants: towards improved salt stress tolerance in crop plants. Genetics and Molecular Biology 40 (suppl), 326-345. doi:10.1590/1678-4685-GMB-2016-0106
Al-Saleh GFS, Gamal el-din AY, Abbas JA, Saeed NA (1997). Phytochemical and biological studies of medicinal plants in Bahrain: the family Chenopodiaceae Part 2. International Journal of Pharmacognosy 35 (1):38-42. doi:10.1076/ phbi.35.1. 38.13266
Al-Zahrani HS, Hajar AS, 1998. Salt tolerance in the halophyte Halopeplis perfoliata (Forssk.) Bge. ex. Schweint: Effect of NaCl salinity on growth and ion uptake. Indian Journal of Plant Physiology 2 (2):135–137.
Araus JL, Rezzouk FZ, Thushar S, Shahid M, Elouafi IA et al. (2021). Effect of irrigation salinity and ecotype on the growth, physiological indicators and seed yield and quality of Salicornia europaea. Plant Science 304 110819. doi:10.1016/ j.plantsci.2021.110819
Benito B, Haro R, Amtmann A, Cuin TA, Dreyer I (2014). The twins K+ and Na+ in plants. Journal of Plant Physiology 171 (9):723- 731. doi:10.1016/j.jplph. 2013.10.014
Camacho-Sanchez M, Barcia-Piedras JM, Redondo-Gómez S, Camacho M (2020). Mediterranean seasonality and the halophyte Arthrocnemum macrostachyum determine the bacterial community in salt marsh soils in Southwest Spain. Applied Soil Ecology 151 103532. doi:10.1016/j. apsoil.2020.103532
Chen J, Li LG, Liu ZH, Yuan YJ, Guo LL et al. (2009). Magnesium transporter AtMGT9 is essential for pollen development in Arabidopsis. Cell Research 19 887-898. Doi:10.1038/cr.2009.58
Colmer TD, Vos H, Pedersen O (2009). Tolerance of combined submergence and salinity in the halophytic stem-succulent Tecticornia pergranulata. Annals of Botany 103 (2):303-312. doi:10.1093/aob/mcn120
Cui J, Lamade E, Fourel F, Tcherkez G (2020). δ15N values in plants are determined by both nitrate assimilation and circulation. New Phytologist 226 (6):1696–1707. doi:10.1111/nph.16480
Ehleringer JR, Osmond CB (1989). Stable isotopes. In: Pearcy RW, Ehleringer JR, Mooney HA, Rundel PW (editors) Plant Physiological Ecology Field Methods and Instrumentations. New York: Chapman and Hall, pp. 281-300. doi:10.1007 /978- 94-010-9013–1_13
Elnaggar A, Mosa KA, El-Keblawy A, Tammam A, El-Naggar M (2020). Physiological and biochemical insights of salt stress tolerance in the habitat-indifferent halophyte Salsola drummondii during the vegetative stage. Botany. 98 (11):673- 689. doi: 10.1139 /cjb-2019-0160
English JP, Colmer TD (2013). Tolerance of extreme salinity in two stem-succulent halophytes (Tecticornia species). Functional Plant Biology 40 (9):897-912. doi:10.1071/FP12304
Epstein E (1972). Mineral nutrition in plants principles and perspectives. In: Physiological Genetics of Plant Nutrition. New York: John Wiley and Sons, pp. 325-344.
Flowers TJ, Colmer TD (2008). Salinity tolerance in halophytes. New Phytologist 179 (4):945-963. doi:10.1111/j.1469- 8137.2008.02531.x
Flowers TJ, Colmer TD (2015). Plant salt tolerance: adaptations in halophytes. Annals of Botany 115 (3):327-331. doi:10.1093/ aob/mcu267
Flowers TJ, Edward P, Volkov GV (2019). Could vesicular transport of Na+ and Cl- be a feature of salt tolerance in halophytes? Annals of Botany 123 (1):1–18. doi:10.1093/aob/mcy164
Gul B, Ansari R, Khan MA (2009). Salt tolerance of Salicornia utahensis from the great basin desert. Pakistan Journal of Botany 4 (6):2925-2932.
Gul B, Khan MA (2006). Role of calcium in alleviating salinity effects in coastal halophytes. In: Khan MA, Weber DJ (editors) Ecophysiology of high salinity tolerant plants. Netherlands: Springer, pp. 107–114. doi: 10.1007/1-4020-4018-0_6
Guo R, Shi L, Yan C, Zhong X, Gu F, et al. (2017). Ionomic and metabolic responses to neutral salt or alkaline salt stresses in maize (Zea mays L.) seedlings. BMC Plant Biology 17 (14):1– 13. doi:10.1186/s12870-017-0994-6
Hameed A, Ahmed MZ, Gulzar S, Gul B, Alam J et al. (2013). Seed germination and recovery responses of Suaeda heterophylla to abiotic stresses. Pakistan Journal of Botany 45 (5):1649–1656.
Hameed A, Hussain T, Gulzar S, Aziz I, Gul B, Khan MA et al. (2012). Salt tolerance of a cash crop halophyte Suaeda fruticosa: biochemical responses to salt and exogenous chemical treatments. Acta Physiologiae Plantarum 34 2331-2340. doi: 10.1007/s11738-012–1035-6.
Heath RL, Packer L (1968). Photo-peroxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics 125 (1):189–198. doi: 10.1016/0003-9861(68)90654–1
Hedge IC (1997). Halopeplis. In: Rechinger KH (editor) Flora Iranica: Chenopodiaceae. Akad: Druck, Graz, p. 123–125.
Hedrich R, Kurkdjian A, Guern J, Flügge UI (1989). Comparative studies on the electrical properties of the H+ translocating ATPase and pyrophosphatase of the vacuolar-lysosomal compartment. The EMBO Journal 8 (10):2835-2841.
Hussin S, Geissler N, Koyro HW (2013). Effect of NaCl salinity on Atriplex nummularia (L.) with special emphasis on carbon and nitrogen metabolism. Acta Physiologiae Plantarum 35 (4):1025–1038. doi: 10.1007/s11738-012–1141-5
Jacob PT, Siddiqui SA, Rathore MS (2020). Seed germination, seedling growth and seedling development associated physiochemical changes in Salicornia brachiata (Roxb.) under salinity and osmotic stress. Aquatic Botany 166 103272. doi: 10.1016/j.aquabot.2020.103272
Ji H, Pardo JM, Batelli G, Van-Oosten MJ, Bressan RA et al. (2013). The salt overly sensitive (SOS) pathway: established and emerging roles. Molecular Plant. 6 (2):275-286. doi:10.1093/ mp/sst017
Katschnig D, Broekman R, Rozema J (2013). Salt tolerance in the halophyte Salicornia dolichostachya Moss: growth, morphology and physiology. Environmental and Experimental Botany 92 32-42. doi: 10.1016/j.envexpbot.2012.04.002
Köster AK, Wood CA, Thomas-Tran R, Chavan TS, Almqvist J et al. (2018). A selective class of inhibitors for the CLC-Ka chloride ion channel. Proceedings of the National Academy of the Sciences 115 (21): E4900-E4909. doi: 10.1073/pnas.1720584115
Kramer PJ, Boyer JS (1995). Water relations of plants and soils. San Diego, California, USA: Academic press.
Lima AR, Castañeda-Loaizab V, Salazarc M, Nunesc C, Quintasa C et al. (2020). Influence of cultivation salinity in the nutritional composition, antioxidant capacity and microbial quality of Salicornia ramosissima commercially produced in soilless systems. Food Chemistry 333 127525. doi: 10.1016/j. foodchem.2020.127525
Marco P, Carvajal M, Martínez-Ballesta MC (2019). Efficient leaf solute partitioning in Salicornia fruticosa allows growth under salinity. Environmental and Experimental Botany 157 177– 186. doi: 10.1016/j.envexpbot.2018.10.001
Marschner H (1995). Mineral nutrition of higher plants. London: Academic Press, p. 889. doi:10.1016/B978-0–12-473542-2. X5000-7
McNulty IB (1985). Rapid osmotic adjustment by a succulent halophyte to saline shock. Plant Physiology 78 (1): 100–103. doi: 10.1104/pp.78.1.100
Moghaieb RE, Saneoka H, Fujita K (2004). Effect of salinity on osmotic adjustment, glycinebetaine accumulation and the betaine aldehyde dehydrogenase gene expression in two halophytic plants, Salicornia europaea and Suaeda maritima. Plant Science 166 (5):1345–1349. doi: 10.1016/j.plantsci.2004.01.016
Munns R (2011). Plant adaptations to salt and water stress: differences and commonalities. Advances in Botanical Research 57 1-32. doi: 10.1016/B978-0–12-387692-8.00001–1
Munns R, Tester M (2008). Mechanisms of salinity tolerance. Annual Review of Plant Biology 59 651-681. doi:10.1146/annurev. arplant.59.032607.092911
Ning J, Ai S, Yang S, Cui L, Chen Y et al. (2015). Physiological and antioxidant responses of Basella alba to NaCl or $Na_2SO_4$ stress.
Acta Physiologiae Plantarum 37 (7):126. doi: 10.1007/s11738- 015–1860-5
Osman MS, Badawy AA, Osman AI, Abdel-Latef AAH (2020). Ameliorative impact of an extract of the halophyte Arthrocnemum macrostachyum on growth and biochemical parameters of Soybean under salinity stress. Journal of Plant Growth Regulation 40 1245–1256. doi:10.1007/s00344-020– 10185-2
Öztürk M, Altay V, Güvensen A (2019). Sustainable use of halophytic taxa as food and fodder: an important genetic resource in Southwest Asia. In: Hasanuzzaman M, Nahar K, Öztürk MA (editors) Ecophysiology, Abiotic Stress Responses and Utilization of Halophytes. Singapore: Springer, pp. 235-257. doi:10.1007/978-981–13-3762-8_11
Pardo-Domènech LL, Tifrea A, Grigore MN, Boscaiu M, Vicente O (2016). Proline and glycine betaine accumulation in two succulent halophytes under natural and experimental conditions. Plant Biosystems 150 (5):904-915. doi:10.1080/ 11263504. 2014.990943
Pilcher NJ, Phillips RC, Aspinall S, Al-Madany I, King H et al. (2003). Hawar islands protected area (Kingdom of Bahrain). Management Plan. 1st draft. Doha: UNESCO, p. 30.
Plieth C (2005). Calcium: just another regulator in the machinery of life? Annals of Botany 96 (1):1-8. doi:10.1093/aob/mci144
Pujol JA, Calvo JF, Ramírez-Díaz L (2001). Seed germination, growth, and osmotic adjustment in response to NaCl in a rare succulent halophyte from southeastern Spain. Wetlands. 21 256-264. doi:10.1672/ 02775212 (2001)021
Rabhi M, Farhat N, Msilini N, Rajhi H, Smaoui A et al. (2018). Physiological responses of Carthamus tinctorius to CaCl2 salinity under Mg-sufficient and Mg-deficient conditions. Flora 246 96–101. doi:10.1016/j.flora.2018.07.008
Ramadan HZ, Bantan RA (2013). Hypersaline benthic foraminifera from the Shuaiba lagoon, eastern red sea, Saudi Arabia: Their environmental controls and usefulness in sea-level reconstruction. Marine Micropaleontology 103 51-67. doi:10.1016 /j.marmicro.2013.07.005
Rasool SG, Gulzar S, Hameed A, Edwards GE, Khan MA et al. (2019). Maintenance of photosynthesis and the antioxidant defence systems have key roles for survival of Halopeplis perfoliata (Amaranthaceae) in a saline environment. Plant Biology 21 (6):1167–1175. doi:10.1111/plb.13033
Redondo-Gómez S, Mateos-Naranjo E, Figueroa ME, Davy AJ (2010). Salt stimulation of growth and photosynthesis in an extreme halophyte, Arthrocnemum macrostachyum. Plant Biology 12 (1):79-87. doi:10.1111/j.1438-8677.2009
Rozema J, Schat H (2013). Salt tolerance of halophytes, research questions reviewed in the perspective of saline agriculture. Environmental and Experimental Botany 92 83-95. doi:10.1016/j.envexpbot.2012.08.004
Shabala SN, Mackay AS (2011). Ion transport in halophytes. Advances in Botanical Research 57 151–187. doi:10.1016/ B978-0–12-387692-8.00005-9
Shaul O (2002). Magnesium transport and function in plants: The tip of the iceberg. BioMetals 15 309-323. doi:10.1023/A:1016091118585
Short DC, Colmer TD (1999). Salt Tolerance in the halophyte Halosarcia pergranulata subsp. pergranulata. Annals of Botany 83 (3):207-213. doi:10.1006/anbo. 1998. 0812
Song J, Shi G, Xing S, Yin C, Fan H et al. (2009). Eco-physiological responses of the eu-halophyte Suaeda salsa to the interactive effects of salinity and nitrate availability. Aquatic Botany 91 (4):311-317. doi:10.1016/j.aquabot.2009.08.003
Spalding EP, Harper JF (2011). The ins and outs of cellular Ca++ transport. Current Opinion in Plant Biology 14 (6):715-720. doi:10.1016/j.pbi.2011.08.001
Swarbreck SM, Colaço R, Davies JM (2013). Plant calcium-permeable channels. Plant Physiology 163 (2):514-522. doi:10.1104/ pp.113.220855
Tran TKA, Islam R, Vand DL, Rahman MM, Yu RMK et al. (2020). Accumulation and partitioning of metals and metalloids in the halophytic saltmarsh grass, saltwater couch, Sporobolus virginicus. Science of the Total Environment 713 13657. doi:10.1016/j.scitotenv.2020.136576
Yasseen BT, Al-Thani RF (2007). Halophytes and associated properties of natural soils in the Doha area, Qatar. Aquatic Ecosystem Health and Management 10 (3):320-326. doi:10.1080/14634980701519462
Yemm EW, Willis AJ (1954). The estimation of carbohydrates in plant extracts by anthrone. Biochemical Journal 57 (3):508-514. doi:10.1042/bj0570508
Yohannes E, Hansson B, Lee RW, Waldenström J, Westerdahl H et al. (2008). Isotope signatures in winter moulted feathers predict malaria prevalence in a breeding avian host. Oecologia. 158 299-306. doi: 10.1007/s00442-008–1138-3
Yousfi S, Serret MD, M´arquez AJ, Voltas J, Araus JL (2012). Combined use of δ13C, δ18O and δ15N tracks nitrogen metabolism and genotypic adaptation of durum wheat to salinity and water deficit. New Phytologist 194 (1):230-244. doi:0.1111 /j.1469 813.2011.04036.x
Yue LJ, Li SX, Ma Q, Zhou XR, Wu GQ et al. (2012). NaCl stimulates growth and alleviates water stress in the xerophyte Zygophyllum xanthoxylum. Journal of Arid Environments 87 153–160. doi:10.1016/j.jaridenv.2012.06.002
Yun P, Shabala S (2020). Ion transport in salt glands and bladders in halophyte species. In: Grigore MN (editor). Handbook of Halophytes. Switzerland: Springer, pp. 1–19.
Zia S, Egan TP, Khan MA (2008). Growth and selective ion transport of Limonium stocksii Plumbaginacea under saline conditions. Pakistan Journal of Botany 40 (2):697-709.
Zreik R (1990). The domestication and economic cultivation of halophytes. In: Developing World Agriculture. London: Grosvenor press, pp. 74-79.