Nonspecific phospholipase C6 increases seed oil production in oilseed Brassicaceae plants.
Brassicaceae
lipid turnover
nonspecific phospholipase C
seed oil
seed yield
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
05 2020
05 2020
Historique:
received:
17
10
2019
accepted:
13
12
2019
pubmed:
17
3
2020
medline:
15
5
2021
entrez:
17
3
2020
Statut:
ppublish
Résumé
Plant oils are valuable commodities for food, feed, renewable industrial feedstocks and biofuels. To increase vegetable oil production, here we show that the nonspecific phospholipase C6 (NPC6) promotes seed oil production in the Brassicaceae seed oil species Arabidopsis, Camelina and oilseed rape. Overexpression of NPC6 increased seed oil content, seed weight and oil yield both in Arabidopsis and Camelina, whereas knockout of NPC6 decreased seed oil content and seed size. NPC6 is associated with the chloroplasts and microsomal membranes, and hydrolyzes phosphatidylcholine and galactolipids to produce diacylglycerol. Knockout and overexpression of NPC6 decreased and increased, respectively, the flux of fatty acids from phospholipids and galactolipids into triacylglycerol production. Candidate-gene association study in oilseed rape indicates that only BnNPC6.C01 of the four homeologues NPC6s is associated with seed oil content and yield. Haplotypic analysis indicates that the BnNPC6.C01 favorable haplotype can increase both seed oil content and seed yield. These results indicate that NPC6 promotes membrane glycerolipid turnover to accumulate TAG production in oil seeds and that NPC6 has a great application potential for oil yield improvement.
Substances chimiques
Fatty Acids
0
Plant Oils
0
Phospholipases
EC 3.1.-
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
1055-1073Informations de copyright
© 2020 The Authors. New Phytologist © 2020 New Phytologist Trust.
Références
Aznar-Moreno J, Durrett T. 2017. Simultaneous targeting of multiple gene homeologs to alter seed oil production in Camelina sativa. Plant and Cell Physiology 58: 1260-1267.
Bates PD, Durrett TP, Ohlrogge JB, Pollard M. 2009. Analysis of acyl fluxes through multiple pathways of triacylglycerol synthesis in developing soybean embryos. Plant Physiology 150: 55-72.
Bates PD, Fatihi A, Snapp AR, Carlsson AS, Lu C. 2012. Acyl editing and headgroup exchange are the major mechanisms that direct polyunsaturated fatty acid flux into triacylglycerols. Plant Physiology 160: 1530-1539.
Baud S, Dubreucq B, Miquel M, Rochat C, Lepiniec L. 2008. Storage reserve accumulation in Arabidopsis: metabolic and developmental control of seed filling. The Arabidopsis Book 6: e0113.
Baud S, Lepiniec L. 2010. Physiological and developmental regulation of seed oil production. Progress in Lipid Research 49: 235-249.
Branham SE, Wright SJ, Reba A, Linder CR. 2015. Genome-wide association study of Arabidopsis thaliana identifies determinants of natural variation in seed oil composition. Journal of Heredity 107: 248-256.
Cai G, Yang Q, Chen H, Yang Q, Zhang C, Fan C, Zhou Y. 2016. Genetic dissection of plant architecture and yield-related traits in Brassica napus. Scientific Reports 6: 21625.
Cai Y, Goodman JM, Pyc M, Mullen RT, Dyer JM, Chapman KD. 2015. Arabidopsis SEIPIN proteins modulate triacylglycerol accumulation and influence lipid droplet proliferation. Plant Cell 27: 2616-2636.
Carter C, Pan S, Zouhar J, Avila EL, Girke T, Raikhel NV. 2004. The vegetative vacuole proteome of Arabidopsis thaliana reveals predicted and unexpected proteins. Plant Cell 16: 3285-3303.
Cernac A, Andre C, Hoffmann-Benning S, Benning C. 2006. WRI1 is required for seed germination and seedling establishment. Plant Physiology 141: 745-757.
Cernac A, Benning C. 2004. WRINKLED1 encodes an AP2/EREB domain protein involved in the control of storage compound biosynthesis in Arabidopsis. The Plant Journal 40: 575-585.
Chalhoub B, Denoeud F, Liu S, Parkin IA, Tang H, Wang X, Chiquet J, Belcram H, Tong C, Samans B et al. 2014. Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science 345: 950-953.
Chapman KD, Ohlrogge JB. 2012. Compartmentation of triacylglycerol accumulation in plants. Journal of Biological Chemistry 287: 2288-2294.
Dahlqvist A, Stahl U, Lenman M, Banas A, Lee M, Sandager L, Ronne H, Stymne S. 2000. Phospholipid:diacylglycerol acyltransferase: an enzyme that catalyzes the acyl-CoA-independent formation of triacylglycerol in yeast and plants. Proceedings of the National Academy of Sciences, USA 97: 6487-6492.
Eastmond PJ. 2006. SUGAR-DEPENDENT1 encodes a patatin domain triacylglycerol lipase that initiates storage oil breakdown in germinating Arabidopsis seeds. Plant Cell 18: 665-675.
Fan C, Cai G, Qin J, Li Q, Yang M, Wu J, Fu T, Liu K, Zhou Y. 2010. Mapping of quantitative trait loci and development of allele-specific markers for seed weight in Brassica napus. Theoretical and Applied Genetics 121: 1289-1301.
Gaude N, Nakamura Y, Scheible WR, Ohta H, Dörmann P. 2008. Phospholipase C5 (NPC5) is involved in galactolipid accumulation during phosphate limitation in leaves of Arabidopsis. The Plant Journal 56: 28-39.
Graham IA. 2008. Seed storage oil mobilization. Annual Review of Plant Biology 59: 115-142.
Guo L, Ma F, Wei F, Fanella B, Allen DK, Wang X. 2014. Cytosolic phosphorylating glyceraldehyde-3-phosphate dehydrogenases affect Arabidopsis cellular metabolism and promote seed oil accumulation. Plant Cell 26: 3023-3035.
Hobbs DH, Flintham JE, Hills MJ. 2004. Genetic control of storage oil synthesis in seeds of Arabidopsis. Plant Physiology 136: 3341-3349.
Hong Y, Zhao J, Guo L, Kim S-C, Deng X, Wang G, Zhang G, Li M, Wang X. 2016. Plant phospholipases D and C and their diverse functions in stress responses. Progress in Lipid Research 62: 55-74.
Hooper CM, Castleden IR, Tanz SK, Aryamanesh N, Millar AH. 2016. SUBA4: the interactive data analysis centre for Arabidopsis subcellular protein locations. Nucleic Acids Research 45: D1064-D1074.
Hwang E-Y, Song Q, Jia G, Specht JE, Hyten DL, Costa J, Cregan PB. 2014. A genome-wide association study of seed protein and oil content in soybean. BMC Genomics 15: 1.
Kelly AA, Feussner I. 2016. Oil is on the agenda: lipid turnover in higher plants. Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids 1861: 1253-1268.
Kelly AA, Quettier A-L, Shaw E, Eastmond PJ. 2011. Seed storage oil mobilization is important but not essential for germination or seedling establishment in Arabidopsis. Plant Physiology 157: 866-875.
Kim S, Yamaoka Y, Ono H, Kim H, Shim D, Maeshima M, Martinoia E, Cahoon EB, Nishida I, Lee Y. 2013. AtABCA9 transporter supplies fatty acids for lipid synthesis to the endoplasmic reticulum. Proceedings of the National Academy of Sciences, USA 110: 773-778.
Kim S-C, Guo L, Wang X. 2013. Phosphatidic acid binds to cytosolic glyceraldehyde-3-phosphate dehydrogenase and promotes its cleavage in Arabidopsis. Journal of Biological Chemistry 288: 11834-11844.
Kim SC, Nusinow DA, Sorkin ML, Pruneda-Paz J, Wang X. 2019. Interaction and regulation between lipid mediator phosphatidic acid and circadian clock regulators in Arabidopsis. Plant Cell 31: 399-416.
Klinkenberg J. 2014. Extraction of chloroplast proteins from transiently transformed Nicotiana benthamiana leaves. Bio-Protocol 4: e1238.
Krčková Z, Brouzdová J, Daněk M, Kocourková D, Rainteau D, Ruelland E, Valentová O, Pejchar P, Martinec J. 2015. Arabidopsis non-specific phospholipase C1: characterization and its involvement in response to heat stress. Frontiers in Plant Science 6: 928.
Krčková Z, Kocourková D, Daněk M, Brouzdová J, Pejchar P, Janda M, Pokotylo I, Ott PG, Valentová O, Martinec J. 2017. The Arabidopsis thaliana non-specific phospholipase C2 is involved in the response to Pseudomonas syringae attack. Annals of Botany 121: 297-310.
Li F, Chen B, Xu K, Wu J, Song W, Bancroft I, Harper AL, Trick M, Liu S, Gao G. 2014. Genome-wide association study dissects the genetic architecture of seed weight and seed quality in rapeseed (Brassica napus L.). DNA Research 21: 355-367.
Li H, Peng Z, Yang X, Wang W, Fu J, Wang J, Han Y, Chai Y, Guo T, Yang N. 2013. Genome-wide association study dissects the genetic architecture of oil biosynthesis in maize kernels. Nature Genetics 45: 43-48.
Li M, Bahn SC, Fan C, Li J, Phan T, Ortiz M, Roth MR, Welti R, Jaworski J, Wang X. 2013. Patatin-related phospholipase pPLAIIIδ increases seed oil content with long-chain fatty acids in Arabidopsis. Plant Physiology 162: 39-51.
Li M, Bahn SC, Guo L, Musgrave W, Berg H, Welti R, Wang X. 2011. Patatin-related phospholipase pPLAIIIβ-induced changes in lipid metabolism alter cellulose content and cell elongation in Arabidopsis. Plant Cell 23: 1107-1123.
Li M, Wei F, Tawfall A, Tang M, Saettele A, Wang X. 2015. Overexpression of patatin-related phospholipase AIII δ altered plant growth and increased seed oil content in camelina. Plant Biotechnology Journal 13: 766-778.
Li N, Gügel IL, Giavalisco P, Zeisler V, Schreiber L, Soll J, Philippar K. 2015. FAX1, a novel membrane protein mediating plastid fatty acid export. PLoS Biology 13: e1002053.
Li-Beisson Y, Shorrosh B, Beisson F, Andersson MX, Arondel V, Bates PD, Baud S, Bird D, DeBono A, Durrett TP. 2013. Acyl-lipid metabolism. The Arabidopsis Book 11: e0161.
Lippert C, Listgarten J, Liu Y, Kadie CM, Davidson RI, Heckerman D. 2011. FaST linear mixed models for genome-wide association studies. Nature methods 8: 833.
Liu J, Hao W, Liu J, Fan S, Zhao W, Deng L, Wang X, Hu Z, Hua W, Wang H. 2019. A novel chimeric mitochondrial gene confers cytoplasmic effects on seed oil content in polyploid rapeseed (Brassica napus L.). Molecular Plant 12: 582-596.
Liu S, Fan C, Li J, Cai G, Yang Q, Wu J, Yi X, Zhang C, Zhou Y. 2016. A genome-wide association study reveals novel elite allelic variations in seed oil content of Brassica napus. Theoretical and Applied Genetics 129: 1203-1215.
Liu Y, Wang G, Wang X. 2015. Role of aminoalcoholphosphotransferases 1 and 2 in phospholipid homeostasis in Arabidopsis. Plant Cell 27: 1512-1528.
Lu C, Xin Z, Ren Z, Miquel M. 2009. An enzyme regulating triacylglycerol composition is encoded by the ROD1 gene of Arabidopsis. Proceedings of the National Academy of Sciences, USA 106: 18837-18842.
Lu K, Wei L, Li X, Wang Y, Wu J, Liu M, Zhang C, Chen Z, Xiao Z, Jian H. 2019. Whole-genome resequencing reveals Brassica napus origin and genetic loci involved in its improvement. Nature Communications 10: 1154.
Mhaske V, Beldjilali K, Ohlrogge J, Pollard M. 2005. Isolation and characterization of an Arabidopsis thaliana knockout line for phospholipid: diacylglycerol transacylase gene (At5g13640). Plant Physiology and Biochemistry 43: 413-417.
Mu J, Tan H, Zheng Q, Fu F, Liang Y, Zhang J, Yang X, Wang T, Chong K, Wang X-J. 2008. LEAFY COTYLEDON1 is a key regulator of fatty acid biosynthesis in Arabidopsis. Plant Physiology 148: 1042-1054.
Nakamura Y, Awai K, Masuda T, Yoshioka Y, Takamiya K-i, Ohta H. 2005. A novel phosphatidylcholine-hydrolyzing phospholipase C induced by phosphate starvation in Arabidopsis. Journal of Biological Chemistry 280: 7469-7476.
Ngo AH, Lin YC, Yc Liu, Gutbrod K, Peisker H, Dörmann P, Nakamura Y. 2018. A pair of nonspecific phospholipases C, NPC 2 and NPC 6, are involved in gametophyte development and glycerolipid metabolism in Arabidopsis. New Phytologist 219: 163-175.
Pejchar P, Potocký M, Krčková Z, Brouzdová J, Daněk M, Martinec J. 2015. Non-specific phospholipase C4 mediates response to aluminum toxicity in Arabidopsis thaliana. Frontiers in Plant Science 6: 66.
Peters C, Kim SC, Devaiah S, Li M, Wang X. 2014. Non-specific phospholipase C5 and diacylglycerol promote lateral root development under mild salt stress in Arabidopsis. Plant, Cell & Environment 37: 2002-2013.
Peters C, Li M, Narasimhan R, Roth M, Welti R, Wang X. 2010. Nonspecific phospholipase C NPC4 promotes responses to abscisic acid and tolerance to hyperosmotic stress in Arabidopsis. Plant Cell 22: 2642-2659.
Pokotylo I, Pejchar P, Potocký M, Kocourková D, Krčková Z, Ruelland E, Kravets V, Martinec J. 2013. The plant non-specific phospholipase C gene family. Novel competitors in lipid signalling. Progress in Lipid Research 52: 62-79.
Porebski S, Bailey LG, Baum BR. 1997. Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components. Plant Molecular Biology Reporter 15: 8-15.
Pyc M, Cai Y, Gidda SK, Yurchenko O, Park S, Kretzschmar FK, Ischebeck T, Valerius O, Braus GH, Chapman KD. 2017. Arabidopsis lipid droplet-associated protein (LDAP)-interacting protein (LDIP) influences lipid droplet size and neutral lipid homeostasis in both leaves and seeds. The Plant Journal 92: 1182-1201.
Raj A, Stephens M, Pritchard JK. 2014. fastSTRUCTURE: variational inference of population structure in large SNP data sets. Genetics 197: 573-589.
Santeramo FG, Searle S. 2019. Linking soy oil demand from the US Renewable Fuel Standard to palm oil expansion through an analysis on vegetable oil price elasticities. Energy Policy 127: 19-23.
Santos-Mendoza M, Dubreucq B, Baud S, Parcy F, Caboche M, Lepiniec L. 2008. Deciphering gene regulatory networks that control seed development and maturation in Arabidopsis. The Plant Journal 54: 608-620.
Shen B, Allen WB, Zheng P, Li C, Glassman K, Ranch J, Nubel D, Tarczynski MC. 2010. Expression of ZmLEC1 and ZmWRI1 increases seed oil production in maize. Plant Physiology 153: 980-987.
Slack CR, Campbell LC, Browse JA, Roughan PG. 1983. Some evidence for the reversibility of the cholinephosphotransferasecatalysed reaction in developing linseed cotyledons in vivo. Biochimica et Biophysica Acta (BBA) - Lipids and Lipid Metabolism 754: 10-20.
Stymne S, Stobart A. 1987. Triacylglycerol biosynthesis. In: Stumpf P, Conn E, eds. Lipids: structure and function. Orlando, FL, USA: Academic Press, 175-214.
Su Y, Li M, Guo L, Wang X. 2018. Different effects of phospholipase Dζ2 and non-specific phospholipase C4 on lipid remodeling and root hair growth in Arabidopsis response to phosphate deficiency. The Plant Journal 94: 315-326.
Tjellström H, Yang Z, Allen DK, Ohlrogge JB. 2012. Rapid kinetic labeling of Arabidopsis cell suspension cultures: implications for models of lipid export from plastids. Plant Physiology 158: 601-611.
Vanhercke T, Dyer JM, Mullen RT, Kilaru A, Rahman MM, Petrie JR, Green AG, Yurchenko O, Singh SP. 2019. Metabolic engineering for enhanced oil in biomass. Progress in Lipid Research 74: 103-129.
Voelker T, Kinney AJ. 2001. Variations in the biosynthesis of seed-storage lipids. Annual Review of Plant Biology 52: 335-361.
Wang K, Froehlich JE, Zienkiewicz A, Hersh HL, Benning C. 2017. A plastid phosphatidylglycerol lipase contributes to the export of acyl groups from plastids for seed oil biosynthesis. Plant Cell 29: 1678-1696.
Wang L, Shen W, Kazachkov M, Chen G, Chen Q, Carlsson AS, Stymne S, Weselake RJ, Zou J. 2012. Metabolic interactions between the Lands cycle and the Kennedy pathway of glycerolipid synthesis in Arabidopsis developing seeds. Plant Cell 24: 4652-4669.
Wang X. 2005. Regulatory functions of phospholipase D and phosphatidic acid in plant growth, development, and stress responses. Plant Physiology 139: 566-573.
Wang X, Su Y, Liu Y, Kim S, Fanella B. 2014. Phospholipases in plant signaling. Heidelberg, Germany: Springer, Berlin.
Welti R, Li W, Li M, Sang Y, Biesiada H, Zhou H-E, Rajashekar C, Williams TD, Wang X. 2002. Profiling membrane lipids in plant stress responses role of phospholipase Dα in freezing-induced lipid changes in Arabidopsis. Journal of Biological Chemistry 277: 31994-32002.
Wimalasekera R, Pejchar P, Holk A, Martinec J, Scherer GF. 2010. Plant phosphatidylcholine-hydrolyzing phospholipases C NPC3 and NPC4 with roles in root development and brassinolide signaling in Arabidopsis thaliana. Molecular Plant 3: 610-625.
Wu D, Liang Z, Yan T, Xu Y, Xuan L, Tang J, Zhou G, Lohwasser U, Hua S, Wang H. 2019. Whole-genome resequencing of a worldwide collection of rapeseed accessions reveals the genetic basis of ecotype divergence. Molecular Plant 12: 30-43.
Xing Y, Zhang Q. 2010. Genetic and molecular bases of rice yield. Annual Review of Plant Biology 61: 421-442.
Yang W, Wang G, Li J, Bates PD, Wang X, Allen DK. 2017. Phospholipase Dζ enhances diacylglycerol flux into triacylglycerol. Plant Physiology 174: 110-123.
Zhang M, Fan J, Taylor DC, Ohlrogge JB. 2009. DGAT1 and PDAT1 acyltransferases have overlapping functions in Arabidopsis triacylglycerol biosynthesis and are essential for normal pollen and seed development. Plant Cell 21: 3885-3901.
Zhou Z, Jiang Y, Wang Z, Gou Z, Lyu J, Li W, Yu Y, Shu L, Zhao Y, Ma Y. 2015. Resequencing 302 wild and cultivated accessions identifies genes related to domestication and improvement in soybean. Nature Biotechnology 33: 408-414.