DELLA Proteins Promote Anthocyanin Biosynthesis via Sequestering MYBL2 and JAZ Suppressors of the MYB/bHLH/WD40 Complex in Arabidopsis thaliana

Molecular Plant

Volumn 9, Issue 5, 2016, Pages 711-721

  Xie, Ye ^a,b   Tan, Huijuan ^a,b   Ma, Zhaoxue ^a,b   Huang, Jirong ^a  

^a INSTITUTE OF PLANT PHYSIOLOGY AND ECOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

abiotic stresses; anthocyanin biosynthesis; DELLA; JAZ; MYBL2

Indexed keywords

ANTHOCYANIN; ARABIDOPSIS PROTEIN; ATMYBL2 PROTEIN, ARABIDOPSIS; DNA BINDING PROTEIN; GAI PROTEIN, ARABIDOPSIS; GIBBERELLIC ACID; GIBBERELLIN; REPRESSOR PROTEIN; TRANSCRIPTION FACTOR;

ARABIDOPSIS; BIOSYNTHESIS; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM;

ANTHOCYANINS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, PLANT; GIBBERELLINS; REPRESSOR PROTEINS; TRANSCRIPTION FACTORS;

EID: 84966564942     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1016/j.molp.2016.01.014     Document Type: Article

References (55)

1. P. Achard, F. Gong, S. Cheminant, M. Alioua, P. Hedden, and P. Genschik The cold-inducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism Plant Cell 20 2008 2117 2129
2. P. Achard, J.P. Renou, R. Berthomé, N.P. Harberd, and P. Genschik Plant DELLAs restrain growth and promote survival of adversity by reducing the levels of reactive oxygen species Curr. Biol. 18 2008 656 660
3. N.W. Albert, K.M. Davies, D.H. Lewis, H. Zhang, M. Montefiori, C. Brendolise, M.R. Boase, H. Ngo, P.E. Jameson, and K.E. Schwinn A conserved network of transcriptional activators and repressors regulates anthocyanin pigmentation in eudicots Plant Cell 26 2014 962 980
4. J.O. Borevitz, Y. Xia, J. Blount, R.A. Dixon, and C. Lamb Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis Plant Cell 12 2000 2383 2394
5. P. Broun Transcriptional control of flavonoid biosynthesis: a complex network of conserved regulators involved in multiple aspects of differentiation in Arabidopsis Curr. Opin. Plant Biol. 8 2005 272 279
6. E. Butelli, L. Titta, M. Giorgio, H.P. Mock, A. Matros, S. Peterek, E.G. Schijlen, R.D. Hall, A.G. Bovy, J. Luo, and et al. Enrichment of tomato fruit with health-promoting anthocyanins by expression of select transcription factors Nat. Biotechnol. 26 2008 1301 1308
7. H. Claeys, S. De Bodt, and D. Inzé Gibberellins and DELLAs: central nodes in growth regulatory networks Trends Plant Sci. 19 2014 231 239
8. S.J. Clough, and A.F. Bent Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana Plant J. 16 1998 735 743
9. E.H. Colebrook, S.G. Thomas, A.L. Phillips, and P. Hedden The role of gibberellin signaling in plant responses to abiotic stress J. Exp. Biol. 217 2014 67 75
10. P.K. Das, D.H. Shin, S.B. Choi, and Y.I. Park Sugar-hormone cross-talk in anthocyanin biosynthesis Mol. Cells 34 2012 501 507
11. J.M. Davière, and P. Achard Gibberellin signaling in plants Development 140 2013 1147 1151
12. A. Dill, H.S. Jung, and T.P. Sun The DELLA motif is essential for gibberellin-induced degradation of RGA Proc. Natl. Acad. Sci. USA 98 2001 14162 14167
13. C. Dubos, J. Le Gourrierec, A. Baudry, G. Huep, E. Lanet, I. Debeaujon, J.M. Routaboul, A. Alboresi, B. Weisshaar, and L. Lepiniec MYBL2 is a new regulator of flavonoid biosynthesis in Arabidopsis thaliana Plant J. 55 2008 940 953
14. R.A. Dixon, and N.L. Paiva Stress-induced phenylpropanoid metabolism Plant Cell 7 1995 1085 1097
15. R.A. Dixon, C. Liu, and J.H. Jun Metabolic engineering of anthocyanins and condensed tannins in plants Curr. Opin. Biotechnol. 24 2013 329 335
16. D.N. Feyissa, T. Løvdal, K.M. Olsen, R. Slimestad, and C. Lillo The endogenous GL3, but not EGL3, gene is necessary for anthocyanin accumulation as induced by nitrogen depletion in Arabidopsis rosette stage leaves Planta 230 2009 747 754
17. S. Feng, C. Martinez, G. Gusmaroli, Y. Wang, J. Zhou, F. Wang, L. Chen, L. Yu, J.M. Iglesias-Pedraz, S. Kircher, and et al. Coordinated regulation of Arabidopsis thaliana development by light and gibberellins Nature 451 2008 475 479
18. Y. Gan, H. Li, Y. Xie, W. Wu, M. Li, X. Wang, and J. Huang THF1 mutations lead to increased basal and wound-induced levels of oxylipins that stimulate anthocyanin biosynthesis via COI1 signaling in Arabidopsis J. Integr. Plant Biol. 56 2014 916 927
19. J. Gou, F.F. Felippes, C. Liu, D. Weigel, and J. Wang Negative regulation of anthocyanin biosynthesis in Arabidopsis by a miR156-targeted SPL transcription factor Plant Cell 23 2011 1512 1522
20. A. Gonzalez, M.Z. Zhao, J.M. Leavitt, and A.M. Lloyd Regulation of the anthocyanin biosynthetic pathway by TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings Plant J. 53 2008 814 827
21. R. Hopkins, and M.D. Rausher Identification of two genes causing reinforcement in the Texas wildflower Phlox drummondii Nature 469 2011 411 414
22. X. Hou, L.Y. Lee, K. Xia, Y. Yan, and H. Yu DELLAs modulate jasmonate signaling via competitive binding to JAZs Dev. Cell. 19 2010 884 894
23. X. Hou, Li. Ding, and H. Yu Crosstalk between GA and JA signaling mediates plant growth and defense Plant Cell Rep. 32 2013 1067 1074
24. L. Jaakola New insights into the regulation of anthocyanin biosynthesis in fruits Trends Plant Sci. 18 2013 477 483
25. C. Jiang, X. Gao, L. Liao, N.P. Harberd, and X. Fu Phosphate starvation root architecture and anthocyanin accumulation responses are modulated by the gibberellin-DELLA signaling pathway in Arabidopsis Plant Physiol. 145 2007 1460 1470
26. Y. Li, W. Van den Ende, and F. Rolland Sucrose induction of anthocyanin biosynthesis is mediated by DELLA Mol. Plant 7 2013 570 572
27. T. Li, K.P. Jia, H.L. Lian, X. Yang, L. Li, and H.Q. Yang Jasmonic acid enhancement of anthocyanin accumulation is dependent on phytochrome A signaling pathway under far-red light in Arabidopsis Biochem. Biophys. Res. Commun. 454 2014 78 83
28. H. Liu, X. Yu, K. Li, J. Klejnot, H. Yang, D. Lisiero, and C. Lin Photoexcited CRY2 interacts with CIB1 to regulate transcription and floral initiation in Arabidopsis Science 322 2008 1535 1539
29. K. Lorenc-Kukuła, S. Jafra, J. Oszmiañski, and J. Szopa Ectopic expression of anthocyanin 5-O-glucosyltransferase in potato tuber causes increased resistance to bacteria J. Agric. Food Chem. 53 2005 272 281
30. E. Loreti, G. Povero, G. Novi, C. Solfanelli, A. Alpi, and P. Perata Gibberellins, jasmonate and abscisic acid modulate the sucrose-induced expression of anthocyanin biosynthetic genes in Arabidopsis New Phytol. 179 2008 1004 1016
31. Z. Ma, X. Hu, W. Cai, W. Huang, X. Zhou, Q. Luo, H. Yang, J. Wang, and J. Huang Arabidopsis miR171-targeted scarecrow-like proteins bind to GT cis-elements and mediate gibberellin-regulated chlorophyll biosynthesis under light conditions PLos Genet. 10 2014 e1004519
32. K. Matsui, Y. Umemura, and M. Ohme-Takagi AtMYBL2, a protein with a single MYB domain, acts as a negative regulator of anthocyanin biosynthesis in Arabidopsis Plant J. 55 2008 954 967
33. K. Morohashi, and E. Grotewold A systems approach reveals regulatory circuitry for Arabidopsis trichome initiation by the GL3 and GL1 selectors PLoS Genet. 5 2009 e1000396
34. K. Murase, Y. Hirano, T.P. Sun, and T. Hakoshima Gibberellin-induced DELLA recognition by the gibberellin receptor GID1 Nature 456 2008 459 463
35. R. Nakabayashi, K. Yonekura-Sakakibara, K. Urano, M. Suzuki, Y. Yamada, T. Nishizawa, F. Matsuda, M. Kojima, H. Sakakibara, K. Shinozaki, and et al. Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids Plant J. 77 2014 367 379
36. N. Nesi, C. Jond, I. Debeaujon, M. Caboche, and L. Lepiniec The TT8 gene encodes a basic helix-loop-helix domain protein required for expression of DFR and BAN genes in Arabidopsis siliques Plant Cell 12 2000 1863 1878
37. T. Qi, S. Song, Q. Ren, D. Wu, H. Huang, Y. Chen, M. Fan, W. Peng, C. Ren, and D. Xie The Jasmonate-ZIM-domain proteins interact with the WD-Repeat/bHLH/MYB complexes to regulate jasmonate-mediated anthocyanin accumulation and trichome initiation in Arabidopsis thaliana Plant Cell 23 2011 1795 1814
38. T. Qi, H. Huang, D. Wu, J. Yan, Y. Qi, S. Song, and D. Xie Arabidopsis DELLA and JAZ proteins bind the WD-repeat/bHLH/MYB complex to modulate gibberellin and jasmonate signaling synergy Plant Cell 26 2014 1118 1133
39. I. Rabino, and A.L. Mancinelli Light, temperature, and anthocyanin production Plant Physiol. 81 1986 922 924
40. G. Rubin, T. Tohge, F. Matsuda, K. Saito, and W.R. Scheible Members of the LBD family of transcription factors repress anthocyanin synthesis and affect additional nitrogen repress in Arabidopsis Plant Cell 21 2009 3567 3584
41. K. Saito, K. Yonekura-Sakakibara, R. Nakabayashi, Y. Higashi, M. Yamazaki, T. Tohge, and A.R. Fernie The flavonoid biosynthetic pathway in Arabidopsis: structural and genetic diversity Plant Physiol. Biochem. 72 2013 21 34
42. S. Sawa Overexpression of the Atmybl2 gene represses trichome development in Arabidopsis DNA Res. 9 2002 31 34
43. X. Shan, Y. Zhang, W. Peng, Z. Wang, and D. Xie Molecular mechanism for jasmonate-induction of anthocyanin accumulation in Arabidopsis J. Exp. Bot. 60 2009 3849 3860
44. C. Solfanelli, A. Poggi, E. Loreti, A. Alpi, and P. Perata Sucrose-specific induction of the anthocyanin biosynthesis pathway in Arabidopsis Plant Physiol. 140 2006 637 646
45. W. Steyn, S. Wand, D. Holcroft, and G. Jacobs Anthocyanins in vegetative tissues: a proposed unified function in photoprotection New Phytol. 155 2002 349 361
46. Y. Sun, H. Li, and J.R. Huang Arabidopsis TT19 functions as a carrier to transport anthocyanin from the cytosol to tonoplasts Mol. Plant 5 2012 387 400
47. H. Wang, W. Fan, H. Li, J. Yang, J. Huang, and P. Zhang Functional characterization of dihydroflavonol-4-reductase in anthocyanin biosynthesis of purple sweet potato underlies the direct evidence of anthocyanins function against abiotic stresses PLoS One 8 2013 e78484
48. M. Wild, J.M. Davière, S. Cheminant, T. Regnault, N. Baumberger, D. Heintz, R. Baltz, P. Genschik, and P. Achard The Arabidopsis DELLA RGA-LIKE3 is a direct target of MYC2 and modulates jasmonate signaling responses Plant Cell 24 2012 3307 3319
49. B. Winkel-Shirley Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology Plant Physiol. 126 2001 485 493
50. D.L. Yang, J. Yao, C.S. Mei, X.H. Tong, L.J. Zeng, Q. Li, L.T. Xiao, T.P. Sun, J. Li, X.W. Deng, and et al. Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade Proc. Natl. Acad. Sci. USA 109 2012 E1192 E1200
51. S.D. Yoo, Y.H. Cho, and J. Sheen Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis Nat. Protoc. 2 2007 1565 1572
52. S. Yu, V.C. Galvão, Y.C. Zhang, D. Horrer, T.Q. Zhang, Y.H. Hao, Y.Q. Feng, S. Wang, M. Schmid, and J.W. Wang Gibberellin regulates the Arabidopsis floral transition through miR156-targeted SQUAMOSA promoter binding-like transcription factors Plant Cell 24 2012 3320 3332
53. F. Zhang, A. Gonzalez, M. Zhao, C.T. Payne, and A. Lloyd A network of redundant bHLH proteins functions in all TTG1-dependent pathways of Arabidopsis Development 130 2003 4859 4869
54. Y. Zhang, E. Butelli, R. De Stefano, H.J. Schoonbeek, A. Maqusin, C. Paqliarani, N. Wellner, L. Hill, D. Orzaez, A. Granell, and et al. Anthocyanins double the shelf life of tomatoes by delaying overripening and reducing susceptibility to gray mold Curr. Biol. 23 2013 1094 1100
55. I.M. Zimmermann, M.A. Heim, B. Weisshaar, and J.F. Uhrig Comprehensive identification of Arabidopsis thaliana MYB transcription factors interacting with R/B-like BHLH proteins Plant J. 40 2004 22 34