Selection for a zinc-finger protein contributes to seed oil increase during soybean domestication

Plant Physiology

Volumn 173, Issue 4, 2017, Pages 2208-2224

  Li, Qing Tian ^a,b   Lu, Xiang ^a,b   Song, Qing Xin ^a,b   Chen, Hao Wei ^a,b   Wei, Wei ^a,b   Tao, Jian Jun ^a,b   Bian, Xiao Hua ^a,b   Shen, Ming ^a,b   Ma, Biao ^a,b   Zhang, Wan Ke ^a,b   Bi, Ying Dong ^c   Li, Wei ^c   Lai, Yong Cai ^c   Lam, Sin Man ^a   Shui, Guang Hou ^a   Chen, Shou Yi ^a,b   Zhang, Jin Song ^a,b  

^a INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

[No Author keywords available]

Indexed keywords

FATTY ACID; LIPID; PLANT PROTEIN; TRIACYLGLYCEROL; VEGETABLE OIL; ZINC FINGER PROTEIN;

AMINO ACID SEQUENCE; ARABIDOPSIS; BIOSYNTHESIS; CLASSIFICATION; DOMESTICATION; GENE EXPRESSION REGULATION; GENETICS; LIPID METABOLISM; METABOLISM; PHYLOGENY; PHYSIOLOGY; PLANT SEED; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY; SOYBEAN; TRANSGENIC PLANT;

AMINO ACID SEQUENCE; ARABIDOPSIS; DOMESTICATION; FATTY ACIDS; GENE EXPRESSION REGULATION, PLANT; LIPID METABOLISM; LIPIDS; PHYLOGENY; PLANT OILS; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEEDS; SEQUENCE HOMOLOGY, AMINO ACID; SOYBEANS; TRIGLYCERIDES; ZINC FINGERS;

EID: 85016519497     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.16.01610     Document Type: Article

References (63)

1. Andre C, Froehlich JE, Moll MR, Benning C (2007) A heteromeric plastidic pyruvate kinase complex involved in seed oil biosynthesis in Arabidopsis. Plant Cell 19: 2006-2022.
2. Angeles-Nunez JG, Tiessen A (2010) Arabidopsis sucrose synthase 2 and 3 modulate metabolic homeostasis and direct carbon towards starch synthesis in developing seeds. Planta 232: 701-718.
3. Baud S, Lepiniec L (2009) Regulation of de novo fatty acid synthesis in maturing oilseeds of Arabidopsis. Plant Physiol Biochem 47: 448-455.
4. Baud S, Lepiniec L (2010) Physiological and developmental regulation of seed oil production. Prog Lipid Res 49: 235-249.
5. Baud S, Mendoza MS, To A, Harscoet E, Lepiniec L, Dubreucq B (2007) WRINKLED1 specifies the regulatory action of LEAFY COTYLEDON2 towards fatty acid metabolism during seed maturation in Arabidopsis. Plant J 50: 825-838.
6. Baud S, Wuilleme 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.
7. Bellaloui N, Bruns HA, Abbas HK, Mengistu A, Fisher DK, Reddy KN (2015) Agricultural practices altered soybean seed protein, oil, fatty acids, sugars, and minerals in the midsouth USA. Front Plant Sci 6: 31
8. Bogamuwa S, Jang JC (2013) The Arabidopsis tandem CCCH zinc finger proteins AtTZF4, 5 and 6 are involved in light-, abscisic acid-and gibberellic acid-mediated regulation of seed germination. Plant Cell Environ 36: 1507-1519.
9. Cernac A, Benning C (2004) WRINKLED1 encodes an AP2/EREB domain protein involved in the control of storage compound biosynthesis in Arabidopsis. Plant J 40: 575-585.
10. Chai G, Kong Y, Zhu M, Yu L, Qi G, Tang X, Wang Z, Cao Y, Yu C, Zhou G (2015) Arabidopsis C3H14 and C3H15 have overlapping roles in the regulation of secondary wall thickening and anther development. J Exp Bot 66: 2595-2609.
11. Chen LY, Lee JH, Weber H, Tohge T, Witt S, Roje S, Fernie AR, Hellmann H (2013) Arabidopsis BPM proteins function as substrate adaptors to a CULLIN3-based E3 ligase to affect fatty acid metabolism in plants. Plant Cell 25: 2253-2264.
12. Chen M, Wang Z, Zhu Y, Li Z, Hussain N, Xuan L, Guo W, Zhang G, Jiang L (2012) The effect of TRANSPARENT TESTA2 on seed fatty acid biosynthesis and tolerance to environmental stresses during young seedling establishment in Arabidopsis. Plant Physiol 160: 1023-1036.
13. Chen M, Zhang B, Li C, Kulaveerasingam H, Chew FT, Yu H (2015) TRANSPARENT TESTA GLABRA1 regulates the accumulation of seed storage reserves in Arabidopsis. Plant Physiol 169: 391-402.
14. Chen R, Jiang H, Li L, Zhai Q, Qi L, Zhou W, Liu X, Li H, Zheng W, Sun J, et al (2012) The Arabidopsis mediator subunit MED25 differentially regulates jasmonate and abscisic acid signaling through interacting with the MYC2 and ABI5 transcription factors. Plant Cell 24: 2898-2916.
15. Dekkers BJW, Willems L, Bassel GW, van Bolderen-Veldkamp RP, Ligterink W, Hilhorst HWM, Bentsink L (2012) Identification of reference genes for RT-qPCR expression analysis in Arabidopsis and tomato seeds. Plant Cell Physiol 53: 28-37.
16. Dong Y, Yang X, Liu J, Wang BH, Liu BL, Wang YZ (2014) Pod shattering resistance associated with domestication is mediated by a NAC gene in soybean. Nat Commun 5: 3352
17. Fehr WR, Caviness CE (1977) Stages of Soybean Development. Agricultural and Home Economics Experiment Station, Iowa State University, Ames, IA
18. Guo J, Wang Y, Song C, Zhou J, Qiu L, Huang H, Wang Y (2010) A single origin and moderate bottleneck during domestication of soybean (Glycine max): implications from microsatellites and nucleotide sequences. Ann Bot (Lond) 106: 505-514.
19. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, Cheng JX, Murre C, Singh H, Glass CK (2010) Simple combinations of lineagedetermining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell 38: 576-589.
20. Kanai M, Mano S, Kondo M, Hayashi M, Nishimura M (2016) Extension of oil biosynthesis during the mid-phase of seed development enhances oil content in Arabidopsis seeds. Plant Biotechnol J 14: 1241-1250.
21. Kim DH, Yamaguchi S, Lim S, Oh E, Park J, Hanada A, Kamiya Y, Choi G (2008) SOMNUS, a CCCH-type zinc finger protein in Arabidopsis, negatively regulates light-dependent seed germination downstream of PIL5. Plant Cell 20: 1260-1277.
22. Kusnetsov V, Landsberger M, Meurer J, Oelmuller R (1999) The assembly of the CAAT-box binding complex at a photosynthesis gene promoter is regulated by light, cytokinin, and the stage of the plastids. J Biol Chem 274: 36009-36014.
23. Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357-359.
24. Li Q, Shao JH, Tang SH, Shen QW, Wang TH, Chen WL, Hong YY (2015) Wrinkled1 accelerates flowering and regulates lipid homeostasis between oil accumulation and membrane lipid anabolism in Brassica napus. Front Plant Sci 6: 1015
25. Li Z, Thomas TL (1998) PEI1, an embryo-specific zinc finger protein gene required for heart-stage embryo formation in Arabidopsis. Plant Cell 10: 383-398.
26. Lin PC, Pomeranz MC, Jikumaru Y, Kang SG, Hah C, Fujioka S, Kamiya Y, Jang JC (2011) The Arabidopsis tandem zinc finger protein AtTZF1 affects ABA-and GA-mediated growth, stress and gene expression responses. Plant J 65: 253-268.
27. Liu WX, Liu HL, Qu LQ (2013) Embryo-specific expression of soybean oleosin altered oil body morphogenesis and increased lipid content in transgenic rice seeds. Theor Appl Genet 126: 2289-2297.
28. Liu YF, Li QT, Lu X, Song QX, Lam SM, Zhang WK, Ma B, Lin Q, Man WQ, Du WG, et al (2014) Soybean GmMYB73 promotes lipid accumulation in transgenic plants. BMC Plant Biol 14: 73
29. Lu X, Li QT, Xiong Q, Li W, Bi YD, Lai YC, Liu XL, Man WQ, Zhang WK, Ma B, et al (2016) The transcriptomic signature of developing soybean seeds reveals genetic basis of seed trait adaptation during domestication. Plant J 86: 530-544.
30. Ma W, Kong Q, Grix M, Mantyla JJ, Yang Y, Benning C, Ohlrogge JB (2015) Deletion of a C-terminal intrinsically disordered region of WRINKLED1 affects its stability and enhances oil accumulation in Arabidopsis. Plant J 83: 864-874.
31. Ma W, Kong Q, Mantyla JJ, Yang Y, Ohlrogge JB, Benning C (2016) 14-3-3. protein mediates plant seed oil biosynthesis through interaction with AtWRI1. Plant J 88: 228-235.
32. 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.
33. Mendes A, Kelly AA, van Erp H, Shaw E, Powers SJ, Kurup S, Eastmond PJ (2013) bZIP67 regulates the omega-3 fatty acid content of Arabidopsis seed oil by activating fatty acid desaturase3. Plant Cell 25: 3104-3116.
34. Mendoza MS, Dubreucq B, Miquel M, Caboche M, Lepiniec L (2005) LEAFY COTYLEDON 2 activation is sufficient to trigger the accumulation of oil and seed specific mRNAs in Arabidopsis leaves. FEBS Lett 579: 4666-4670.
35. Mu JY, Tan HL, Hong SL, Liang Y, Zuo JR (2013) Arabidopsis transcription factor genes NF-YA1, 5, 6, and 9 play redundant roles in male gametogenesis, embryogenesis, and seed development. Mol Plant 6: 188-201.
36. Mu JY, Tan HL, Zheng Q, Fu FY, Liang Y, Zhang JA, Yang XH, Wang T, Chong K, Wang XJ, et al (2008) LEAFY COTYLEDON1 is a key regulator of fatty acid biosynthesis in Arabidopsis. Plant Physiol 148: 1042-1054
37. Ping JQ, Liu YF, Sun LJ, Zhao MX, Li YH, She MY, Sui Y, Lin F, Liu XD, Tang ZX, et al (2014) Dt2 is a gain-of-function MADS-domain factor gene that specifies semideterminacy in soybean. Plant Cell 26: 2831-2842.
38. Retief JD (2000) Phylogenetic analysis using PHYLIP. Methods Mol Biol 132: 243-258.
39. Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP (2011) Integrative genomics viewer. Nat Biotechnol 29: 24-26.
40. Roscoe TT, Guilleminot J, Bessoule JJ, Berger F, Devic M (2015) Complementation of seed maturation phenotypes by ectopic expression of ABSCISIC ACID INSENSITIVE3, FUSCA3 and LEAFY COTYLEDON2 in Arabidopsis. Plant Cell Physiol 56: 1215-1228.
41. Salman-Minkov A, Sabath N, Mayrose I (2016) Whole-genome duplication as a key factor in crop domestication. Nat Plants 2: 16115
42. 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. Plant J 54: 608-620.
43. Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, et al (2010) Genome sequence of the palaeopolyploid soybean. Nature 463: 178-183.
44. Settlage SB, Kwanyuen P, Wilson RF (1998) Relation between diacylglycerol acyltransferase activity and oil concentration in soybean. J Am Oil Chem Soc 75: 775-781.
45. 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 Physiol 153: 980-987.
46. Shen B, Sinkevicius KW, Selinger DA, Tarczynski MC (2006) The homeobox gene GLABRA2 affects seed oil content in Arabidopsis. Plant Mol Biol 60: 377-387.
47. Song QX, Li QT, Liu YF, Zhang FX, Ma B, Zhang WK, Man WQ, Du WG, Wang GD, Chen SY, et al (2013) Soybean GmbZIP123 gene enhances lipid content in the seeds of transgenic Arabidopsis plants. J Exp Bot 64: 4329-4341.
48. Sun J, Jiang H, Xu Y, Li H, Wu X, Xie Q, Li C (2007) The CCCH-type zinc finger proteins AtSZF1 and AtSZF2 regulate salt stress responses in Arabidopsis. Plant Cell Physiol 48: 1148-1158.
49. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
50. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882.
51. Tian Z, Wang X, Lee R, Li Y, Specht JE, Nelson RL, McClean PE, Qiu L, Ma J (2010) Artificial selection for determinate growth habit in soybean. Proc Natl Acad Sci USA 107: 8563-8568.
52. To A, Joubes J, Barthole G, Lecureuil A, Scagnelli A, Jasinski S, Lepiniec L, Baud S (2012) WRINKLED transcription factors orchestrate tissuespecific regulation of fatty acid biosynthesis in Arabidopsis. Plant Cell 24: 5007-5023.
53. 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.
54. Wang L, Li Q, Lei Q, Feng C, Gao Y, Zheng X, Zhao Y, Wang Z, Kong J (2015) MzPIP2;1: an aquaporin involved in radial water movement in both water uptake and transportation, altered the drought and salt tolerance of transgenic Arabidopsis. PLoS ONE 10: e0142446
55. Wang XH, Li QT, Chen HW, Zhang WK, Ma B, Chen SY, Zhang JS (2014) Trihelix transcription factor GT-4 mediates salt tolerance via interaction with TEM2 in Arabidopsis. BMC Plant Biol 14: 339
56. Wei W, Zhang YQ, Tao JJ, Chen HW, Li QT, Zhang WK, Ma B, Lin Q, Zhang JS, Chen SY (2015) The Alfin-like homeodomain finger protein AL5 suppresses multiple negative factors to confer abiotic stress tolerance in Arabidopsis. Plant J 81: 871-883.
57. Wilson RF (2008) Soybean: market-driven research needs in genetics and genomics. In G Stacey, ed, Genetics and Genomics of Soybean. Springer, New York, pp 3-15.
58. Yu J, Zhang Z, Wei J, Ling Y, Xu W, 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 Genomics 15: 271
59. Zeng P, Vadnais DA, Zhang Z, Polacco JC (2004) Refined glufosinate selection in Agrobacterium-mediated transformation of soybean Glycine max (L.) Merrill. Plant Cell Rep 22: 478-482.
60. Zhang H, Cui F, Wu Y, Lou L, Liu L, Tian M, Ning Y, Shu K, Tang S, Xie Q (2015) The RING finger ubiquitin E3 ligase SDIR1 targets SDIR1-INTERACTING PROTEIN1 for degradation to modulate the salt stress response and ABA signaling in Arabidopsis. Plant Cell 27: 214-227.
61. Zhang J, Hao Q, Bai L, Xu J, Yin W, Song L, Xu L, Guo X, Fan C, Chen Y, et al (2014) Overexpression of the soybean transcription factor GmDof4 significantly enhances the lipid content of Chlorella ellipsoidea. Biotechnol Biofuels 7: 128
62. Zhang L, Wang SB, Li QG, Song J, Hao YQ, Zhou L, Zheng HQ, Dunwell JM, Zhang YM (2016) An integrated bioinformatics analysis reveals divergent evolutionary pattern of oil biosynthesis in high-and low-oil plants. PLoS ONE 11: e0154882
63. Zhou Z, Jiang Y, Wang Z, Gou Z, Lyu J, Li W, Yu Y, Shu L, Zhao Y, Ma Y, et al (2015) Resequencing 302 wild and cultivated accessions identifies genes related to domestication and improvement in soybean. Nat Biotechnol 33: 408-414.