Theoretical and Experimental Plant Physiology

, Volume 30, Issue 4, pp 335–345 | Cite as

Exogenous application of gibberellic acid participates in up-regulation of lipid biosynthesis under salt stress in rice

  • Xiaoxiao Liu
  • Xinyue Wang
  • Lina YinEmail author
  • Xiping Deng
  • Shiwen Wang


Alterations in membrane lipid composition lead to improved plant salt tolerance. Gibberellic acid (GA3) has also been widely reported to reduce growth inhibition induced by increased salinity. However, little is known about whether exogenous application of GA3 participates in up-regulation of lipid biosynthesis under salt stress. In this study, one of the major lipid biosynthesis genes in rice (Oryza sativa L. cv. Nipponbare), monogalactosyldiacylglycerol synthase (OsMGD) was found to be significantly up-regulated by GA3 treatment. Lipid analysis showed that after salt disturbance, the concentrations of all the measured lipids, including monogalactosyldiacylglycerol (MGDG), digalactosyldiacylglycerol (DGDG) and phospholipid lipids + sulfoquinovosyl diacylglycerol (PL + SQDG) were decreased significantly. However, GA3 treatment prior to salt disturbance caused those lipids to remain at high levels, as well as preserving a high DGDG/MGDG ratio. The desaturation of DGDG (DBI) was also increased in GA3 pre-treatment plants as compared with no GA3 pre-treatment, primarily due to a decrease of 16:0 fatty acids and an increase of 18:3 fatty acids in DGDG. Plants pre-treated with GA3 prior to salt disturbance had higher dry weights than those without pre-treatment. The chlorophyll concentration was also higher in GA3 treated plants than in untreated plants under salt disturbance. Taken together, these results indicate that exogenous application of GA3 participates in up-regulation of chloroplast lipid biosynthesis under salt disturbance in rice.


Chloroplast membrane lipids Fatty acids Gibberellic acid Salt stress Rice 



Gibberellic acid


Monogalactosyldiacylglycerol synthase






Phospholipid lipids


Sulfoquinovosyl diacylglycerol


Double bond index




Abscisic acid


Methyl jasmonate


Thin Layer Chromatography


Fatty acyl methylester


Flame ionization detector


Light-harvesting chlorophyll complex II


Photosystem II



This work was supported by the “Youth Elite Project” and “Young Faculty Study Abroad Program” of Northwest A&F University, the Youth Innovation Promotion Association of the Chinese Academy of Sciences [No. 2015389], the West Light Foundation of the Chinese Academy of Sciences, and the Project of Youth Science and Technology New Star in Shaanxi Province [2016KJXX-66].

Author contributions

LY planned the experiments and prepared the manuscript. XL and XW conducted the experiments, collected and analyzed the data and prepared a draft of the manuscript. XD and SW helped in drafting the manuscript and interpreting the results.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

40626_2018_129_MOESM1_ESM.docx (30 kb)
Supplementary material 1 (DOCX 29 kb)


  1. Acharya UT (1983) Effect of GA3 on germination of paddy (Oryza sativa L. var. GR-3) under saline condition. Ph.D. thesis, The M S University of Baroda, BarodaGoogle Scholar
  2. Afzal I, Basra S, Iqbal A (2005) The effect of seed soaking with plant growth refulators on seedling vigor of wheat under salinity stress. J Stress Physiol Biochen 1:6–14Google Scholar
  3. Allakhverdiev SI, Sakamoto A, Nishiyama Y, Inaba M, Murata N (2000) Ionic and osmotic effects of NaCl-induced inactivation of photosystems I and II in Synechococcus sp. Plant Physiol 123:1047–1056CrossRefPubMedPubMedCentralGoogle Scholar
  4. Allakhverdiev SI, Kinoshita M, Inaba M, Suzuki I, Murata N (2001) Unsaturated fatty acids in membrane lipids protect the photosynthetic machinery against salt-induced damage in Synechococcus. Plant Physiol 125:1842–1853CrossRefPubMedPubMedCentralGoogle Scholar
  5. Andersson MX, Stridh MH, Larsson KE, Lijenberg C, Sandelius AS (2003) Phosphate-deficient oat replaces a major portion of the plasma membrane phospholipids with the galactolipid digalactosyldiacylglycerol. FEBS Lett 537:128–132CrossRefPubMedGoogle Scholar
  6. Ashraf M, Karim F, Rasul E (2000) Interactive effects of gibberellic acid (GA3) and salt stress on growth, ion accumulation and photosynthetic capacity of two spring wheat (Triticum aestivum L.) cultivars differing in salt tolerance. Plant Growth Regul 36:49–59CrossRefGoogle Scholar
  7. Awai K, Marechal E, Block MA, Brun D, Masuda T, Shimada H, Joyard J (2001) Two types of MGDG synthase genes, found widely in both 16:3 and 18:3 plants, differentially mediate galactolipid syntheses in photosynthetic and nonphotosynthetic tissues in Arabidopsis thaliana. P Natl Acad Sci USA 98:10960–10965CrossRefGoogle Scholar
  8. Bejaoui F, Salas JJ, Nouairi I, Smaoui A, Abdelly C, Martinez-Force E, Youssef NB (2016) Changes in chloroplast lipid contents and chloroplast ultrastructure in Sulla carnosa and Sulla coronaria leaves under salt stress. J Plant Physiol 198:32–38CrossRefPubMedGoogle Scholar
  9. Block MA, Dorne A-J, Joyard J, Douce R (1983) Preparation and characterization of membrane fractions enriched in outer and inner envelope membranes from Spinach chloroplast. J Biol Chem 258:13281–13286PubMedGoogle Scholar
  10. Chen J, Burke JJ, Xin Z, Xu C, Velten J (2006) Characterization of the Arabidopsis thermosensitive mutant atts02 reveals an important role for galactolipids in thermotolerance. Plant, Cell Environ 29:1437–1448CrossRefGoogle Scholar
  11. Chen DQ, Wang SW, Qi LY, Yin LN, Deng XP (2018) Galactolipid remodeling is involved in drought-induced leaf senescence in maize. Environ Exp Bot 150:57–68CrossRefGoogle Scholar
  12. Colebrook EH, Thomas SG, Phillips AL, Hedden P (2014) The role of gibberellin signalling in plant responses to abiotic stress. J Exp Biol 217:67–75CrossRefPubMedGoogle Scholar
  13. Dakhma WS, Zarrouk M, Cherif A (1995) Effects of drought-stress on lipids in rape leaves. Phytochemistry 40:1383–1386CrossRefGoogle Scholar
  14. Egamberdieva D (2009) Alleviation of salt stress by plant growth regulators and IAA producing bacteria in wheat. Acta Physiol Plant 31:861–864CrossRefGoogle Scholar
  15. Erdei L, Stuiver CEE, Kuiper PJC (1980) The effect of salinity on lipid-composition and on activity of Ca2+-stimulated and Mg2+-stimulated Atpases in salt-sensitive and salt-tolerant Plantago species. Physiol Plantarum 49:315–319CrossRefGoogle Scholar
  16. Flowers TJ, Troke PF, Yeo AR (1977) The mechanism of salt tolerence in halophytes. Ann Rew Plant Physiol 28:89–121CrossRefGoogle Scholar
  17. Gigon A, Matos AR, Laffray D, Zuily-Fodil Y, Pham-Thi AT (2004) Effect of drought stress on lipid metabolism in the leaves of Arabidopsis thaliana (ecotype Columbia). Ann Bot 94:345–351CrossRefPubMedPubMedCentralGoogle Scholar
  18. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Ann Rev Plant Physiol 51:463–499CrossRefGoogle Scholar
  19. Huynh VB, Repellin A, Zuily-Fodil Y, Pham-Thi AT (2012) Aluminum stress response in rice: effects on membrane lipid composition and expression of lipid biosynthesis genes. Physiol Plantarum 146:272–284CrossRefGoogle Scholar
  20. Iqbal M, Ashraf M (2013) Gibberellic acid mediated induction of salt tolerance in wheat plants: growth, ionic partitioning, photosynthesis, yield and hormonal homeostasis. Environ Exp Bot 86:76–85CrossRefGoogle Scholar
  21. Jarvis P, Dörmann P, Peto CA, Lutes J, Benning C, Chory J (2000) Galactolipid deficiency and abnormal chloroplast development in the Arabidopsis MGD synthase 1 mutant. P Natl Acad Sci USA 97:8175–8179CrossRefGoogle Scholar
  22. Kang DJ, Seo YJ, Lee JD, Ishii R, Kim KU, Shin DH, Park SK, Jang SW, Lee IJ (2005) Jasmonic acid differentially affects growth, ion uptake and abscisic acid concentration in salt-tolerant and salt-sensitive rice cultivars. J Agron Crop Sci 191:273–282CrossRefGoogle Scholar
  23. Keskin BC, Sarikaya AT, Yuksel B, Memon AR (2010) Abscisic acid regulated gene expression in bread wheat. Aust J Crop Sci 4:617–625Google Scholar
  24. Kobayashi K, Kondo M, Fukuda H, Nishimura M, Ohta H (2007) Galactolipid synthesis in chloroplast inner envelope is essential for proper thylakoid biogenesis, photosynthesis, and embryogenesis. P Natl Acad Sci USA 104:17216–17221CrossRefGoogle Scholar
  25. Krumova SB, Laptenok SP, Kovács L, Tóth T, van Hoek A, Garab G, van Amerongen H (2010) Digalactosyl-diacylglycerol-deficiency lowers the thermal stability of thylakoid membranes. Plant Physiol Biochem 47:518–525Google Scholar
  26. Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Method Enzymol 148:350–382CrossRefGoogle Scholar
  27. Liu P, Yin LN, Deng XP, Wang SW, Tanaka K, Zhang SQ (2014) Aquaporin-mediated increase in root hydraulic conductance is involved in silicon-induced improved root water uptake under osmotic stress in Sorghum bicolor L. J Exp Bot 65:4747–4756CrossRefPubMedPubMedCentralGoogle Scholar
  28. Maggio A, Barbieri G, Raimondi G, De Pascale S (2010) Contrasting effects of GA3 treatments on tomato plants exposed to increasing salinity. J Plant Growth Regu 29:63–72CrossRefGoogle Scholar
  29. Marechal E, Block MA, Joyard J, Douce R (1994) MGDG synthase of spinach chloroplast envelope: Properties of the substrate binding sites. Plant Lipid Metabolism 144-151Google Scholar
  30. Matos MC, Campos PS, Ramalho JC, Medeira MC, Maia MI, Semedo JM, Matos A (2002) Photosynthetic activity and cellular integrity of the Andean legume Pachyrhizus ahipa (Wedd.) Parodi under heat and water stress. Photosynthetica 40:493–501CrossRefGoogle Scholar
  31. Moellering ER, Benning C (2011) Galactoglycerolipid metabolism under stress: a time for remodeling. Trends Plant Sci 16:98–107CrossRefPubMedGoogle Scholar
  32. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681CrossRefPubMedGoogle Scholar
  33. Nakamura Y, Shimojima M, Ohta H, Shimojima K (2010) Biosynthesis and function of Monogalactosyldiacylglycerol (MGDG), the signature lipid of chloroplasts. The Chloroplast 185-202Google Scholar
  34. Omoto E, Iwasaki Y, Miyake H, Taniguchi M (2016) Salinity induces membrane structure and lipid changes in maize mesophyll and bundle sheath chloroplasts. Physiol Plantarum 157:13–23CrossRefGoogle Scholar
  35. Parida AK, Das AB (2004) Salt tolerance and salinity effects on plants: a review. Ecotox Environ Safe 60:324–349CrossRefGoogle Scholar
  36. Popov VN, Antipina OV, Pchelkin VP, Tsydendambaev VD (2012) Changes in the content and composition of lipid fatty acids in tobacco leaves and roots at low-temperature hardening. Russ J Plant Physiol 59:177–182CrossRefGoogle Scholar
  37. Prakash L, Prathapasenan G (1990) Interactive effect of NaCl salinity and gibberellic acid on shoot growth, content of abscisic acid and gibberellin-like substabces and yield of rice (Oryza sativa L. var GR-3). Proc Indian Acad Sci 100:173–181Google Scholar
  38. Qi YH, Yamauchi Y, Ling JQ, Kaoyoshi N, Li DB, Tanaka K (2004) Cloning of a putative monogalactosyldiacylglycerol synthase gene from rice (Oryza sativa L.) plants and its expression in response to submergence and other stresses. Planta 219:450–458PubMedGoogle Scholar
  39. Rawyler A, Pavelic D, Gianinazzi C, Oberson J, Braendle R (1999) Membrane lipid integrity relies on a threshold of ATP production rate in potato cell cultures submitted to anoxia. Plant Physiol 120:293–300CrossRefPubMedPubMedCentralGoogle Scholar
  40. Ruiz-Lozano JM, Porcel R, Azcón C, Aroca R (2012) Regulation by arbuscular mycorrhizae of the integrated physiological response to salinity in plants: new challenges in physiological and molecular studies. J Exp Bot 63:4033–4044CrossRefPubMedGoogle Scholar
  41. Shaterian J, Waterer D, De Jong H, Tanino KK (2005) Differential stress responses to NaCl salt application in early- and late maturing diploid potato (Solanum sp.) clones. Environ Exp Bot 54:202–212CrossRefGoogle Scholar
  42. Spychalla JP, Desborough SL (1990) Fatty acids, membrane permeability, and sugars of stored potato tubers. Plant Phy siol 94:1207–1213CrossRefGoogle Scholar
  43. Stevanovic B, Thu PTA, Depaula FM, Dasilva JV (1992) Effects of dehydration and rehydration on the polar lipid and fatty-acid composition of Ramonda species. Can J Bot 70:107–113CrossRefGoogle Scholar
  44. Sui N, Han GL (2014) Salt-induced photoinhibition of PSII is alleviated in halophyte Thellungiella halophila by increases of unsaturated fatty acids in membrane lipids. Acta Physiol Plant 36:983–992CrossRefGoogle Scholar
  45. Sui N, Li M, Shu DF, Zhao SJ, Meng QW (2007) Antisense-mediated depletion of tomato chloroplast glycerol-3-phosphate acyltransferase affects male fertility and increases thermal tolerance. Physiol Plantarum 130:301–314CrossRefGoogle Scholar
  46. Sui N, Li M, Li K, Song J, Wang BS (2010) Increase in unsaturated fatty acids in membrane lipids of Suaeda salsa L. enhances protection of photosystem II under high salinity. Photosynthetica 48:623–629CrossRefGoogle Scholar
  47. Sun YL, Li F, Su N, Sun XL, Zhao SJ, Meng QW (2010) The increase in unsaturation of fatty acids of phosphatidylglycerol in thylakoid membrane enhanced salt tolerance in tomato. Photosynthetica 48:400–408CrossRefGoogle Scholar
  48. Thomas PG, Dominy PJ, Vigh L, Mansourian AR, Quinn PJ, Williams WP (1986) Increased thermal stability of pigment-protein complexes of pea thylakoids following catalytic hydrogenation of membrane lipids. Biochimica et Biophysica Acta (BBA) –. Bioenergetics 849:131–140CrossRefGoogle Scholar
  49. Walia H, Wilson C, Condamine P, Liu X, Ismail AM (2007) Large-scale expressiom profiling and physiological characterization of jasmonic acid-mediated adaptation of barley to salintiy stress. Plant, Cell Environ 30:410–421CrossRefGoogle Scholar
  50. Wang SY, Lin HS (2006) Effect of plant growth temperature on membrane lipids in strawberry (Fragaria × ananassa Duch.). Sci Hortic 108:35–42CrossRefGoogle Scholar
  51. Wang SW, Uddin MI, Tanaka K, Yin LN, Shi ZH, Qi YH, Deng XP (2014) Maintenance of chloroplast structure and function by overexpression of the rice monogalactosyldiacylglycerol synthase gene leads to enhanced salt tolerance in Tobacco. Plant Physiol 165:1144–1155CrossRefPubMedPubMedCentralGoogle Scholar
  52. Wen FP, Zhang ZH, Bai T, Xu Q, Pan YH (2010) Proteomics reveals the effects of gibberellic acid (GA3) on salt-stressed rice (Oryza sativa L.) shoots. Plant Sci 178:170–175CrossRefGoogle Scholar
  53. Wewer V, Dörmann P, Hölzl G (2013) Analysis and quantification of plant membrane lipids by thin-layer chromatography and gas chromatography. Plant Lipid Signaling Protocols 1009:69–78CrossRefGoogle Scholar
  54. Wu JL, Seliskar DM, Gallagher JL (1998) Stress tolerance in the marsh plant Spartina patens impact of NaCl on growth and root plasma membrane lipid composition. Physiol Plantarum 102:307–317CrossRefGoogle Scholar
  55. Yamamoto Y, Kai S, Ohnishi A, Tsumura N, Ishikawa T, Hori H, Ishikawa Y (2014) Quality control of PSII: behavior of PSII in the highly crowded grana thylakoids under excessive light. Plant Cell Physiol 55:1206–1215CrossRefPubMedPubMedCentralGoogle Scholar
  56. Yoshida S, Forno DA, Cock JH, Gomez KA (1976) Laboratory manual for physiological studies of rice [M]. 3rd ed. Manila Int. Rice Res. InstGoogle Scholar
  57. Zhang MJ, Deng XP, Yin LN, Qi LY, Wang XY, Wang SW, Li HB (2016) Regulation of galactolipid biosynthesis by overexpression of the rice MGD gene contributes to enhanced Aluminum tolerance in Tobacco. Front Plant Sci 7:337PubMedPubMedCentralGoogle Scholar
  58. Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71CrossRefPubMedGoogle Scholar

Copyright information

© Brazilian Society of Plant Physiology 2018

Authors and Affiliations

  • Xiaoxiao Liu
    • 1
    • 2
    • 3
  • Xinyue Wang
    • 2
  • Lina Yin
    • 1
    • 2
    Email author
  • Xiping Deng
    • 1
    • 2
  • Shiwen Wang
    • 1
    • 2
  1. 1.State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau, Institute of Soil and Water ConservationNorthwest A&F UniversityYanglingChina
  2. 2.Institute of Soil and Water ConservationChinese Academy of Science and Ministry of Water ResourceYanglingChina
  3. 3.University of Chinese Academy of SciencesBeijingChina

Personalised recommendations