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Soybean (Glycine max) WRINKLED1 transcription factor, GmWRI1a, positively regulates seed oil accumulation

Abstract

Soybean is the world’s most important leguminous crop producing high-quality protein and oil. Elevating oil accumulation in soybean seed is always many researchers’ goal. WRINKLED1 (WRI1) encodes a transcription factor of the APETALA2/ethylene responsive element-binding protein (AP2/EREBP) family that plays important roles during plant seed oil accumulation. In this study, we isolated and characterized three distinct orthologues of WRI1 in soybean (Glycine max) that display different organ-specific expression patterns, among which GmWRI1a was highly expressed in maturing soybean seed. Electrophoretic mobility shift assays and yeast one-hybrid experiments demonstrated that the GmWRI1a protein was capable of binding to AW-box, a conserved sequence in the proximal upstream regions of many genes involved in various steps of oil biosynthesis. Transgenic soybean seeds overexpressing GmWRI1a under the control of the seed-specific napin promoter showed the increased total oil and fatty acid content and the changed fatty acid composition. Furthermore, basing on the activated expressions in transgenic soybean seeds and existence of AW-box element in the promoter regions, direct downstream genes of GmWRI1a were identified, and their products were responsible for fatty acid production, elongation, desaturation and export from plastid. We conclude that GmWRI1a transcription factor can positively regulate oil accumulation in soybean seed by a complex gene expression network related to fatty acid biosynthesis.

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Abbreviations

AP2/EREBP:

APETALA2/ethylene responsive element-binding protein

CaMV:

Cauliflower mosaic virus

DAF:

Days after flowering

EMSA:

Electrophoretic mobility shift assay

FA:

Fatty acid

ORF:

Open reading frame

qRT-PCR:

Quantitative real-time PCR

TAG:

Triacylglycerols

TF:

Transcription factor

WRI:

WRINKLED

References

  1. Bates PD, Stymne S, Ohlrogge J (2013) Biochemical pathways in seed oil synthesis. Curr Opin Plant Biol 16:358–364

  2. Baud S, Lepiniec L (2009) Regulation of de novo fatty acid synthesis in maturing oilseeds of Arabidopsis. Plant Physiol Bioch 47:448–455

  3. Baud S, Wuillème S, To A, Rochat C, Lepiniec L (2009) Role of WRINKLED1 in the transcriptional regulation of glycolytic and fatty acid biosynthetic genes in Arabidopsis. Plant J 60:933–947

  4. Bolton MD, Kolmer JA, Xu WW, Garvin DF (2008) Lr34-mediated leaf rust resistance in wheat: transcript profiling reveals a high energetic demand supported by transient recruitment of multiple metabolic pathways. Mol Plant Microbe In 21:1515–1527

  5. Cagliari A, Margis R, dos Santos MF, Turchetto-Zolet AC, Loss G, Margis-Pinheiro M (2011) Biosynthesis of Triacylglycerols (TAGs) in plants and algae. Int J Plant Biol 2:10

  6. Chai G, Bai Z, Wei F, King GJ, Wang C, Shi L, Dong C, Chen H, Liu S (2010) Brassica GLABRA2 genes: analysis of function related to seed oil content and development of functional markers. Theor Appl Genet 120:1597–1610

  7. Chapman KD, Ohlrogge JB (2012) Compartmentation of triacylglycerol accumulation in plants. J Biol Chem 287:2288–2294

  8. Chen JE, Smith AG (2012) A look at diacylglycerol acyltransferases (DGATs) in algae. J Biotechnol 162:28–39

  9. Chen L, Zhang ZY, Liang HX, Liu HX, Du LP, Xu HJ, Xin ZY (2008) Overexpression of TiERF1 enhances resistance to sharp eyespot in transgenic wheat. J Exp Bot 59:4195–4204

  10. Chen H, Wang FW, Dong YY, Wang N, Sun YP, Li XY, Liu L, Fan XD, Yin HL, Jing YY, Zhang XY, Li YL, Chen G, Li HY (2012) Sequence mining and transcript profiling to explore differentially expressed genes associated with lipid biosynthesis during soybean seed development. BMC Plant Biol 12:1

  11. Clemente TE, Cahoon EB (2009) Soybean oil: genetic approaches for modification of functionality and total content. Plant Physiol 151:1030–1040

  12. Courchesne NMD, Parisien A, Wang B, Lan CQ (2009) Enhancement of lipid production using biochemical, genetic and transcription factor engineering approaches. J Biotechnol 141:31–41

  13. Dussert S, Guerin C, Andersson M, Joët T, Tranbarger TJ, Pizot M, Sarah G, Omore A, Durand-Gasselin T, Morcillo F (2013) Comparative transcriptome analysis of three oil palm fruit and seed tissues that differ in oil content and fatty acid composition. Plant Physiol 162:1337–1358

  14. Eskandari M, Cober ER, Rajcan I (2013) Using the candidate gene approach for detecting genes underlying seed oil concentration and yield in soybean. Theor Appl Genet 126:1839–1850

  15. Gietz RD, Woods RA (2002) Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Method Enzymol 350:87–96

  16. Grotewold E (2008) Transcription factors for predictive plant metabolic engineering: are we there yet? Curr Opin Plant Biol 19:138–144

  17. Hwang EY, 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 Genom 15:1

  18. Ibáñez-Salazar A, Rosales-Mendoza S, Rocha-Uribe A, Ramírez-Alonso JI, Lara-Hernández I, Hernández-Torres A, Paz-Maldonado LMT, Silva-Ramírez AS, Bañuelos-Hernández B, Martínez-Salgado JL, Soria-Guerra RE (2014) Over-expression of Dof-type transcription factor increases lipid production in Chlamydomonas reinhardtii. J Biotechnol 184:27–38

  19. Iwase A, Matsui K, Ohme-Takagi M (2009) Manipulation of plant metabolic pathways by transcription factors. Plant Biotechnol 26:29–38

  20. Jako C, Kumar A, Wei Y, Zou J, Barton DL, Giblin EM, Covello PS, Taylor DC (2001) Seed-specific over-expression of an Arabidopsis cDNA encoding a diacylglycerol acyltransferase enhances seed oil content and seed weight. Plant Physiol 126:861–874

  21. La Russa M, Bogen C, Uhmeyer A, Doebbe A, Filippone E, Kruse O, Mussgnug JH (2012) Functional analysis of three type-2 DGAT homologue genes for triacylglycerol production in the green microalga Chlamydomonas reinhardtii. J Biotechnol 162:13–20

  22. Laibach N, Post J, Twyman RM, Gronover CS, Prüfer D (2015) The characteristics and potential applications of structural lipid droplet proteins in plants. J Biotechnol 201:15–27

  23. Li QT, Lu X, Song QX, Chen HW, Wei W, Tao JJ, Bian XH, Shen M, Ma B, Zhang WK, Bi YD, Li W, Lai YC, Lam SM, Shui GH, Chen SY, Zhang JS (2017) Selection for a zinc-finger protein contributes to seed oil increase during soybean domestication. Plant Physiol 173:2208–2224

  24. Liu J, Hua W, Zhan GM, Wei F, Wang XF, Liu GH, Wang HZ (2010) Increasing seed mass and oil content in transgenic Arabidopsis by the overexpression of wri1-like gene from Brassica napus. Plant Physiol Bioch 48:9–15

  25. Liu J, Hua W, Yang HL, Zhan GM, Li RJ, Deng LB, Wang XF, Liu GH, Wang HZ (2012) The BnGRF2 gene (GRF2-like gene from Brassica napus) enhances seed oil production through regulating cell number and plant photosynthesis. J Exp Bot 63:3727–3740

  26. Liu YF, Li QT, Lu X, Song QX, Lam SM, Zhang WK, Ma B, Lin Q, Man WQ, Du WG, Shui GH, Chen SY (2014) Soybean GmMYB73 promotes lipid accumulation in transgenic plants. BMC Plant Biol 14:73

  27. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−∆∆CT method. Methods 25:402–408

  28. Ma W, Kong Q, Arondel V, Kilaru A, Bates PD, Thrower NA, Benning C, Ohlrogge JB (2013) WRINKLED1, a ubiquitous regulator in oil accumulating tissues from Arabidopsis embryos to oil palm mesocarp. PLoS One 8:e68887

  29. Maeo K, Tokuda T, Ayame A, Mitsui N, Kawai T, Tsukagoshi H, Ishiguro S, Nakamura K (2009) 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 60:476–487

  30. Manan S, Chen B, She G, Wan X, Zhao J (2017) Transport and transcriptional regulation of oil production in plants. Crit Rev Biotechnol 37:641–655

  31. Nölke G, Fischer R, Schillberg S (2006) Antibody-based metabolic engineering in plants. J Biotechnol 124:271–283

  32. Paz MM, Shou HX, Guo ZB, Zhang ZY, Banerjee AK, Wang K (2004) Assessment of conditions affecting Agrobacterium-mediated soybean transformation using the cotyledonary node explant. Euphytica 136:167–179

  33. Pelletier JM, Kwong RW, Park S, Le BH, Baden R, Cagliari A, Hashimoto M, Munoz MD, Fischer RL, Goldberg RB, Harada JJ (2017) LEC1 sequentially regulates the transcription of genes involved in diverse developmental processes during seed development. Proc Natl Acad Sci USA 114:E6710–E6719

  34. Pouvreau B, Baud S, Vernoud V, Morin V, Py C, Gendrot G, Pichon JP, Rouster J, Paul W, Rogowsky PM (2011) Duplicate maize wrinkled1 transcription factors activate target genes involved in seed oil biosynthesis. Plant Physiol 156:674–686

  35. Rachael S, Tang JH (2006) Modification of oil using conventional and transgenic approaches. Crop Sci 46:1225–1236

  36. Sanjaya Durrett TP, Weise SE, Benning C (2011) Increasing the energy density of vegetative tissues by diverting carbon from starch to oil biosynthesis in transgenic Arabidopsis. Plant Biotechnol J 9:874–883

  37. Shen B, Allen WB, Zheng PZ, Li CJ, Glassman K, Ranch J, Nubel D, Tarczynski MC (2010) Expression of ZmLEC1 and ZmWRI1 increases seed oil production in maize. Plant Physiol 153:980–987

  38. Song QX, Li QT, Liu YF, Zhang FX, Ma B, Zhang WK, Man WQ, Du WG, Wang GD, Chen SY, Zhang JS (2013) Soybean GmbZIP123 gene enhances lipid content in the seeds of transgenic Arabidopsis plants. J Exp Bot 64:4329–4341

  39. Stalberg K, Ellerstom M, Ezcurra I, Ablov S, Rask L (1996) Disruption of an overlapping E-box/ABRE motif abolished high transcription of the napA storage-protein promoter in transgenic Brassica napus seeds. Planta 199:515–519

  40. Storey JD, Tibshirani R (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci 100:9440–9445

  41. Tajima D, Kaneko A, Sakamoto M, Ito Y, Hue NT, Miyazaki M, Ishibashi Y, Yuasa T, Iwaya-Inoue M (2013) Wrinkled1 (WRI1) homologs, AP2-type transcription factors involving master regulation of seed storage oil synthesis in castor bean (Ricinus communis L.). Am J Plant Sci 4:333–339

  42. van Erp H, Kelly AA, Menard G, Eastmond PJ (2014) Multigene engineering of triacylglycerol metabolism boosts seed oil content in Arabidopsis. Plant Physiol 165:30–36

  43. 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

  44. Wang HW, Zhang B, Hao YJ, Huang J, Tian AG, Liao Y, Zhang JS, Chen SY (2007) The soybean Dof-type transcription factor genes, GmDof4 and GmDof11, enhance lipid content in the seeds of transgenic Arabidopsis plants. Plant J 52:716–729

  45. Weselake RJ, Taylor DC, Rahman HM, Shah S, Laroche A, McVetty PBE, Harwood JL (2009) Increasing the flow of carbon into seed oil. Biotechnol Adv 27:866–878

  46. Xia W, Mason AS, Xiao Y, Liu Z, Yang Y, Lei X, Wu X, Ma Z, Peng M (2014) Analysis of multiple transcriptomes of the African oil palm (Elaeis guineensis) to identify reference genes for RT-qPCR. J Biotechnol 184:63–73

  47. Yu J, Zhang ZH, Wei JG, Ling Y, Xu WY, Su Z (2014) SFGD: a comprehensive platform for mining functional information from soybean transcriptome data and its use in identifying acyl-lipid metabolism pathways. BMC Genom 15:1

  48. Zhang ZY, Yao WL, Dong N, Liang HX, Liu HX, Huang RF (2007) A novel ERF transcription activator in wheat and its induction kinetics after pathogen and hormone treatments. J Exp Bot 58:2993–3003

  49. Zhang J, Hao Q, Bai L, Xu J, Yin W, Song L, Xu L, Guo X, Fan C, Chen Y, Ruan J, Hao S, Li Y, Wang RR-C, Hu Z (2014) Overexpression of the soybean transcription factor GmDof4 significantly enhances the lipid content of Chlorella ellipsoidea. Biotechnol Biofuels 7:128

  50. Zhang YQ, Lu X, Zhao FY, Li QT, Niu SL, Wei W, Zhang WK, Ma B, Chen SY, Zhang JS (2016) Soybean GmDREBL increases lipid content in seeds of transgenic Arabidopsis. Sci Rep 6:34307

  51. Zhao JY, Huang JX, Chen F, Xu F, Ni XY, Xu HM, Wang YL, Jiang CC, Wang H, Xu AX, Huang RZ, Li DR, Meng JL (2012) Molecular mapping of Arabidopsis thaliana lipid-related orthologous genes in Brassica napus. Theor Appl Genet 124:407–421

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Acknowledgements

The authors thank the Science and Technology Development Program of Jilin Province (Grant No. 20150520121JH), the Special Foundation for Fostering Talents of Jilin Province (2017–2019), the Agricultural Science and Technology Innovation Project of Jilin Province (Grant No. CXGC2017ZY007 & CXGC2017TD018), Modern Agricultural Industry Technology System (Grant No. CARS-004-PS11), the National Natural Science Foundation of China (Grant No. 31301347) and Key Laboratory of Soybean Biology in Northeast Agricultural University (Grant No. SB16A01) for funding this project.

Author information

Correspondence to Zhimin Dong or Shuming Wang.

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The authors declare that they have no conflict of interest.

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This article does not contain any studies with human participants or animals performed by any of the authors.

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Communicated by S. Hohmann.

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Chen, L., Zheng, Y., Dong, Z. et al. Soybean (Glycine max) WRINKLED1 transcription factor, GmWRI1a, positively regulates seed oil accumulation. Mol Genet Genomics 293, 401–415 (2018). https://doi.org/10.1007/s00438-017-1393-2

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Keywords

  • Soybean (Glycine max)
  • Seed oil
  • WRI1
  • AP2/EREBP transcription factor
  • Fatty acid biosynthesis
  • Transcriptional machinery