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Choline priming-induced plasma membrane lipid alterations contributed to improved wheat salt tolerance

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Abstract

Salt stress is a major environmental threat influencing crop growth and yield. The plasma membrane (PM) is believed to be one facet of the cellular mechanisms of salt adaptation. Choline priming has been reported to enhance salt tolerance of the sensitive wheat cultivar used in this work. The study was, therefore, undertaken to examine whether changes in the PM lipids will participate in choline-improved salt tolerance. The caryopses were primed in choline chloride (0, 5 and 10 mM) for 24 h. They were then germinated in sand for 10 days, watered with 1/4-strength modified Hoagland solution (MHS). The seedlings were grown in the sand, watered with MHS containing 150 mM NaCl for 3 weeks. Root PM was isolated by two-phase partitioning method and its lipid classes were determined. Choline maintained the PM total lipids, sterol and phospholipids, which were altered by NaCl. The PM sterols/phospholipids ratio was decreased by NaCl, whereas choline retained this ratio. Salt stress reduced the PM unsaturated fatty acids while increased its saturated fatty acids. Choline alleviated PM unsaturated/saturated ratio reduction. NaCl declined the PM phosphatidylcholine (PC), phosphatidylglycerol (PG) and diphosphatidylglycerol (DPG) whereas increased phosphatidylserine (PS), phosphatidylinositol (PI) and phosphatidylethanolamine (PE). Choline decreased PS and PE, while increased PC level. The PM cholesterol, campesterol and β-sitosterol were increased while stigmasterol was declined under NaCl. Choline increased stigmasterol whereas decreased cholesterol and campesterol. The alterations in the PM lipids were discussed in relation to choline-enhanced salt tolerance.

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References

  • Alvarez-Pizarro JC, Gomes-Filho E, de Lacerda CF, Alencar NLM, Prisco JT (2009) Salt-induced changes on H+-ATPase activity, sterol and phospholipid content and lipid peroxidation of root plasma membrane from dwarf-cashew activity and lipid composition of plasma membrane vesicles isolated from roots (Anacardium occidentale L.) seedlings. Plant Growth Regul 59:125–135

    Article  CAS  Google Scholar 

  • Ames BN (1966) Assay of inorganic phosphate, total phosphate and phosphatases. Methods Enzymol 8:115–118

    Article  CAS  Google Scholar 

  • Ashraf M, Foolad MR (2005) Pre-sowing seed treatment—a shotgun approach to improve germination, plant growth, and crop yield under saline and non-saline conditions. Adv Agron 88:825–831

    Google Scholar 

  • Bybordi A (2011) Effects of NaCl salinity levels on lipids and proteins of canola (Brassica napus L.) cultivars. Roman Agri Res 28:197–206

    Google Scholar 

  • Cramer RC, Laughlin A, Polite S (1985) Displacement of Ca2+ by Na+ from the plasmalemma of root cells. A primary response to salt stress? Plant Physiol 79:207–211

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Deinstrop EH, Weinheim WV (2000) Applied thin layer chromatography. Scottish Crop Research Institute, Scotland

    Google Scholar 

  • Douglas TJ (1985) NaCl effects on sterol composition of plasma membrane-enriched preparation from citrus root plants. Plant Cell Environ 8:687–692

    Article  CAS  Google Scholar 

  • Douglas TJ, Sykes SR (1985) Phospholipid, galactolipid and free sterol composition of fibrous roots from citrus genotypes differing in chloride exclusion ability. Plant Cell Environ 8:693–699

    CAS  Google Scholar 

  • Douglas TJ, Walker RR (1983) 4-Desmethylsterol composition of citrus root-stocks of different salt exclusion capacity. Physiol Plant 58:69–74

    Article  CAS  Google Scholar 

  • Epstein E (1972) Mineral nutrition of plants: principles and perspectives. Wiley, New York

    Google Scholar 

  • Flowers TJ, Flowers SA (2005) Why does salinity pose such a difficult problem for plant breeders. Agri Water Manag 78:15–24

    Article  Google Scholar 

  • Grandmougin-Ferjani A, Schuler-Muller I, Hartmann M (1997) Sterol modulation of the plasma membrane H+-ATPase activity from corn roots reconstituted into soybean lipids. Plant Physiol 113:163–174

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hajlaoui H, Denden M, Elyeb N (2009) Changes in fatty acids composition, hydrogen peroxide generation and lipid peroxidation of salt-stressed corn (Zea mays L.) root. Acta Physiol Plant 31:33–39

    Article  Google Scholar 

  • Hasanuzzaman M, Nahar K, Fujita M (2013) Plant response to salt stress and role of exogenous protectants to mitigate salt-induced damages. In: Ahmad P, Azooz MM, Prasad MNV (eds) Ecophysiology and responses of plants under salt stress. Springer, New York, pp 25–87

    Chapter  Google Scholar 

  • Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Ann Rev Plant Physiol Plant Mol Biol 51:463–499

    Article  CAS  Google Scholar 

  • Huang B (2006) Cellular mechanisms in stress sensing and regulation of plant adaptation to abiotic stress. In: Huang B (ed) Plant–environment interactions. CRC Press, Taylor and Francis, Boca Raton, pp 1–25

    Google Scholar 

  • Kates M (1972) Techniques of lipidology. Isolation, analysis and identification of lipids. In: Work TS, Work E (eds) Laboratory techniques in biochemistry and molecular biology. North Holland Publishing, Amsterdam, pp 347–390

    Google Scholar 

  • Kerkeb L, Donaire JP, Rodriguez-Rosales MP (2001) Plasma membrane H+-ATPase activity is involved in adaptation of tomato to NaCl. Physiol Plant 111:483–490

    Article  CAS  PubMed  Google Scholar 

  • Kreslavski VD, Balakhnina TI, Khristin MS, Bukhov NG (2001) Pre-treatment of bean seedlings with choline compounds increases the resistance of photosynthetic apparatus to UV-B radiation and elevated temperatures. Photosynth 39:353–358

    Article  Google Scholar 

  • Kuiper PJC (1984) Functioning of plant cell membranes under saline conditions: membrane lipid composition and ATPases. In: Staples RC, Toenniessen GH (eds) Salinity tolerance in plants. Wiley, New York, pp 77–91

    Google Scholar 

  • Kumari P, Kumar M, Reddy CRK, Jha B (2013) Algal lipids, fatty acids and sterols. In: Dominguez H (ed) Functional ingredients from algae for foods and nutraceuticals. Woodhead Publishing, Cambridge, pp 87–134

    Chapter  Google Scholar 

  • Lauchli A (1990) Calcium, salinity and the plasma membrane. In: Leonard RT, Hepler PK (eds) Calcium in plan growth and development. Am Soc Plant Physiol, Rockville, pp 26–35

    Google Scholar 

  • Liang Y, Zhang W, Chen Q, Liu Y, Ding R (2006) Effect of exogenous silicon (Si) on H+-ATPase activity, phospholipids and fluidity of plasma membrane in leaves of salt-stressed barley (Hordeum vulgare L.). Environ Exp Bot 57:212–219

    Article  CAS  Google Scholar 

  • López-Perez L, Martinez-Ballesta M, 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

    Article  PubMed  Google Scholar 

  • Lu N, Weia D, Jianga X, Chen F, Yang S (2012) Regulation of lipid metabolism in the snow alga Chlamydomonas nivalis in response to NaCl stress: an integrated analysis by cytomic and lipidomic approaches. Proc Biochem 47:1163–1170

    Article  CAS  Google Scholar 

  • Mansour MMF (2000) Nitrogen containing compounds and adaptation of plants to salinity stress. Biol Plant 43:491–500

    Article  CAS  Google Scholar 

  • Mansour MMF (2013) Plasma membrane permeability as an indicator of salt tolerance in plants. Biol Plant 57:1–10

    Article  CAS  Google Scholar 

  • Mansour MMF (2014) Plasma membrane transport systems and adaptation to salinity. J Plant Physiol 171:1787–1800

    Article  CAS  PubMed  Google Scholar 

  • Mansour MMF, Salama KHA (2004) Cellular basis of salinity tolerance in plants. Environ Exp Bot 52:113–122

    Article  CAS  Google Scholar 

  • Mansour MMF, Stadelmann EJ, Lee-Stadelmann OY (1993) Salt acclimation of Triticum aestivum by choline chloride: plant growth, mineral content, and cell permeability. Plant Physiol Biochem 31:341–348

    CAS  Google Scholar 

  • Mansour MMF, Van Hasselt PR, Kuiper PJC (1994) Plasma membrane lipid alterations by NaCl in winter wheat roots. Physiol Plant 92:473–476

    Article  CAS  Google Scholar 

  • Mansour MMF, Salama KHA, Al-Mutawa MM, Abou Hadid AF (2002) Effect of NaCl and polyamines on plasma membrane lipids of wheat roots. Biol Plant 45:235–239

    Article  CAS  Google Scholar 

  • Mansour MMF, Salama KHA, Ali FZM, Abou Hadid AF (2005) Cell and plant responses to NaCl in (Zea mays L.) cultivars differing in salt tolerance. Gen Appl Plant Physiol 31:29–41

    CAS  Google Scholar 

  • Mansour MMF, Salama KHA, Allam HYH (2015) Role of the plasma membrane in saline conditions: lipids and proteins. Bot Rev. doi:10.1007/s12229-015-9156-4

    Google Scholar 

  • March JB, Weinstein DB (1966) Simple charring method for determination of lipids. J Lipid Res 7:574–576

    Google Scholar 

  • Morales-Cedillo F, Gonzalez-Solis A, Gutierrez-Angoa L, Cano-Ramirez DL, Gavilanes-Ruiz M (2015) Plant lipid environment and membrane enzymes: the case of the plasma membrane H+-ATPase. Plant Cell Rep. doi:10.1007/s00299-014-1735-z

    PubMed  Google Scholar 

  • Munnik T, Testerink C (2009) Plant phospholipid signaling: ‘in a nutshell’. J Lipid Res 50:260–265

    Article  Google Scholar 

  • Munns R, Tester M (2008) Mechanism of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  CAS  PubMed  Google Scholar 

  • Racagni G, Pedranzani AS, Taleisnik E, Abdala G (2003) Effect of short-term salinity on lipid metabolism and ion accumulation in tomato roots. Biol Plant 47:373–377

    Article  CAS  Google Scholar 

  • Ros R, Cooke D, James R (1990) Effect of herbicide MCPA and the heavy metals, cadmium and nickel on the lipid composition, Mg2+-ATPase activity and fluidity of plasma membranes from rice, Oryza sativa (cv. Bahia) shoots. J Exp Bot 41:457–462

    Article  CAS  Google Scholar 

  • Russell NJ (1989) Function of lipids: Structural roles and membrane function. In: Ratledge C, Wilkinson SC (eds) Microbial lipids. Academic Press, London, pp 279–365

    Google Scholar 

  • Salama KHA, Mansour MMF, Ali FZM, Abou Hadid AF (2007) NaCl-induced changes in plasma membrane lipids and proteins of Zea mays L. cultivars differing in their response to salinity. Acta Physiol Plant 29:351–359

    Article  CAS  Google Scholar 

  • Salama KHA, Mansour MMF, Hassan NS (2011) Choline priming improves salt tolerance in wheat (Triticum aestivum L.). Aust J Basic Appl Sci 5:126–132

    CAS  Google Scholar 

  • Senaratna T, McKersie BD, Stinon RH (1984) Association between membrane phase properties and dehydration injury in soybean axes. Plant Physiol 76:759–762

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sheng RY, Li PM, Xue GX, Gao HY (2006) Choline chloride protects cell membrane and the photosynthetic apparatus in cucumber seedling leaves at low temperature and weak light. PubMed 32:87–93

    CAS  Google Scholar 

  • Su J, Hirji R, Zhang L, He C, Selvaraj G, Wu R (2006) Evaluation of the stress-inducible production of choline oxidase in transgenic rice as a strategy for producing the stress-protectant glycine betaine. J Exp Bot 57:1129–1135

    Article  CAS  PubMed  Google Scholar 

  • The National Academies (1998) Choline. Dietary reference intakes for thiamin, riboflavin, niacin, vitamin B6, folate, vitamin B12, pantothenic acid and choline. National Academy Press, Washington, pp 390–422

    Google Scholar 

  • Upchurch RG (2008) Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress. Biotechnol Lett 30:967–977

    Article  CAS  PubMed  Google Scholar 

  • Wu J, Seliskar DM, Gallagher JL (2005) The response of plasma membrane lipid composition in callus of the halophyte, Spartina patens, to salinity stress. Amer J Bot 92:852–858

    Article  CAS  Google Scholar 

  • Zamani S, Bybordi A, Khorshidi MB, Nezami T (2010) Effect of NaCl salinity levels on lipids and proteins of Canola (Brassica napus L.) cultivars. Adv Environ Biol 4:397–403

    CAS  Google Scholar 

  • Zlatkis A, Zak B (1969) Study of new cholesterol reagent. Anal Biochem 29:143–148

    Article  CAS  PubMed  Google Scholar 

Download references

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Authors and Affiliations

  1. Department of Biology, Faculty of Science, Taif University, Taif, 21944, Saudi Arabia

    Mohamed Magdy F. Mansour

  2. Department of Botany, Faculty of Science, Ain Shams University, Cairo, 11566, Egypt

    Karima H. A. Salama & Mohamed Magdy F. Mansour

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  1. Karima H. A. Salama
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  2. Mohamed Magdy F. Mansour
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Correspondence to Mohamed Magdy F. Mansour.

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Communicated by K. Apostol.

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Salama, K.H.A., Mansour, M.M.F. Choline priming-induced plasma membrane lipid alterations contributed to improved wheat salt tolerance. Acta Physiol Plant 37, 170 (2015). https://doi.org/10.1007/s11738-015-1934-4

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  • DOI: https://doi.org/10.1007/s11738-015-1934-4

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