TRANSPARENT TESTA1 interacts with R2R3-MYB factors and affects early and late steps of flavonoid biosynthesis in the endothelium of Arabidopsis thaliana seeds

Plant Journal

Volumn 67, Issue 3, 2011, Pages 406-419

  Appelhagen, Ingo ^a   Lu, Gui Hua ^b   Huep, Gunnar ^a   Schmelzer, Elmon ^b   Weisshaar, Bernd ^a   Sagasser, Martin ^a  

^a BIELEFELD UNIVERSITY   (Germany)

^b MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

Author keywords

gene regulation; MYB BHLH WD40 complex; proanthocyanidin; seed coat; transparent testa; WIP zinc finger

Indexed keywords

MYB-BHLH-WD40 COMPLEX; PROANTHOCYANIDINS; SEED COAT; TRANSPARENT TESTA; WIP ZINC FINGER;

BIOCHEMISTRY; BIOSYNTHESIS; ENCODING (SYMBOLS); GENE EXPRESSION; PROTEINS; ZINC;

SEED;

ARABIDOPSIS PROTEIN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; DNA BINDING PROTEIN; FLAVONOID; TT2 PROTEIN, ARABIDOPSIS; TT8 PROTEIN, ARABIDOPSIS; TTG1 PROTEIN, ARABIDOPSIS;

ALLELE; ARABIDOPSIS; ARTICLE; BIOSYNTHESIS; CELL NUCLEUS; GENE EXPRESSION REGULATION; GENE LOCUS; GENETIC TRANSFECTION; GENETICS; METABOLISM; MUTATION; PHENOTYPE; PIGMENTATION; PLANT GENE; PLANT SEED; REGULON; TRANSCRIPTION INITIATION;

ALLELES; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL NUCLEUS; DNA-BINDING PROTEINS; FLAVONOIDS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENETIC LOCI; MUTATION; PHENOTYPE; PIGMENTATION; REGULON; SEEDS; TRANSCRIPTIONAL ACTIVATION; TRANSFECTION;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 79960921597     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2011.04603.x     Document Type: Article

References (68)

1. Abrahams, S., Tanner, G.J., Larkin, P.J., and, Ashton, A.R., (2002) Identification and biochemical characterization of mutants in the proanthocyanidin pathway in Arabidopsis. Plant Physiol. 130, 561-576. (Pubitemid 35224766)
2. Abrahams, S., Lee, E., Walker, A.R., Tanner, G.J., Larkin, P.J., and, Ashton, A.R., (2003) The Arabidopsis TDS4 gene encodes leukoanthocyanidin dioxygenase (LDOX) and is essential for proanthocyanidin synthesis and vacuole development. Plant J. 35, 624-636. (Pubitemid 37110717)
3. Albert, S., Delseny, M., and, Devic, M., (1997) BANYULS, a novel negative regulator of flavonoid biosynthesis in the Arabidopsis seed coat. Plant J. 11, 289-299. (Pubitemid 27147975)
4. Appelhagen, I., Huep, G., Lu, G.H., Strompen, G., Weisshaar, B., and, Sagasser, M., (2010) Weird fingers: functional analysis of WIP domain proteins. FEBS Lett. 584, 3116-3122.
5. von Arnim, A.G., Deng, X.-W., and, Stacey, M.G., (1998) Cloning vectors for the expression of green fluorescent protein fusion proteins in transgenic plants. Gene, 221, 35-43. (Pubitemid 28529606)
6. Bailey, P.C., Martin, C., Toledo-Ortiz, G., Quail, P.H., Huq, E., Heim, M.A., Jakoby, M., Werber, M., and, Weisshaar, B., (2003) Update on the basic helix-loop-helix transcription factor gene family in Arabidopsis thaliana. Plant Cell, 15, 2497-2502.
7. Baudry, A., Heim, M.A., Dubreucq, B., Caboche, M., Weisshaar, B., and, Lepiniec, L., (2004) TT2, TT8, and TTG1 synergistically specify the expression of BANYULS and proanthocyanidin biosynthesis in Arabidopsis thaliana. Plant J. 39, 366-380. (Pubitemid 39040142)
8. Baudry, A., Caboche, M., and, Lepiniec, L., (2006) 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. 46, 768-779. (Pubitemid 43780624)
9. Baxter, I.R., Young, J.C., Armstrong, G., Foster, N., Bogenschutz, N., Cordova, T., Peer, W.A., Hazen, S.P., Murphy, A.S., and, Harper, J.F., (2005) A plasma membrane H+-ATPase is required for the formation of proanthocyanidins in the seed coat endothelium of Arabidopsis thaliana. Proc. Natl Acad. Sci. USA, 102, 2649-2654. (Pubitemid 40279431)
10. Bechtold, N., Ellis, J., and, Pelletier, G., (1993) In planta Agrobacterium mediated gene transfer by infiltration of adult Arabidopsis thaliana plants. CR Acad. Sci. III Sci. Vie. 316, 1194-1199. (Pubitemid 23336519)
11. Borevitz, J.O., Xia, Y.J., Blount, J., Dixon, R.A., and, Lamb, C., (2000) Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell, 12, 2383-2393. (Pubitemid 32106413)
12. Broun, P., (2005) Transcriptional control of flavonoid biosynthesis: a complex network of conserved regulators involved in multiple aspects of differentiation in Arabidopsis. Curr. Opin. Plant Biol. 8, 272-279. (Pubitemid 40599981)
13. Brunaud, V., Balzergue, S., Dubreucq, B., et al. (2002) T-DNA integration into the Arabidopsis genome depends on sequences of pre-insertion sites. EMBO Rep. 3, 1152-1157. (Pubitemid 36105003)
14. Crawford, B.C., Ditta, G., and, Yanofsky, M.F., (2007) The NTT gene is required for transmitting-tract development in carpels of Arabidopsis thaliana. Curr. Biol. 17, 1101-1108. (Pubitemid 46990892)
15. Debeaujon, I., Leon-Kloosterziel, K., and, Koornneef, M., (2000) Influence of the testa on seed dormancy, germination, and longevity in Arabidopsis. Plant Physiol. 122, 403-413. (Pubitemid 30153108)
16. Debeaujon, I., Peeters, A.J.M., Léon-Kloosterziel, K.M., and, Koornneef, M., (2001) The TRANSPARENT TESTA12 gene of Arabidopsis encodes a multidrug secondary transporter-like protein required for flavonoid sequestration in vacuoles of the seed coat endothelium. Plant Cell, 13, 853-872.
17. Debeaujon, I., Nesi, N., Perez, P., Devic, M., Grandjean, O., Caboche, M., and, Lepiniec, L., (2003) Proanthocyanidin-accumulating cells in Arabidopsis testa: regulation of differentiation and role in seed development. Plant Cell, 15, 2514-2531. (Pubitemid 37470655)
18. DeBolt, S., Scheible, W.R., Schrick, K., et al. (2009) Mutations in UDP-glucose:sterol glucosyltransferase in Arabidopsis cause transparent testa phenotype and suberization defect in seeds. Plant Physiol. 151, 78-87.
19. Devic, M., Guilleminot, J., Debeaujon, I., Bechtold, N., Bensaude, E., Koornneef, M., Pelletier, G., and, Delseny, M., (1999) The BANYULS gene encodes a DFR-like protein and is a marker of early seed coat development. Plant J. 19, 387-398.
20. Dubos, C., Le Gourrierec, J., Baudry, A., Huep, G., Lane, E., Debeaujon, I., Routaboul, J.M., Alboresi, A., Weisshaar, B., and, Lepiniec, L., (2008) MYBL2 is a new regulator of flavonoid biosynthesis in Arabidopsis thaliana. Plant J. 55, 940-953.
21. Dubos, C., Stracke, R., Grotewold, E., Weisshaar, B., Martin, C., and, Lepiniec, L., (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci. 15, 573-581.
22. Englbrecht, C.C., Schoof, H., and, Bohm, S., (2004) Conservation, diversification and expansion of C2H2 zinc finger proteins in the Arabidopsis thaliana genome. BMC Genomics, 5, 39.
23. Gietz, R.D., and, Schiestl, R.H., (2007) Frozen competent yeast cells that can be transformed with high efficiency using the LiAc/SS carrier DNA/PEG method. Nat. Protoc. 2, 1-4. (Pubitemid 47040061)
24. Gonzalez, A., Zhao, M., Leavitt, J.M., and, Lloyd, A.M., (2008) Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings. Plant J. 53, 814-827. (Pubitemid 351495869)
25. Greb, T., Clarenz, O., Schafer, E., Muller, D., Herrero, R., Schmitz, G., and, Theres, K., (2003) Molecular analysis of the LATERAL SUPPRESSOR gene in Arabidopsis reveals a conserved control mechanism for axillary meristem formation. Genes Dev. 17, 1175-1187. (Pubitemid 36534991)
26. Haasen, D., Kohler, C., Neuhaus, G., and, Merkle, T., (1999) Nuclear export of proteins in plants: AtXPO1 is the export receptor for leucine-rich nuclear export signals in Arabidopsis thaliana. Plant J. 20, 695-705.
27. Haughn, G., and, Chaudhury, A., (2005) Genetic analysis of seed coat development in Arabidopsis. Trends Plant Sci. 10, 472-477. (Pubitemid 41395268)
28. Heim, M.A., Jakoby, M., Werber, M., Martin, C., Weisshaar, B., and, Bailey, P.C., (2003) The basic helix-loop-helix transcription factor family in plants: a genome-wide study of protein structure and functional diversity. Mol. Biol. Evol. 20, 735-747. (Pubitemid 36539009)
29. Hu, C.D., Chinenov, Y., and, Kerppola, T.K., (2002) Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. Mol. Cell, 9, 789-798. (Pubitemid 34454889)
30. Jakoby, M.J., Weinl, C., Pusch, S., Kuijt, S.J., Merkle, T., Dissmeyer, N., and, Schnittger, A., (2006) Analysis of the subcellular localization, function, and proteolytic control of the Arabidopsis cyclin-dependent kinase inhibitor ICK1/KRP1. Plant Physiol. 141, 1293-1305. (Pubitemid 44223282)
31. James, P., Halladay, J., and, Craig, E.A., (1996) Genomic libraries and a host strain designed for highly efficient two- hybrid selection in yeast. Genetics, 144, 1425-1436.
32. Johnson, C.S., Kolevski, B., and, Smyth, D.R., (2002) TRANSPARENT TESTA GLABRA2, a trichome and seed coat development gene of Arabidopsis, encodes a WRKY transcription factor. Plant Cell, 14, 1359-1375. (Pubitemid 34780437)
33. Kitamura, S., Shikazono, N., and, Tanaka, A., (2004) TRANSPARENT TESTA 19 is involved in the accumulation of both anthocyanins and proanthocyanidins in Arabidopsis. Plant J. 37, 104-114. (Pubitemid 38078269)
34. Koornneef, M., (1990) Mutations affecting the testa colour in Arabidopsis. Arabidopsis Inf. Serv. 27, 1-4.
35. Kubasek, W.L., Shirley, B.W., McKillop, A., Goodman, H.M., Briggs, W., and, Ausubel, F.M., (1992) Regulation of flavonoid biosynthetic genes in germinating Arabidopsis seedlings. Plant Cell, 4, 1229-1236.
36. Le, B.H., Cheng, C., Bui, A.Q., et al. (2010) Global analysis of gene activity during Arabidopsis seed development and identification of seed-specific transcription factors. Proc. Natl Acad. Sci. USA, 107, 8063-8070.
37. Lepiniec, L., Debeaujon, I., Routaboul, J.M., Baudry, A., Pourcel, L., Nesi, N., and, Caboche, M., (2006) Genetics and biochemistry of seed flavonoids. Annu. Rev. Plant Biol. 57, 405-430. (Pubitemid 44061031)
38. Marinova, K., Pourcel, L., Weder, B., Schwarz, M., Barron, D., Routaboul, J.M., Debeaujon, I., and, Klein, M., (2007) The Arabidopsis MATE transporter TT12 acts as a vacuolar flavonoid/H+ -antiporter active in proanthocyanidin- accumulating cells of the seed coat. Plant Cell, 19, 2023-2038. (Pubitemid 47218856)
39. Martin, A., Troadec, C., Boualem, A., Rajab, M., Fernandez, R., Morin, H., Pitrat, M., Dogimont, C., and, Bendahmane, A., (2009) A transposon-induced epigenetic change leads to sex determination in melon. Nature, 461, 1135-1138.
40. Mehrtens, F., Kranz, H., Bednarek, P., and, Weisshaar, B., (2005) The Arabidopsis transcription factor MYB12 is a flavonol-specific regulator of phenylpropanoid biosynthesis. Plant Physiol. 138, 1083-1096. (Pubitemid 43793183)
41. Nawy, T., Lee, J.Y., Colinas, J., Wang, J.Y., Thongrod, S.C., Malamy, J.E., Birnbaum, K., and, Benfey, P.N., (2005) Transcriptional profile of the Arabidopsis root quiescent center. Plant Cell, 17, 1908-1925.
42. Nesi, N., Debeaujon, I., Jond, C., Pelletier, G., Caboche, M., and, Lepiniec, L., (2000) 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, 1863-1878.
43. Nesi, N., Jond, C., Debeaujon, I., Caboche, M., and, Lepiniec, L., (2001) The Arabidopsis TT2 gene encodes an R2R3 MYB domain protein that acts as a key determinant for proanthocyanidin accumulation in developing seed. Plant Cell, 13, 2099-2114. (Pubitemid 32925416)
44. Nesi, N., Debeaujon, I., Jond, C., Stewart, A.J., Jenkins, G.I., Caboche, M., and, Lepiniec, L., (2002) 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, 14, 2463-2479. (Pubitemid 35224843)
45. Parenicova, L., de Folter, S., Kieffer, M., et al. (2003) Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS world. Plant Cell, 15, 1538-1551. (Pubitemid 36872595)
46. Petricka, J.J., Clay, N.K., and, Nelson, T.M., (2008) Vein patterning screens and the defectively organized tributaries mutants in Arabidopsis thaliana. Plant J. 56, 251-263.
47. Pourcel, L., Routaboul, J.M., Kerhoas, L., Caboche, M., Lepiniec, L., and, Debeaujon, I., (2005) TRANSPARENT TESTA10 encodes a laccase-like enzyme involved in oxidative polymerization of flavonoids in Arabidopsis seed coat. Plant Cell, 17, 2966-2980.
48. Pourcel, L., Routaboul, J.M., Cheynier, V., Lepiniec, L., and, Debeaujon, I., (2007) Flavonoid oxidation in plants: from biochemical properties to physiological functions. Trends Plant Sci. 12, 29-36. (Pubitemid 46096808)
49. Routaboul, J.M., Kerhoas, L., Debeaujon, I., Pourcel, L., Caboche, M., Einhorn, J., and, Lepiniec, L., (2006) Flavonoid diversity and biosynthesis in seed of Arabidopsis thaliana. Planta, 224, 96-107. (Pubitemid 43800705)
50. Sagasser, M., Lu, G.-H., Hahlbrock, K., and, Weisshaar, B., (2002) A. thaliana TRANSPARENT TESTA 1 is involved in seed coat development and defines the WIP subfamily of plant zinc finger proteins. Genes Dev. 16, 138-149. (Pubitemid 34049644)
51. Shaner, N.C., Campbell, R.E., Steinbach, P.A., Giepmans, B.N., Palmer, A.E., and, Tsien, R.Y., (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat. Biotechnol. 22, 1567-1572. (Pubitemid 40039460)
52. Sharma, S.B., and, Dixon, R.A., (2005) Metabolic engineering of proanthocyanidins by ectopic expression of transcription factors in Arabidopsis thaliana. Plant J. 44, 62-75.
53. Shikazono, N., Yokota, Y., Kitamura, S., Suzuki, C., Watanabe, H., Tano, S., and, Tanaka, A., (2003) Mutation rate and novel tt mutants of Arabidopsis thaliana induced by carbon ions. Genetics, 163, 1449-1455. (Pubitemid 36523395)
54. Shirley, B.W., Kubasek, W.L., Storz, G., Bruggemann, E., Koornneef, M., Ausubel, F.M., and, Goodman, H.M., (1995) Analysis of Arabidopsis mutants deficient in flavonoid biosynthesis. Plant J. 8, 659-671.
55. Stracke, R., Werber, M., and, Weisshaar, B., (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr. Opin. Plant Biol. 4, 447-456. (Pubitemid 32792562)
56. Stracke, R., Ishihara, H., Huep, G., Barsch, A., Mehrtens, F., Niehaus, K., and, Weisshaar, B., (2007) Differential regulation of closely related R2R3-MYB transcription factors controls flavonol accumulation in different parts of the Arabidopsis thaliana seedling. Plant J. 50, 660-677. (Pubitemid 46733755)
57. Stracke, R., Favory, J.-J., Gubler, H., Bartelniewöhner, L., Bartels, S., Binkert, M., Funk, M., Weisshaar, B., and, Ulm, R., (2010a) The Arabidopsis bZIP transcription factor HY5 regulates expression of the PFG1/MYB12 gene in response to light and ultraviolet-B radiation. Plant Cell Environ. 33, 88-103.
58. Stracke, R., Jahns, O., Keck, M., Tohge, T., Niehaus, K., Fernie, A.R., and, Weisshaar, B., (2010b) Analysis of PRODUCTION OF FLAVONOL GLYCOSIDES-dependent flavonol glycoside accumulation in Arabidopsis thaliana plants reveals MYB11-, MYB12-, MYB111-independent flavonol glycoside accumulation. New Phytol. 188, 985-1000.
59. Vicient, C.M., and, Delseny, M., (1999) Isolation of total RNA from Arabidopsis thaliana seeds. Anal. Biochem. 268, 412-413. (Pubitemid 29147161)
60. Walker, A.R., Davison, P.A., Bolognesi-Winfield, A.C., James, C.M., Srinivasan, N., Blundell, T.L., Esch, J.J., Marks, M.D., and, Gray, J.C., (1999) The TRANSPARENT TESTA GLABRA1 locus, which regulates trichome differentiation and anthocyanin biosynthesis in Arabidopsis, encodes a WD40 repeat protein. Plant Cell, 11, 1337-1350.
61. Weisshaar, B., and, Jenkins, G.I., (1998) Phenylpropanoid biosynthesis and its regulation. Curr. Opin. Plant Biol. 1, 251-257. (Pubitemid 128653981)
62. Winkel-Shirley, B., (2001) Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol. 126, 485-493. (Pubitemid 32566604)
63. Winkel-Shirley, B., (2002) Biosynthesis of flavonoids and effects of stress. Curr. Opin. Plant Biol. 5, 218-223. (Pubitemid 34452068)
64. Wisman, E., Hartmann, U., Sagasser, M., Baumann, E., Palme, K., Hahlbrock, K., Saedler, H., and, Weisshaar, B., (1998) Knock-out mutants from an En-1 mutagenized Arabidopsis thaliana population generate new phenylpropanoid biosynthesis phenotypes. Proc. Natl Acad. Sci. USA, 95, 12432-12437. (Pubitemid 28483782)
65. Xie, D.Y., Sharma, S.B., Paiva, N.L., Ferreira, D., and, Dixon, R.A., (2003) Role of anthocyanidin reductase, encoded by BANYULS in plant flavonoid biosynthesis. Science, 299, 396-399. (Pubitemid 36120043)
66. Zhao, J., and, Dixon, R.A., (2009) MATE transporters facilitate vacuolar uptake of epicatechin 3′-O-glucoside for proanthocyanidin biosynthesis in Medicago truncatula and Arabidopsis. Plant Cell, 21, 2323-2340.
67. Zhao, J., Pang, Y., and, Dixon, R.A., (2010) The Mysteries of Proanthocyanidin Transport and Polymerization. Plant Physiol. 153, 437-443.
68. Zimmermann, I.M., Heim, M.A., Weisshaar, B., and, Uhrig, J.F., (2004) Comprehensive identification of Arabidopsis thaliana MYB transcription factors interacting with R/B-like BHLH proteins. Plant J. 40, 22-34. (Pubitemid 39342591)