WRINKLED1, a “Master Regulator” in Transcriptional Control of Plant Oil Biosynthesis
Abstract
:1. Introduction
2. WRI1 Acts as a Key Transcriptional Regulator in Governing Plant Oil Biosynthesis
3. Regulators Involved in Mediating the Expression of WRI1
4. Molecular Regulatory Mechanism of AtWRI1 Activity
5. WRI1 Orthologs Identified in Various Plant Species
6. Newly Identified Targets of AtWRI1 That Are Not in Oil Biosynthetic Pathway
7. Applications of WRI1 in Bioengineering of Plant Oil Production
8. Future Perspectives
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Chapman, K.D.; Ohlrogge, J.B. Compartmentation of triacylglycerol accumulation in plants. J. Biol. Chem. 2012, 287, 2288–2294. [Google Scholar] [CrossRef] [PubMed]
- Ohlrogge, J.B.; Chapman, K.D. The seeds of green energy: Expanding the contribution of plant oils as biofuels. Biochemist 2011, 33, 34–38. [Google Scholar] [Green Version]
- Bates, P.D.; Durrett, T.P.; Ohlrogge, J.B.; Pollard, M. Analysis of acyl fluxes through multiple pathways of triacylglycerol synthesis in developing soybean embryos. Plant Physiol. 2009, 150, 55–72. [Google Scholar] [CrossRef] [PubMed]
- Dahlqvist, A.; Stahl, U.; Lenman, M.; Banas, A.; Lee, M.; Sandager, L.; Ronne, H.; Stymne, S. Phospholipid:diacylglycerol acyltransferase: An enzyme that catalyzes the acyl-CoA-independent formation of triacylglycerol in yeast and plants. Proc. Natl. Acad. Sci. USA 2000, 97, 6487–6492. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, M.; Fan, J.; Taylor, D.C.; Ohlrogge, J.B. DGAT1 and PDAT1 acyltransferases have overlapping functions in Arabidopsis triacylglycerol biosynthesis and are essential for normal pollen and seed development. Plant Cell 2009, 21, 3885–3901. [Google Scholar] [CrossRef] [PubMed]
- Zou, J.; Wei, Y.; Jako, C.; Kumar, A.; Selvaraj, G.; Taylor, D.C. The Arabidopsis thaliana TAG1 mutant has a mutation in a diacylglycerol acyltransferase gene. Plant J. 1999, 19, 645–653. [Google Scholar] [CrossRef] [PubMed]
- Focks, N.; Benning, C. wrinkled1: A novel, low-seed-oil mutant of Arabidopsis with a deficiency in the seed-specific regulation of carbohydrate metabolism. Plant Physiol. 1998, 118, 91–101. [Google Scholar] [CrossRef]
- Cernac, A.; Benning, C. WRINKLED1 encodes an AP2/EREB domain protein involved in the control of storage compound biosynthesis in Arabidopsis. Plant J. 2004, 40, 575–585. [Google Scholar] [CrossRef] [PubMed]
- Masaki, T.; Mitsui, N.; Tsukagoshi, H.; Nishii, T.; Morikami, A.; Nakamura, K. ACTIVATOR of Spomin::LUC1/WRINKLED1 of Arabidopsis thaliana transactivates sugar-inducible promoters. Plant Cell Physiol. 2005, 46, 547–556. [Google Scholar] [CrossRef]
- Ruuska, S.A.; Girke, T.; Benning, C.; Ohlrogge, J.B. Contrapuntal networks of gene expression during Arabidopsis seed filling. Plant Cell 2002, 14, 1191–1206. [Google Scholar] [CrossRef]
- Baud, S.; Mendoza, M.S.; To, A.; Harscoet, E.; Lepiniec, L.; Dubreucq, B. WRINKLED1 specifies the regulatory action of LEAFY COTYLEDON2 towards fatty acid metabolism during seed maturation in Arabidopsis. Plant J. 2007, 50, 825–838. [Google Scholar] [CrossRef] [PubMed]
- Maeo, K.; Tokuda, T.; Ayame, A.; Mitsui, N.; Kawai, T.; Tsukagoshi, H.; Ishiguro, S.; Nakamura, K. An AP2-type transcription factor, WRINKLED1, of Arabidopsis thaliana binds to the AW-box sequence conserved among proximal upstream regions of genes involved in fatty acid synthesis. Plant J. 2009, 60, 476–487. [Google Scholar] [CrossRef] [PubMed]
- Casson, S.A.; Lindsey, K. The turnip mutant of Arabidopsis reveals that LEAFY COTYLEDON1 expression mediates the effects of auxin and sugars to promote embryonic cell identity. Plant Physiol. 2006, 142, 526–541. [Google Scholar] [CrossRef] [PubMed]
- Mu, J.; Tan, H.; Zheng, Q.; Fu, F.; Liang, Y.; Zhang, J.; Yang, X.; Wang, T.; Chong, K.; Wang, X.J.; et al. LEAFY COTYLEDON1 is a key regulator of fatty acid biosynthesis in Arabidopsis. Plant Physiol. 2008, 148, 1042–1054. [Google Scholar] [CrossRef] [PubMed]
- Marchive, C.; Nikovics, K.; To, A.; Lepiniec, L.; Baud, S. Transcriptional regulation of fatty acid production in higher plants: Molecular bases and biotechnological outcomes. Eur. J. Lipid Sci. Technol. 2014, 116, 1332–1343. [Google Scholar]
- Santos-Mendoza, M.; Dubreucq, B.; Baud, S.; Parcy, F.; Caboche, M.; Lepiniec, L. Deciphering gene regulatory networks that control seed development and maturation in Arabidopsis. Plant J. 2008, 54, 608–620. [Google Scholar] [CrossRef] [PubMed]
- Manan, S.; Ahmad, M.Z.; Zhang, G.; Chen, B.; Haq, B.U.; Yang, J.; Zhao, J. Soybean LEC2 Regulates Subsets of Genes Involved in Controlling the Biosynthesis and Catabolism of Seed Storage Substances and Seed Development. Front. Plant Sci. 2017, 8, 1604. [Google Scholar] [CrossRef] [PubMed]
- Shen, B.; Allen, W.B.; Zheng, P.; Li, C.; Glassman, K.; Ranch, J.; Nubel, D.; Tarczynski, M.C. Expression of ZmLEC1 and ZmWRI1 increases seed oil production in maize. Plant Physiol. 2010, 153, 980–987. [Google Scholar] [CrossRef] [PubMed]
- Pelletier, J.M.; Kwong, R.W.; Park, S.; Le, B.H.; Baden, R.; Cagliari, A.; Hashimoto, M.; Munoz, M.D.; Fischer, R.L.; Goldberg, R.B.; et al. LEC1 sequentially regulates the transcription of genes involved in diverse developmental processes during seed development. Proc. Natl. Acad. Sci. USA 2017, 114, E6710–E6719. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yamamoto, A.; Kagaya, Y.; Usui, H.; Hobo, T.; Takeda, S.; Hattori, T. Diverse roles and mechanisms of gene regulation by the Arabidopsis seed maturation master regulator FUS3 revealed by microarray analysis. Plant Cell Physiol. 2010, 51, 2031–2046. [Google Scholar] [CrossRef] [PubMed]
- Wang, F.; Perry, S.E. Identification of direct targets of FUSCA3, a key regulator of Arabidopsis seed development. Plant Physiol. 2013, 161, 1251–1264. [Google Scholar] [CrossRef] [PubMed]
- Zhang, M.; Cao, X.; Jia, Q.; Ohlrogge, J. FUSCA3 activates triacylglycerol accumulation in Arabidopsis seedlings and tobacco BY2 cells. Plant J. 2016, 88, 95–107. [Google Scholar] [CrossRef]
- Bourgis, F.; Kilaru, A.; Cao, X.; Ngando-Ebongue, G.F.; Drira, N.; Ohlrogge, J.B.; Arondel, V. Comparative transcriptome and metabolite analysis of oil palm and date palm mesocarp that differ dramatically in carbon partitioning. Proc. Natl. Acad. Sci. USA 2011, 108, 12527–12532. [Google Scholar] [CrossRef] [Green Version]
- Yeap, W.C.; Lee, F.C.; Shabari Shan, D.K.; Musa, H.; Appleton, D.R.; Kulaveerasingam, H. WRI1-1, ABI5, NF-YA3 and NF-YC2 increase oil biosynthesis in coordination with hormonal signaling during fruit development in oil palm. Plant J. 2017, 91, 97–113. [Google Scholar] [CrossRef]
- Li, D.; Jin, C.; Duan, S.; Zhu, Y.; Qi, S.; Liu, K.; Gao, C.; Ma, H.; Zhang, M.; Liao, Y.; et al. MYB89 Transcription Factor Represses Seed Oil Accumulation. Plant Physiol. 2017, 173, 1211–1225. [Google Scholar] [CrossRef]
- Chen, L.; Lee, J.H.; Weber, H.; Tohge, T.; Witt, S.; Roje, S.; Fernie, A.R.; Hellmann, H. Arabidopsis BPM Proteins Function as Substrate Adaptors to a CULLIN3-Based E3 Ligase to Affect Fatty Acid Metabolism in Plants. Plant Cell 2013, 25, 2253–2264. [Google Scholar] [CrossRef] [Green Version]
- Valsecchi, I.; Guittard-Crilat, E.; Maldiney, R.; Habricot, Y.; Lignon, S.; Lebrun, R.; Miginiac, E.; Ruelland, E.; Jeannette, E.; Lebreton, S. The intrinsically disordered C-terminal region of Arabidopsis thaliana TCP8 transcription factor acts both as a transactivation and self-assembly domain. Mol. Biosyst. 2013, 9, 2282–2295. [Google Scholar] [CrossRef]
- Dyson, H.J.; Wright, P.E. Intrinsically unstructured proteins and their functions. Nat. Rev. Mol. Cell Biol. 2005, 6, 197–208. [Google Scholar] [CrossRef]
- Kragelund, B.B.; Jensen, M.K.; Skriver, K. Order by disorder in plant signaling. Trends Plant Sci. 2012, 17, 625–632. [Google Scholar] [CrossRef]
- Ma, W.; Kong, Q.; Grix, M.; Mantyla, J.J.; Yang, Y.; Benning, C.; Ohlrogge, J.B. Deletion of a C-terminal intrinsically disordered region of WRINKLED1 affects its stability and enhances oil accumulation in Arabidopsis. Plant J. 2015, 83, 864–874. [Google Scholar] [CrossRef]
- Ma, W.; Kong, Q.; Mantyla, J.J.; Yang, Y.; Ohlrogge, J.B.; Benning, C. 14-3-3 protein mediates plant seed oil biosynthesis through interaction with AtWRI1. Plant J. 2016, 88, 228–235. [Google Scholar] [CrossRef] [Green Version]
- Kong, Q.; Ma, W. WRINKLED1 as a novel 14-3-3 client: Function of 14-3-3 proteins in plant lipid metabolism. Plant Signal. Behav. 2018, 13, e1482176. [Google Scholar] [CrossRef] [PubMed]
- Zhai, Z.; Liu, H.; Shanklin, J. Phosphorylation of WRINKLED1 by KIN10 Results in Its Proteasomal Degradation, Providing a Link between Energy Homeostasis and Lipid Biosynthesis. Plant Cell 2017, 29, 871–889. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhai, Z.; Keereetaweep, J.; Liu, H.; Feil, R.; Lunn, J.E.; Shanklin, J. Trehalose 6-Phosphate Positively Regulates Fatty Acid Synthesis by Stabilizing WRINKLED1. Plant Cell 2018, 30, 2616–2627. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhai, Z.; Liu, H.; Xu, C.; Shanklin, J. Sugar Potentiation of Fatty Acid and Triacylglycerol Accumulation. Plant Physiol. 2017, 175, 696–707. [Google Scholar] [CrossRef] [PubMed]
- Kim, M.J.; Jang, I.C.; Chua, N.H. The Mediator Complex MED15 Subunit Mediates Activation of Downstream Lipid-Related Genes by the WRINKLED1 Transcription Factor. Plant Physiol. 2016, 171, 1951–1964. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Grimberg, A.; Carlsson, A.S.; Marttila, S.; Bhalerao, R.; Hofvander, P. Transcriptional transitions in Nicotiana benthamiana leaves upon induction of oil synthesis by WRINKLED1 homologs from diverse species and tissues. BMC Plant Biol. 2015, 15, 192. [Google Scholar] [CrossRef] [PubMed]
- Liu, J.; Hua, W.; Zhan, G.; Wei, F.; Wang, X.; Liu, G.; Wang, H. Increasing seed mass and oil content in transgenic Arabidopsis by the overexpression of wri1-like gene from Brassica napus. Plant Physiol. Biochem. 2010, 48, 9–15. [Google Scholar] [CrossRef]
- Yang, Y.; Munz, J.; Cass, C.; Zienkiewicz, A.; Kong, Q.; Ma, W.; Sedbrook, J.; Benning, C. Ectopic Expression of WRINKLED1 Affects Fatty Acid Homeostasis in Brachypodium distachyon Vegetative Tissues. Plant Physiol. 2015, 169, 1836–1847. [Google Scholar] [CrossRef]
- An, D.; Kim, H.; Ju, S.; Go, Y.S.; Kim, H.U.; Suh, M.C. Expression of Camelina WRINKLED1 Isoforms Rescue the Seed Phenotype of the Arabidopsis wri1 Mutant and Increase the Triacylglycerol Content in Tobacco Leaves. Front. Plant Sci. 2017, 8, 34. [Google Scholar] [CrossRef] [Green Version]
- Sun, R.; Ye, R.; Gao, L.; Zhang, L.; Wang, R.; Mao, T.; Zheng, Y.; Li, D.; Lin, Y. Characterization and Ectopic Expression of CoWRI1, an AP2/EREBP Domain-Containing Transcription Factor from Coconut (Cocos nucifera L.) Endosperm, Changes the Seeds Oil Content in Transgenic Arabidopsis thaliana and Rice (Oryza sativa L.). Front. Plant Sci. 2017, 8, 63. [Google Scholar] [CrossRef]
- Ma, W.; Kong, Q.; Arondel, V.; Kilaru, A.; Bates, P.D.; Thrower, N.A.; Benning, C.; Ohlrogge, J.B. Wrinkled1, a ubiquitous regulator in oil accumulating tissues from Arabidopsis embryos to oil palm mesocarp. PLoS ONE 2013, 8, e68887. [Google Scholar] [CrossRef]
- Zhang, D.; Zhao, M.; Li, S.; Sun, L.; Wang, W.; Cai, C.; Dierking, E.C.; Ma, J. Plasticity and innovation of regulatory mechanisms underlying seed oil content mediated by duplicated genes in the palaeopolyploid soybean. Plant J. 2017, 90, 1120–1133. [Google Scholar] [CrossRef] [Green Version]
- Qu, J.; Ye, J.; Geng, Y.F.; Sun, Y.W.; Gao, S.Q.; Zhang, B.P.; Chen, W.; Chua, N.H. Dissecting functions of KATANIN and WRINKLED1 in cotton fiber development by virus-induced gene silencing. Plant Physiol. 2012, 160, 738–748. [Google Scholar] [CrossRef]
- Ye, J.; Wang, C.; Sun, Y.; Qu, J.; Mao, H.; Chua, N.H. Overexpression of a Transcription Factor Increases Lipid Content in a Woody Perennial Jatropha curcas. Front. Plant Sci. 2018, 9, 1479. [Google Scholar] [CrossRef] [Green Version]
- Kilaru, A.; Cao, X.; Dabbs, P.B.; Sung, H.J.; Rahman, M.M.; Thrower, N.; Zynda, G.; Podicheti, R.; Ibarra-Laclette, E.; Herrera-Estrella, L.; et al. Oil biosynthesis in a basal angiosperm: Transcriptome analysis of Persea Americana mesocarp. BMC Plant Biol. 2015, 15, 203. [Google Scholar] [CrossRef]
- Tajima, D.; Kaneko, A.; Sakamoto, M.; Ito, Y.; Hue, N.T.; Miyazaki, M.; Ishibashi, Y.; Yuasa, T.; Iwaya-Inoue, M. Wrinkled 1 (WRI1) Homologs, AP2-Type Transcription Factors Involving Master Regulation of Seed Storage Oil Synthesis in Castor Bean (Ricinus communis L.). Am. J. Plant Sci. 2013, 4, 333–339. [Google Scholar] [CrossRef]
- Pouvreau, B.; Baud, S.; Vernoud, V.; Morin, V.; Py, C.; Gendrot, G.; Pichon, J.P.; Rouster, J.; Paul, W.; Rogowsky, P.M. Duplicate maize Wrinkled1 transcription factors activate target genes involved in seed oil biosynthesis. Plant Physiol. 2011, 156, 674–686. [Google Scholar] [CrossRef]
- Kong, Q.; Ma, W. WRINKLED1 transcription factor: How much do we know about its regulatory mechanism? Plant Sci. 2018, 272, 153–156. [Google Scholar] [CrossRef]
- Tang, T.; Du, C.; Song, H.; Aziz, U.; Wang, L.; Zhao, C.; Zhang, M. Genome-wide analysis reveals the evolution and structural features of WRINKLED1 in plants. Mol. Genet. Genom. 2019, 294, 329–341. [Google Scholar] [CrossRef]
- Kong, Q.; Ma, W.; Yang, H.; Ma, G.; Mantyla, J.J.; Benning, C. The Arabidopsis WRINKLED1 transcription factor affects auxin homeostasis in roots. J. Exp. Bot. 2017, 68, 4627–4634. [Google Scholar] [CrossRef] [Green Version]
- Shen, S.L.; Yin, X.R.; Zhang, B.; Xie, X.L.; Jiang, Q.; Grierson, D.; Chen, K.S. CitAP2.10 activation of the terpene synthase CsTPS1 is associated with the synthesis of (+)-valencene in ‘Newhall’ orange. J. Exp. Bot. 2016, 67, 4105–4115. [Google Scholar] [CrossRef]
- An, D.; Suh, M.C. Overexpression of Arabidopsis WRI1 enhanced seed mass and storage oil content in Camelina sativa. Plant Biotechnol. Rep. 2015, 9, 137–148. [Google Scholar] [CrossRef]
- Durrett, T.P.; Weise, S.E.; Benning, C. Increasing the energy density of vegetative tissues by diverting carbon from starch to oil biosynthesis in transgenic Arabidopsis. Plant Biotechnol. J. 2011, 9, 874–883. [Google Scholar] [CrossRef]
- Kanai, M.; Mano, S.; Kondo, M.; Hayashi, M.; Nishimura, M. Extension of oil biosynthesis during the mid-phase of seed development enhances oil content in Arabidopsis seeds. Plant Biotechnol. J. 2016, 14, 1241–1250. [Google Scholar] [CrossRef]
- Vanhercke, T.; El Tahchy, A.; Shrestha, P.; Zhou, X.R.; Singh, S.P.; Petrie, J.R. Synergistic effect of WRI1 and DGAT1 coexpression on triacylglycerol biosynthesis in plants. FEBS Lett. 2013, 587, 364–369. [Google Scholar] [CrossRef] [Green Version]
- Li, Q.T.; Lu, X.; Song, Q.X.; Chen, H.W.; Wei, W.; Tao, J.J.; Bian, X.H.; Shen, M.; Ma, B.; Zhang, W.K.; et al. Selection for a Zinc-Finger Protein Contributes to Seed Oil Increase during Soybean Domestication. Plant Physiol. 2017, 173, 2208–2224. [Google Scholar] [CrossRef] [Green Version]
- Zhang, Y.Q.; Lu, X.; Zhao, F.Y.; Li, Q.T.; Niu, S.L.; Wei, W.; Zhang, W.K.; Ma, B.; Chen, S.Y.; Zhang, J.S. Soybean GmDREBL Increases Lipid Content in Seeds of Transgenic Arabidopsis. Sci. Rep. 2016, 6, 34307. [Google Scholar] [CrossRef]
- Zhu, Y.; Xie, L.; Chen, G.Q.; Lee, M.Y.; Loque, D.; Scheller, H.V. A transgene design for enhancing oil content in Arabidopsis and Camelina seeds. Biotechnol. Biofuels 2018, 11, 46. [Google Scholar] [CrossRef]
- Bates, P.D.; Browse, J. The pathway of triacylglycerol synthesis through phosphatidylcholine in Arabidopsis produces a bottleneck for the accumulation of unusual fatty acids in transgenic seeds. Plant J. 2011, 68, 387–399. [Google Scholar] [CrossRef]
- Bates, P.D.; Johnson, S.R.; Cao, X.; Li, J.; Nam, J.W.; Jaworski, J.G.; Ohlrogge, J.B.; Browse, J. Fatty acid synthesis is inhibited by inefficient utilization of unusual fatty acids for glycerolipid assembly. Proc. Natl. Acad. Sci. USA 2014, 111, 1204–1209. [Google Scholar] [CrossRef] [Green Version]
- Adhikari, N.D.; Bates, P.D.; Browse, J. WRINKLED1 Rescues Feedback Inhibition of Fatty Acid Synthesis in Hydroxylase-Expressing Seeds. Plant Physiol. 2016, 171, 179–191. [Google Scholar] [CrossRef]
- Liu, H.; Zhai, Z.; Kuczynski, K.; Keereetaweep, J.; Schwender, J.; Shanklin, J. WRINKLED1 regulates BIOTIN ATTACHMENT DOMAIN-CONTAINING proteins that inhibit fatty acid synthesis. Plant Physiol. 2019. [Google Scholar] [CrossRef]
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Kong, Q.; Yuan, L.; Ma, W. WRINKLED1, a “Master Regulator” in Transcriptional Control of Plant Oil Biosynthesis. Plants 2019, 8, 238. https://doi.org/10.3390/plants8070238
Kong Q, Yuan L, Ma W. WRINKLED1, a “Master Regulator” in Transcriptional Control of Plant Oil Biosynthesis. Plants. 2019; 8(7):238. https://doi.org/10.3390/plants8070238
Chicago/Turabian StyleKong, Que, Ling Yuan, and Wei Ma. 2019. "WRINKLED1, a “Master Regulator” in Transcriptional Control of Plant Oil Biosynthesis" Plants 8, no. 7: 238. https://doi.org/10.3390/plants8070238