Abstract
Lipids are the major constituents of all membranous structures in plants. Plants possess two pathways for lipid biosynthesis: the prokaryotic pathway (i.e., plastidic pathway) and the eukaryotic pathway (i.e., endoplasmic-reticulum (ER) pathway). Whereas some plants synthesize galactolipids from diacylglycerol assembled in the plastid, others, including rice, derive their galactolipids from diacylglycerols assembled by the eukaryotic pathway. Arabidopsis thaliana glycerol-3-phosphate dehydrogenase (G3pDH), coded by SUPPRESSOR OF FATTY ACID DESATURASE 1 (SFD1; alias GLY1) gene, catalyzes the formation of glycerol 3-phosphate (G3p), the backbone of many membrane lipids. Here SFD1 was introduced to rice as a transgene. Arabidopsis SFD1 localizes in rice plastids and its over-expression increases plastidic membrane lipid content in transgenic rice plants without any major impact on ER lipids. The results suggest that over-expression of plastidic G3pDH enhances biosynthesis of plastid-localized lipids in rice. Lipid composition in the transgenic plants is consistent with increased phosphatidylglycerol synthesis in the plastid and increased galactolipid synthesis from diacylglycerol produced via the ER pathway. The transgenic plants show a higher photosynthetic assimilation rate, suggesting a possible application of this finding in crop improvement.






Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.Abbreviations
- DAG:
-
Diacylglycerol
- DGDG:
-
Digalactosyldiacylglycerol
- ER:
-
Endoplasmic reticulum
- FA:
-
Fatty acid
- GLC:
-
Gas–liquid chromatography
- G3p:
-
Glycerol 3-phosphate
- G3pDH:
-
Glycerol-3-phosphate dehydrogenase
- IRGA:
-
Infrared gas analyzer
- MGDG:
-
Monogalactosyldiacylglycerol
- PC:
-
Phosphatidylcholine
- PE:
-
Phosphatidylethanolamine
- PG:
-
Phosphatidylglycerol
- PI:
-
Phosphatidylinositol
- SFD1 :
-
SUPPRESSOR OF FATTY ACID DESATURASE 1
- TAG:
-
Triacylglycerol
References
Allen CF, Good P, Holton RW (1970) Lipid composition of cyanidium. Plant Physiol 46:748–751
Baud S, Lepiniec L (2010) Physiological and developmental regulation of seed oil production. Prog Lipid Res 49:235–249. doi:10.1016/j.plipres.2010.01.001
Benson AA (1971) Lipids of chloroplasts. In: Gibbs M (ed) Structure and function of chloroplasts. Springer Verlag, Berlin, pp 129–148
Browse J (2010) Plant science. Saving the bilayer. Science 330:185–186. doi:10.1126/science.1196737
Browse J, Warwick N, Somerville CR, Slack CR (1986) Fluxes through the prokaryotic and eukaryotic pathways of lipid synthesis in the ‘16:3’ plant Arabidopsis thaliana. Biochem J 235:25–31
Chanda B, Xia Y, Mandal MK, Yu K, Sekine KT, Gao QM, Selote D, Hu Y, Stromberg A, Navarre D, Kachroo A, Kachroo P (2011) Glycerol-3-phosphate is a critical mobile inducer of systemic immunity in plants. Nat Genet 43:421–427. doi:10.1038/ng.798
Chen S, Songkumarn P, Liu J, Wang GL (2009) A versatile zero background T-vector system for gene cloning and functional genomics. Plant Physiol 150:1111–1121. doi:10.1104/pp.109.137125
Domonkos I, Laczko-Dobos H, Gombos Z (2008) Lipid-assisted protein–protein interactions that support photosynthetic and other cellular activities. Prog Lipid Res 47:422–435. doi:10.1016/j.plipres.2008.05.003
Dormann P, Benning C (2002) Galactolipids rule in seed plants. Trend Plant Sci 7:112–118. doi:10.1016/S1360-1385(01)02216-6
Dubots E, Audry M, Yamaryo Y, Bastien O, Ohta H, Breton C, Marechal E, Block MA (2010) Activation of the chloroplast monogalactosyldiacylglycerol synthase MGD1 by phosphatidic acid and phosphatidylglycerol. J Biol Chem 285:6003–6011. doi:10.1074/jbc.M109.071928
Eastmond PJ (2004) Glycerol-insensitive Arabidopsis mutants: gli1 seedlings lack glycerol kinase, accumulate glycerol and are more resistant to abiotic stress. Plant J Cell Mol Biol 37:617–625
Heinz E, Roughan PG (1983) Similarities and differences in lipid metabolism of chloroplasts isolated from 18:3 and 16:3 plants. Plant Physiol 72:273–279
Holzl G, Witt S, Gaude N, Melzer M, Schottler MA, Dormann P (2009) The role of diglycosyl lipids in photosynthesis and membrane lipid homeostasis in arabidopsis. Plant Physiol 150:1147–1159. doi:10.1104/pp.109.139758
Jones MR (2007) Lipids in photosynthetic reaction centres: structural roles and functional holes. Prog Lipid Res 46:56–87. doi:10.1016/j.plipres.2006.06.001
Jordan P, Fromme P, Witt HT, Klukas O, Saenger W, Krauss N (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 A resolution. Nature 411:909–917. doi:10.1038/35082000
Kang L, Li J, Zhao T, Xiao F, Tang X, Thilmony R, He S, Zhou JM (2003) Interplay of the Arabidopsis nonhost resistance gene NHO1 with bacterial virulence. Proc Natl Acad Sci USA 100:3519–3524. doi:10.1073/pnas.0637377100
Lorenc-Kukula K, Chaturvedi R, Roth M, Welti R, Shah J (2012) Biochemical and molecular-genetic characterization of sfd1’s involvement in lipid metabolism and defense signaling. Front Plant Sci 3:26. doi:10.3389/fpls.2012.00026
Lu M, Tang X, Zhou JM (2001) Arabidopsis NHO1 is required for general resistance against Pseudomonas bacteria. Plant Cell 13:437–447
Maguire TL, Collins GC, Sedgley M (1991) A modified CTAB DNA extraction procedure for plants belonging to the family proteaceae. Plant Mol Biol Report 12:106–109
Mandal MK, Chanda B, Xia Y, Yu K, Sekine KT, Gao QM, Selote D, Kachroo A, Kachroo P (2011) Glycerol-3-phosphate and systemic immunity. Plant Signal Beh 6:1871–1874. doi:10.4161/psb.6.11.17901
Miquel M, Cassagne C, Browse J (1998) A new class of Arabidopsis mutants with reduced hexadecatrienoic acid fatty acid levels. Plant Physiol 117(3):923–930
Mongrand S, Bessoule JJ, Cabantous F, Cassagne C (1998) The C16:3/C18:3 fatty acid balance in photosynthetic tissues from 468 plant species. Phytochemistry 49:1049–1064
Mukherjee KD (1983) Lipid biosynthesis in developing mustard seed: formation of triacylglycerols from endogenous and exogenous fatty acids. Plant Physiol 73:929–934
Nandi A, Krothapalli K, Buseman CM, Li M, Welti R, Enyedi A, Shah J (2003) Arabidopsis sfd mutants affect plastidic lipid composition and suppress dwarfing, cell death, and the enhanced disease resistance phenotypes resulting from the deficiency of a fatty acid desaturase. Plant Cell 15:2383–2398. doi:10.1105/tpc.015529
Nandi A, Welti R, Shah J (2004) The Arabidopsis thaliana dihydroxyacetone phosphate reductase gene SUPPRESSSOR OF FATTY ACID DESATURASE DEFICIENCY1 is required for glycerolipid metabolism and for the activation of systemic acquired resistance. Plant Cell 16:465–477. doi:10.1105/tpc.016907
Ohlrogge J, Browse J (1995) Lipid biosynthesis. Plant Cell 7:957–970
Parkhill J-P, Maillet G, Cullen JJ (2001) Fluorescence-based maximal quantum yield for PSII as a diagnositic tool of nutrient stress. J Phycol 37:517–529
Perry HJ, Bligny R, Gout E, Harwood JL (1999) Changes in Kennedy pathway intermediates associated with increased triacylglycerol synthesis in oil-seed rape. Phytochemistry 52:799–804. doi:10.1016/S0031-9422(99)00294-0
Ritchie RJ (2006) Consistent sets of spectrophotometric chlorophyll equations for acetone, methanol and ethanol solvents. Photosynth Res 89:27–41. doi:10.1007/s11120-006-9065-9
Roughan PG, Batt RD (1969) The glycerolipid composition of leaves. Phytochemistry 8:363–369
Shen W, Wei Y, Dauk M, Tan Y, Taylor DC, Selvaraj G, Zou J (2006) Involvement of a glycerol-3-phosphate dehydrogenase in modulating the NADH/NAD + ratio provides evidence of a mitochondrial glycerol-3-phosphate shuttle in Arabidopsis. Plant Cell 18:422–441. doi:10.1105/tpc.105.039750
Shen W, Li JQ, Dauk M, Huang Y, Periappuram C, Wei Y, Zou J (2010) Metabolic and transcriptional responses of glycerolipid pathways to a perturbation of glycerol 3-phosphate metabolism in Arabidopsis. J Biol Chem 285:22957–22965. doi:10.1074/jbc.M109.097758
Shimojima M, Watanabe T, Madoka Y, Koizumi R, Yamamoto MP, Masuda K, Yamada K, Masuda S, Ohta H (2013) Differential regulation of two types of monogalactosyldiacylglycerol synthase in membrane lipid remodeling under phosphate-limited conditions in sesame plants. Front Plant Sci 4:469. doi:10.3389/fpls.2013.00469
Singh S, Giri MK, Singh PK, Siddiqui A, Nandi AK (2013) Down-regulation of OsSAG12-1 results in enhanced senescence and pathogen-induced cell death in transgenic rice plants. J Biosci 38:583–592
Stumpf PK (1984) Plant lipid biosynthesis in 1959 and 1984. J Lipid Res 25:1508–1510
Toriyama S, Hinata K, Nishida I, Murata N (1988) Prominent difference of glycerolipids among anther walls, pollen grains adn leaves of rice and maize. Plant Cell Physiol 29:615–618
Vigeolas H, Waldeck P, Zank T, Geigenberger P (2007) Increasing seed oil content in oil-seed rape (Brassica napus L.) by over-expression of a yeast glycerol-3-phosphate dehydrogenase under the control of a seed-specific promoter. Plant Biotechnol J 5:431–441
von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153:376–387. doi:10.1007/BF00384257
Wang H, Chen C, Xu Y, Jiang R, Han Y, Xu Z, Chong K (2004) A practical vector for efficient knockdown of gene expression in rice (Oryza sativa L.). Plant Mol Biol Report 22:409–417
Wang Y, Wu J, Kim SG, Kim ST, Kang KY (2013) A transient gene expression protocol for subcellular protein localization and protein secretion analyses in rice. Protoc Exch. doi:10.1038/protex.2013.064
Welti R, Li W, Li M, Sang Y, Biesiada H, Zhou HE, Rajashekar CB, Williams TD, Wang X (2002) Profiling membrane lipids in plant stress responses. Role of phospholipase D alpha in freezing-induced lipid changes in Arabidopsis. J Biol Chem 277:31994–32002. doi:10.1074/jbc.M205375200
Yu K, Soares JM, Mandal MK, Wang C, Chanda B, Gifford AN, Fowler JS, Navarre D, Kachroo A, Kachroo P (2013) A feedback regulatory loop between G3P and lipid transfer proteins DIR1 and AZI1 mediates azelaic-acid-induced systemic immunity. Cell Rep 3:1266–1278. doi:10.1016/j.celrep.2013.03.030
Zhang Y, Su J, Duan S, Ao Y, Dai J, Liu J, Wang P, Li Y, Liu B, Feng D, Wang J, Wang H (2011) A highly efficient rice green tissue protoplast system for transient gene expression and studying light/chloroplast-related processes. Plant Method 7:30. doi:10.1186/1746-4811-7-30
Acknowledgments
This work is supported by the DST-purse, Capacity Build-up and UGC resource network funds to AKN. SS and ZZB obtained fellowships from CSIR and ICMR respectively. We acknowledge Arabidopsis Biological Resource Centre, Ohio State University, USA for SFD1 cDNA. The lipid profile data were acquired at Kansas Lipidomics Research Center (KLRC). We thank Mary Roth of KLRC for her technical work and Ruth Welti for critical reading and editing of the manuscript. Instrument acquisition and method development at KLRC were supported by NSF grants MCB 0455318, MCB 0920663, DBI 0521587, DBI 1228622, Kansas INBRE (P20 GM103418 from the National Institute of General Medical Sciences), NSF EPSCoR grant EPS-0236913, Kansas Technology Enterprise Corporation, and Kansas State University. We also acknowledge B.C. Tripathy and Amarchand Kunawat for help in photosynthesis related experiments and Tripti Panwar for help in microscopy.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflict of interest to declare.
Additional information
V. Singh and P. K. Singh contributed equally.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Singh, V., Singh, P.K., Siddiqui, A. et al. Over-expression of Arabidopsis thaliana SFD1/GLY1, the gene encoding plastid localized glycerol-3-phosphate dehydrogenase, increases plastidic lipid content in transgenic rice plants. J Plant Res 129, 285–293 (2016). https://doi.org/10.1007/s10265-015-0781-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10265-015-0781-0


