Transcriptional control of flavonoid biosynthesis: Fine-tuning of the MYB-bHLH-WD40 (MBW) complex

Plant Signaling and Behavior

Volumn 9, Issue JAN, 2014, Pages

  Li, Shutian ^a  

^a UNIVERSITY OF OSNABRÜCK   (Germany)

Author keywords

Arabidopsis thaliania; Flavonoids; MBW complexes; MYBL2; SPL9; TCP3; TT1

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN; FLAVONOID; INDOLEACETIC ACID DERIVATIVE; TRANSCRIPTION FACTOR;

ARABIDOPSIS; BIOSYNTHESIS; GENE EXPRESSION REGULATION; METABOLISM; PLANT SEED;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; FLAVONOIDS; GENE EXPRESSION REGULATION, PLANT; INDOLEACETIC ACIDS; SEEDS; TRANSCRIPTION FACTORS;

EID: 84899130287     PISSN: 15592316     EISSN: 15592324     Source Type: Journal    
DOI: 10.4161/psb.27522     Document Type: Review

References (62)

1. Winkel-Shirley B. Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol 2001; 126:485-93;PMID:11402179; http://dx.doi.org/10.1104/pp.126.2.485
2. Nesi N, Debeaujon I, Jond C, Stewart AJ, Jenkins GI, Caboche M, Lepiniec L. The TRANSPARENT TESTA16 locus encodes the ARABIDOPSIS BSISTER MADS domain protein and is required for proper development and pigmentation of the seed coat. Plant Cell 2002; 14:2463-79;PMID:12368498; http://dx.doi.org/10.1105/tpc.004127
3. Appelhagen I, Lu GH, Huep G, Schmelzer E, Weisshaar B, Sagasser M. TRANSPARENT TESTA1 interacts with R2R3-MYB factors and affects early and late steps of flavonoid biosynthesis in the endothelium of Arabidopsis thaliana seeds. Plant J 2011; 67:406-19;PMID:21477081; http://dx.doi.org/10.1111/j.1365-313X.2011.04603.x
4. Gou JY, Felippes FF, Liu CJ, Weigel D, Wang JW. Negative regulation of anthocyanin biosynthesis in Arabidopsis by a miR156-targeted SPL transcription factor. Plant Cell 2011; 23:1512-22;PMID:21487097; http://dx.doi.org/10.1105/tpc.111.084525
5. Mehrtens F, Kranz H, Bednarek P, Weisshaar B. The Arabidopsis transcription factor MYB12 is a flavonol-specific regulator of phenylpropanoid biosynthesis. Plant Physiol 2005; 138:1083-96;PMID:15923334; http://dx.doi.org/10.1104/pp.104.058032
6. Stracke R, Ishihara H, Huep G, Barsch A, Mehrtens F, Niehaus K, Weisshaar B. Differential regulation of closely related R2R3-MYB transcription factors controls flavonol accumulation in different parts of the Arabidopsis thaliana seedling. Plant J 2007; 50:660-77;PMID:17419845; http://dx.doi.org/10.1111/j.1365-313X.2007.03078.x
7. Stafford HA. Flavonoid evolution: an enzymic approach. Plant Physiol 1991; 96:680-5;PMID:16668242; http://dx.doi.org/10.1104/pp.96.3.680
8. Ramsay NA, Glover BJ. MYB-bHLH-WD40 protein complex and the evolution of cellular diversity. Trends Plant Sci 2005; 10:63-70;PMID:15708343; http://dx.doi.org/10.1016/j.tplants.2004.12.011
9. Ishida T, Hattori S, Sano R, Inoue K, Shirano Y, Hayashi H, Shibata D, Sato S, Kato T, Tabata S, et al. Arabidopsis TRANSPARENT TESTA GLABRA2 is directly regulated by R2R3 MYB transcription factors and is involved in regulation of GLABRA2 transcription in epidermal differentiation. Plant Cell 2007; 19:2531-43;PMID:17766401; http://dx.doi.org/10.1105/tpc.107.052274
10. Dubos C, Le Gourrierec J, Baudry A, Huep G, Lanet E, Debeaujon I, Routaboul JM, Alboresi A, Weisshaar B, Lepiniec L. MYBL2 is a new regulator of flavonoid biosynthesis in Arabidopsis thaliana. Plant J 2008; 55:940-53;PMID:18532978; http://dx.doi.org/10.1111/j.1365-313X.2008.03564.x
11. Matsui K, Umemura Y, Ohme-Takagi M. AtMYBL2, a protein with a single MYB domain, acts as a negative regulator of anthocyanin biosynthesis in Arabidopsis. Plant J 2008; 55:954-67;PMID:18532977; http://dx.doi.org/10.1111/j.1365-313X.2008.03565.x
12. Li S, Zachgo S. TCP3 interacts with R2R3-MYB proteins, promotes flavonoid biosynthesis and negatively regulates the auxin response in Arabidopsis thaliana. Plant J 2013; 76:901-13; http://dx.doi.org/10.1111/tpj.12348;PMID:24118612
13. Zimmermann IM, Heim MA, Weisshaar B, Uhrig JF. Comprehensive identification of Arabidopsis thaliana MYB transcription factors interacting with R/B-like BHLH proteins. Plant J 2004; 40:22-34;PMID:15361138; http://dx.doi.org/10.1111/j.1365-313X.2004.02183.x
14. Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L. MYB transcription factors in Arabidopsis. Trends Plant Sci 2010; 15:573-81;PMID:20674465; http://dx.doi.org/10.1016/j.tplants.2010.06.005
15. Feller A, Machemer K, Braun EL, Grotewold E. Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. Plant J 2011; 66:94-116;PMID:21443626; http://dx.doi.org/10.1111/j.1365-313X.2010.04459.x
16. Schellmann S, Hülskamp M, Uhrig J. Epidermal pattern formation in the root and shoot of Arabidopsis. Biochem Soc Trans 2007; 35:146-8;PMID:17233622; http://dx.doi.org/10.1042/BST0350146
17. Simon M, Lee MM, Lin Y, Gish L, Schiefelbein J. Distinct and overlapping roles of single-repeat MYB genes in root epidermal patterning. Dev Biol 2007; 311:566-78;PMID:17931617; http://dx.doi.org/10.1016/j.ydbio.2007.09.001
18. Wang S, Kwak SH, Zeng Q, Ellis BE, Chen XY, Schiefelbein J, Chen JG. TRICHOMELESS1 regulates trichome patterning by suppressing GLABRA1 in Arabidopsis. Development 2007; 134:3873-82;PMID:17933793; http://dx.doi.org/10.1242/dev.009597
19. Koes R, Verweij W, Quattrocchio F. Flavonoids: a colorful model for the regulation and evolution of biochemical pathways. Trends Plant Sci 2005; 10:236-42;PMID:15882656; http://dx.doi.org/10.1016/j.tplants.2005.03.002
20. Riese M, Höhmann S, Saedler H, Münster T, Huijser P. Comparative analysis of the SBP-box gene families in P. patens and seed plants. Gene 2007; 401:28-37;PMID:17689888; http://dx.doi.org/10.1016/j.gene.2007.06.018
21. Xing S, Salinas M, Höhmann S, Berndtgen R, Huijser P. miR156-targeted and nontargeted SBP-box transcription factors act in concert to secure male fertility in Arabidopsis. Plant Cell 2010; 22:3935-50;PMID:21177480; http://dx.doi.org/10.1105/tpc.110.079343
22. Wu G, Park MY, Conway SR, Wang JW, Weigel D, Poethig RS. The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 2009; 138:750-9;PMID:19703400; http://dx.doi.org/10.1016/j.cell.2009.06.031
23. Yamaguchi A, Wu MF, Yang L, Wu G, Poethig RS, Wagner D. The microRNA-regulated SBP-Box transcription factor SPL3 is a direct upstream activator of LEAFY, FRUITFULL, and APETALA1. Dev Cell 2009; 17:268-78;PMID:19686687; http://dx.doi.org/10.1016/j.devcel.2009.06.007
24. Yu N, Cai WJ, Wang S, Shan CM, Wang LJ, Chen XY. Temporal control of trichome distribution by microRNA156-targeted SPL genes in Arabidopsis thaliana. Plant Cell 2010; 22:2322-35;PMID:20622149; http://dx.doi.org/10.1105/tpc.109.072579
25. Dean G, Cao Y, Xiang D, Provart NJ, Ramsay L, Ahad A, White R, Selvaraj G, Datla R, Haughn G. Analysis of gene expression patterns during seed coat development in Arabidopsis. Mol Plant 2011; 4:1074-91;PMID:21653281; http://dx.doi.org/10.1093/mp/ssr040
26. Nesi N, Jond C, Debeaujon I, Caboche M, Lepiniec L. The Arabidopsis TT2 gene encodes an R2R3 MYB domain protein that acts as a key determinant for proanthocyanidin accumulation in developing seed. Plant Cell 2001; 13:2099-114;PMID:11549766
27. Hichri I, Barrieu F, Bogs J, Kappel C, Delrot S, Lauvergeat V. Recent advances in the transcriptional regulation of the flavonoid biosynthetic pathway. J Exp Bot 2011; 62:2465-83;PMID:21278228; http://dx.doi.org/10.1093/jxb/erq442
28. Englbrecht CC, Schoof H, Böhm S. Conservation, diversification and expansion of C2H2 zinc finger proteins in the Arabidopsis thaliana genome. BMC Genomics 2004; 5:39;PMID:15236668; http://dx.doi.org/10.1186/1471-2164-5-39
29. Crawford BC, Ditta G, Yanofsky MF. The NTT gene is required for transmitting-tract development in carpels of Arabidopsis thaliana. Curr Biol 2007; 17:1101-8;PMID:17600712; http://dx.doi.org/10.1016/j.cub.2007.05.079
30. Petricka JJ, Clay NK, Nelson TM. Vein patterning screens and the defectively organized tributaries mutants in Arabidopsis thaliana. Plant J 2008; 56:251-63;PMID:18643975; http://dx.doi.org/10.1111/j.1365-313X.2008.03595.x
31. Sagasser M, Lu GH, Hahlbrock K, Weisshaar B. A. thaliana TRANSPARENT TESTA 1 is involved in seed coat development and defines the WIP subfamily of plant zinc finger proteins. Genes Dev 2002; 16:138-49;PMID:11782451; http://dx.doi.org/10.1101/gad.212702
32. Martín-Trillo M, Cubas P. TCP genes: a family snapshot ten years later. Trends Plant Sci 2010; 15:31-9;PMID:19963426; http://dx.doi.org/10.1016/j.tplants.2009.11.003
33. Kosugi S, Ohashi Y. DNA binding and dimerization specificity and potential targets for the TCP protein family. Plant J 2002; 30:337-48;PMID:12000681; http://dx.doi.org/10.1046/j.1365-313X.2002.01294.x
34. Luo D, Carpenter R, Vincent C, Copsey L, Coen E. Origin of floral asymmetry in Antirrhinum. Nature 1996; 383:794-9;PMID:8893002; http://dx.doi.org/10.1038/383794a0
35. Aguilar-Martínez JA, Poza-Carrión C, Cubas P. Arabidopsis BRANCHED1 acts as an integrator of branching signals within axillary buds. Plant Cell 2007; 19:458-72;PMID:17307924; http://dx.doi.org/10.1105/tpc.106.048934
36. Niwa M, Daimon Y, Kurotani K, Higo A, Pruneda-Paz JL, Breton G, Mitsuda N, Kay SA, Ohme-Takagi M, Endo M, et al. BRANCHED1 interacts with FLOWERING LOCUS T to repress the floral transition of the axillary meristems in Arabidopsis. Plant Cell 2013; 25:1228-42;PMID:23613197; http://dx.doi.org/10.1105/tpc.112.109090
37. Kieffer M, Master V, Waites R, Davies B. TCP14 and TCP15 affect internode length and leaf shape in Arabidopsis. Plant J 2011; 68:147-58;PMID:21668538; http://dx.doi.org/10.1111/j.1365-313X.2011.04674.x
38. Nath U, Crawford BC, Carpenter R, Coen E. Genetic control of surface curvature. Science 2003; 299:1404-7;PMID:12610308; http://dx.doi.org/10.1126/science.1079354
39. Nag A, King S, Jack T. miR319a targeting of TCP4 is critical for petal growth and development in Arabidopsis. Proc Natl Acad Sci U S A 2009; 106:22534-9;PMID:20007771; http://dx.doi.org/10.1073/pnas.0908718106
40. Palatnik JF, Allen E, Wu X, Schommer C, Schwab R, Carrington JC, Weigel D. Control of leaf morphogenesis by microRNAs. Nature 2003; 425:257-63;PMID:12931144; http://dx.doi.org/10.1038/nature01958
41. Koyama T, Furutani M, Tasaka M, Ohme-Takagi M. TCP transcription factors control the morphology of shoot lateral organs via negative regulation of the expression of boundary-specific genes in Arabidopsis. Plant Cell 2007; 19:473-84;PMID:17307931; http://dx.doi.org/10.1105/tpc.106.044792
42. Sarvepalli K, Nath U. Hyper-activation of the TCP4 transcription factor in Arabidopsis thaliana accelerates multiple aspects of plant maturation. Plant J 2011; 67:595-607;PMID:21518050; http://dx.doi.org/10.1111/j.1365-313X.2011.04616.x
43. Schommer C, Palatnik JF, Aggarwal P, Chételat A, Cubas P, Farmer EE, Nath U, Weigel D. Control of jasmonate biosynthesis and senescence by miR319 targets. PLoS Biol 2008; 6:e230;PMID:18816164; http://dx.doi.org/10.1371/journal.pbio.0060230
44. Sugio A, Kingdom HN, MacLean AM, Grieve VM, Hogenhout SA. Phytoplasma protein effector SAP11 enhances insect vector reproduction by manipulating plant development and defense hormone biosynthesis. Proc Natl Acad Sci U S A 2011; 108:E1254-63;PMID:22065743; http://dx.doi.org/10.1073/pnas.1105664108
45. Guo Z, Fujioka S, Blancaflor EB, Miao S, Gou X, Li J. TCP1 modulates brassinosteroid biosynthesis by regulating the expression of the key biosynthetic gene DWARF4 in Arabidopsis thaliana. Plant Cell 2010; 22:1161-73;PMID:20435901; http://dx.doi.org/10.1105/tpc.109.069203
46. Koyama T, Sato F, Ohme-Takagi M. A role of TCP1 in the longitudinal elongation of leaves in Arabidopsis. Biosci Biotechnol Biochem 2010; 74:2145-7;PMID:20944404; http://dx.doi.org/10.1271/bbb.100442
47. Gonzalez A, Zhao M, Leavitt JM, Lloyd AM. Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings. Plant J 2008; 53:814-27;PMID:18036197; http://dx.doi.org/10.1111/j.1365-313X.2007.03373.x
48. Dharmasiri N, Dharmasiri S, Estelle M. The F-box protein TIR1 is an auxin receptor. Nature 2005; 435:441-5;PMID:15917797; http://dx.doi.org/10.1038/nature03543
49. Yin XJ, Volk S, Ljung K, Mehlmer N, Dolezal K, Ditengou F, Hanano S, Davis SJ, Schmelzer E, Sandberg G, et al. Ubiquitin lysine 63 chain forming ligases regulate apical dominance in Arabidopsis. Plant Cell 2007; 19:1898-911;PMID:17586653; http://dx.doi.org/10.1105/tpc.107.052035
50. Leyser HM, Lincoln CA, Timpte C, Lammer D, Turner J, Estelle M. Arabidopsis auxin-resistance gene AXR1 encodes a protein related to ubiquitin-activating enzyme E1. Nature 1993; 364:161-4;PMID:8321287; http://dx.doi.org/10.1038/364161a0
51. Kuhn BM, Geisler M, Bigler L, Ringli C. Flavonols accumulate asymmetrically and affect auxin transport in Arabidopsis. Plant Physiol 2011; 156:585-95;PMID:21502189; http://dx.doi.org/10.1104/pp.111.175976
52. Murphy A, Peer WA, Taiz L. Regulation of auxin transport by aminopeptidases and endogenous flavonoids. Planta 2000; 211:315-24;PMID:10987549; http://dx.doi.org/10.1007/s004250000300
53. Peer WA, Bandyopadhyay A, Blakeslee JJ, Makam SN, Chen RJ, Masson PH, Murphy AS. Variation in expression and protein localization of the PIN family of auxin efflux facilitator proteins in flavonoid mutants with altered auxin transport in Arabidopsis thaliana. Plant Cell 2004; 16:1898-911;PMID:15208397; http://dx.doi.org/10.1105/tpc.021501
54. Petrásek J, Friml J. Auxin transport routes in plant development. Development 2009; 136:2675-88;PMID:19633168; http://dx.doi.org/10.1242/dev.030353
55. Santelia D, Henrichs S, Vincenzetti V, Sauer M, Bigler L, Klein M, Bailly A, Lee Y, Friml J, Geisler M, et al. Flavonoids redirect PIN-mediated polar auxin fluxes during root gravitropic responses. J Biol Chem 2008; 283:31218-26;PMID:18718912; http://dx.doi.org/10.1074/jbc.M710122200
56. Buer CS, Djordjevic MA. Architectural phenotypes in the transparent testa mutants of Arabidopsis thaliana. J Exp Bot 2009; 60:751-63;PMID:19129166; http://dx.doi.org/10.1093/jxb/ern323
57. Peer WA, Brown DE, Tague BW, Muday GK, Taiz L, Murphy AS. Flavonoid accumulation patterns of transparent testa mutants of arabidopsis. Plant Physiol 2001; 126:536-48;PMID:11402185; http://dx.doi.org/10.1104/pp.126.2.536
58. Shirley BW, Kubasek WL, Storz G, Bruggemann E, Koornneef M, Ausubel FM, Goodman HM. Analysis of Arabidopsis mutants deficient in flavonoid biosynthesis. Plant J 1995; 8:659-71;PMID:8528278; http://dx.doi.org/10.1046/j.1365-313X.1995.08050659.x
59. Rubin G, Tohge T, Matsuda F, Saito K, Scheible WR. Members of the LBD family of transcription factors repress anthocyanin synthesis and affect additional nitrogen responses in Arabidopsis. Plant Cell 2009; 21:3567-84;PMID:19933203; http://dx.doi.org/10.1105/tpc.109.067041
60. Baudry A, Caboche M, Lepiniec L. TT8 controls its own expression in a feedback regulation involving TTG1 and homologous MYB and bHLH factors, allowing a strong and cell-specific accumulation of flavonoids in Arabidopsis thaliana. Plant J 2006; 46:768-79;PMID:16709193; http://dx.doi.org/10.1111/j.1365-313X.2006.02733.x
61. Borevitz JO, Xia Y, Blount J, Dixon RA, Lamb C. Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell 2000; 12:2383-94;PMID:11148285
62. Tohge T, Nishiyama Y, Hirai MY, Yano M, Nakajima J, Awazuhara M, Inoue E, Takahashi H, Goodenowe DB, Kitayama M, et al. Functional genomics by integrated analysis of metabolome and transcriptome of Arabidopsis plants over-expressing an MYB transcription factor. Plant J 2005; 42:218-35;PMID:15807784; http://dx.doi.org/10.1111/j.1365-313X.2005.02371.x