A new dominant Arabidopsis transparent testa mutant, sk21-D, and modulation of seed flavonoid biosynthesis by KAN4

Plant Biotechnology Journal

Volumn 8, Issue 9, 2010, Pages 979-993

  Gao, Peng ^a   Li, Xiang ^a,b,c   Cui, Dejun ^a,d   Wu, Limin ^a,e   Parkin, Isobel ^a   Gruber, Margaret Y ^a  

^a SASKATOON RESEARCH CENTRE   (Canada)

^b JILIN UNIVERSITY   (China)

^c NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^d UNIVERSITY OF SASKATCHEWAN   (Canada)

^e ALBERTA RESEARCH COUNCIL   (Canada)

Author keywords

Activation expression; Dominant; Flavonoid; KAN4; Proanthocyanidin; Transparent testa (tt)

Indexed keywords

ARABIDOPSIS PROTEIN; FLAVONOID; KAN4 PROTEIN, ARABIDOPSIS; PROANTHOCYANIDIN; TRANSCRIPTION FACTOR;

ARABIDOPSIS; ARTICLE; BIOSYNTHESIS; GEL MOBILITY SHIFT ASSAY; GENETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; METABOLISM; PHENOTYPE; PLANT SEED; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TANDEM MASS SPECTROMETRY;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; ELECTROPHORETIC MOBILITY SHIFT ASSAY; FLAVONOIDS; PHENOTYPE; PROANTHOCYANIDINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEEDS; TANDEM MASS SPECTROMETRY; TRANSCRIPTION FACTORS;

ANIMALIA; ARABIDOPSIS;

EID: 78149479363     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/j.1467-7652.2010.00525.x     Document Type: Article

References (69)

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.
2. Bassett, M.J. and McClean, P. (2000) A brief review of the genetics of partly coloured seed coats in common bean. Annual Report. Bean Improv. Coop. 43, 99-101.
3. 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.
4. 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.
5. Bharti, A.K. and Khurana, J.P. (2003) Molecular characterization of transparent testa (tt) mutants of Arabidopsis thaliana (ecotype Estland) impaired in flavonoid biosynthetic pathway. Plant Sci. 165, 1321-1332.
6. Burbulis, I.E. and Winkel-Shirley, B. (1999) Interactions among enzymes of the Arabidopsis flavonoid biosynthetic pathway. Proc. Natl Acad. Sci. USA, 96, 12929-12934.
7. Chen, Y., Yang, X., He, K., Lie, M., Lid, J., Gao, Z., Lin, Z., Zhang, Y., Wang, X., Qiu, X., Shen, Y., Zhang, L., Deng, X., Luo, J., Deng, X., Chen, Z., Gu, H. and Qu, L. (2006) The MYB transcription factor superfamily of Arabidopsis: expression analysis and phylogenetic comparison with the rice MYB family. Plant Mol. Biol. 60, 107-124.
8. Clough, S.J. and Bent, A.F. (1998) Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J., 16, 735-743.
9. D'Auria, J.C. and Gershenzon, J. (2005) The secondary metabolism of Arabidopsis thaliana: growing like a weed. Curr. Opin. Plant Biol. 8, 308-316.
10. Debeaujon, I., Leon-Kloosterziel, K.M. and Koornneef, M. (2000) Influence of the testa on seeddormancy, germination, and longevity in Arabidopsis. Plant Physiol. 122, 403-414.
11. 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.
12. Dubos, C., Le Gourrierec, J., Baudry, A., Huep, G., Lanet, 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.
13. Esch, J.J., Chen, M., Sanders, M., Hillestad, M., Ndkium, S., Idelkope, B., Neizer, J. and Marks, M.D. (2003) A contradictory GLABRA3 allele helps define gene interactions controlling trichome development in Arabidopsis. Development, 130, 5885-5894.
14. Eshed, Y., Baum, S.F., Perea, J.V. and Bowman, J.L. (2001) Establishment of polarity in lateral organs of plants. Curr. Biol. 11, 1251-1260.
15. Frangioni, J.V. and Neel, B.G. (1993) Solubilization and purification of enzymatically active glutathione S-transferase (pGEX) fusion proteins. Anal Biochem., 210, 179-187.
16. Garcia-Florenciano, E., Barcelo, A.R., Sabater, F. and Munoz, R. (1989) The spectrophotometric determination of indole-3-methanol in small samples with p-dimethylaminocinnamaldehyde on the basis of the formation of an azafulvenium salt. Anal. Biochem. 183, 172-176.
17. Harborne, J.B. and Williams, C.A. (2000) Advances in flavonoid research since 1992. Phytochemistry, 55, 481-504.
18. Haugh, G. and Chaudhury, A. (2005) Genetic analysis of seed coat development in Arabidopsis. Trends Plant Sci. 10, 472-477.
19. 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.
20. Hosoda, K., Imamura, A., Katoh, E., Hatta, T., Tachiki, M., Yamada, H., Mizuno, T. and Yamazaki, T. (2002) Molecular structure of the GARP family of plant Myb-related DNA binding motifs of the Arabidopsis response regulators. Plant Cell, 14, 2015-2029.
21. Hutchison, C.E. and Kieber, J.J. (2002) Cytokinin signaling in Arabidopsis. Plant Cell, 14(Suppl), S47-S59.
22. 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.
23. Kim, H.J., Fonseca, J.M., Choi, J.H., Kubota, C. and Kwon, D.Y. (2008) Salt in irrigation water affects the nutritional and visual properties of Romaine lettuce (Lactuca sativa L.). J. Agric. Food. Chem. 56, 3772-3776.
24. 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.
25. Koes, R., Verweij, W. and Quattrocchio, F. (2005) Flavonoids: a colorful model for the regulation and evolution of biochemical pathways. Trends Plant Sci. 10, 236-242.
26. Koornneef, M. (1990) Mutations affecting the testa colour in Arabidopsis. Arabidopsis Inf. Serv. 27, 1-4.
27. Koshino-Kimura, Y., Wada, T., Tachibana, T., Tsugeki, R., Ishiguro, S. and Okada, K. (2005) Regulation of CAPRICE transcription by MYB proteins for root epidermis differentiation in Arabidopsis. Plant Cell Physiol. 46, 817-826.
28. 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.
29. Marles, M.A.S., Gruber, M.Y., Scoles, G.J. and Muir, A.D. (2003) Pigmentation in the developing seed coat and seedling leaves of Brassica carinata is controlled at the dihydroflavonol reductase locus. Phytochemistry, 62, 663-672.
30. Marotti, I., Bonetti, A., Biavati, B., Catizone, P. and Dinelli, G. (2007) Biotransformation of common bean (Phaseolus vulgaris L.) flavonoid glycosides by Biridobacterium species from human intestinal origin. J. Agric. Food. Chem. 55, 3913-3919.
31. Matsui, K., Umemura, Y. and Ohme-Takagi, M. (2008) AtMYBL2, a protein with a single MYB domain, acts as a negative regulator of anthocyanin biosynthesis in Arabidopsis. Plant J. 55, 954-967.
32. Mazza, G.J. (2007) Anthocyanins and heart health. Ann. Ist. Super. Sanita. 43, 369-374.
33. McAbee, J.M., Hill, T.A., Skinner, D.J., Izhaki, A., Hauser, B.A., Meister, R.J., Venugopala Reddy, G., Meyerowitz, E.M., Bowman, J.L. and Gasser, C.S. (2006) ABERRANT TESTA SHAPE encodes a KANADI family member, linking polarity determination to separation and growth of Arabidopsis ovule integuments. Plant J. 46, 522-531.
34. McClean, P.E., Lee, R.K., Otto, C., Gepts, P. and Bassett, M.J. (2002) Molecular and phenotypic mapping of genes controlling seed coat pattern and colour in common bean (Phaseolus vulgaris L.). J. Hered., 93, 148-152.
35. 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.
36. 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.
37. 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.
38. 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.
39. Peer, W.A., Brown, D.E., Tague, B.W., Muday, G.K., Taiz, L. and Murphy, A.S. (2001) Flavonoid accumulation patterns of transparent testa mutants of Arabidopsis. Plant Physiol. 126, 536-548.
40. Pelletier, M.K. and Shirley, B.W. (1996) Analysis of flavanone 3-hydroxylase in Arabidopsis seedlings. Coordinate regulation with chalcone synthase and chalcone isomerase. Plant Physiol. 111, 339-345.
41. Pelletier, M.K., Murrell, J.R. and Shirley, B.W. (1997) Characterization of flavonol synthase and leucoanthocyanidin dioxygenase genes in Arabidopsis- further evidence for differential regulation of 'early' and 'late' genes. Plant Physiol. 113, 1437-1445.
42. Pelletier, M.K., Burbulis, I.E. and Winkel-Shirley, B. (1999) Disruption of specific flavonoid genes enhances the accumulation of flavonoid enzymes and end-products in Arabidopsis seedlings. Plant Mol. Biol. 40, 45-54.
43. Porter, L.J., Hrstich, L.N. and Chan, B.G. (1986) The conversion of procyanidins and prodelphinidins to cyanidins and delphinidins. Phytochemistry, 25, 223-230.
44. Pourcel, C., 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.
45. Quattrocchio, F., Baudry, A., Lepiniec, L. and Grotewold, E. (2006) The Regulation of Flavonoid Biosynthesis. New York: Springer Sci. Business Media.
46. Robinson, S., Tang, L., Mooney, B., Clarke, W., Links, M., Karcz, S., Regan, S., Wu, Y., Gruber, M., Cui, D., Yu, M. and Parkin, I. (2009) An archived activation tagged population of Arabidopsis to facilitate forward genetics approaches. BMC Plant Biol. 9, 101.
47. Ross, J.A. and Kasum, C.M. (2002) Dietary flavonoids: bioavailability, metabolic effects, and safety. Annu. Rev. Nutr. 22, 19-34.
48. 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.
49. 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.
50. Sakai, H., Aoyama, T., Bono, H. and Oka, A. (1998) Two-component response regulators from Arabidopsis thaliana contain a putative DNA-binding motif. Plant Cell Physiol. 39, 1232-1239.
51. Sakai, H., Aoyama, T. and Oka, A. (2000) Arabidopsis ARR1 and ARR2 response regulators operate as transcriptional activators. Plant J. 24, 703-711.
52. Scalbert, A., Johnson, I.T. and Saltmarsh, M. (2005) Polyphenols: antioxidants and beyond. Am. J. Clin. Nutr. 81, 215S-217S.
53. Schijlen, E.G., Ric de Vos, C.H., Van Tunen, A.J. and Bovy, A.G. (2004) Modification of flavonoid biosynthesis in crop plants. Phytochemistry, 65, 2631-2648.
54. Schmid, M., Davison, T.S., Henz, S.R., Pape, U.J., Demar, M., Vingron, M., Schölkopf, B., Weigel, D. and Lohmann, J. (2005) A gene expression map of Arabidopsis development. Nat. Genet. 37, 501-506.
55. Shirley, B.W. (1998) Flavonoids in seeds and grains: physiological function, agronomic importance and the genetics of biosynthesis. Seed Sci. Res. 8, 415-422.
56. 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.
57. Sparkes, I.A., Runions, J., Kearns, A. and Hawes, C. (2006) Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nat Protoc, 1, 2019-2025.
58. Stracke, R., Werber, M. and Weisshaar, B. (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr. Opin. Plant Biol. 4, 447-456.
59. 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.
60. Taylor, L.P. and Grotewold, E. (2005) Flavonoids as developmental regulators. Curr. Opin. Plant Biol. 8, 317-323.
61. Treutter, D. (1989) Chemical reaction detection of catechins and proanthocyanidins with 4-dimethylaminocinnamaldehyde. J. Chromatogr. 467, 185-193.
62. Veit, M. and Pauli, G.F. (1999) Major flavonoids from Arabidopsis thaliana leaves. J. Nat. Prod. 62, 1301-1303.
63. 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.
64. Weigel, D., Ahn, J.H., Blazquez, M.A., Borevitz, J.O., Christensen, S.K., Fankhauser, C., Ferrandiz, C., Kardailsky, I., Malancharuvil, E.J., Neff, M.M., Nguyen, J.T., Sato, S., Wang, Z.Y., Xia, Y., Dixon, R.A., Harrison, M.J., Lamb, C.J., Yanofsky, M.F. and Chory, J. (2000) Activation tagging in Arabidopsis. Plant Physiol. 122, 1003-1013.
65. Winkel-Shirley, B. (2001) Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol. 126, 485-493.
66. Winkel-Shirley, B. (2002) Biosynthesis of flavonoids and effects of stress. Curr. Opin. Plant Biol. 5, 218-223.
67. Winter, D., Vinegar, B., Nahal, H., Ammar, R., Wilson, G.V. and Provart, N.J. (2007) An "Electronic Fluorescent Pictograph" Browser for Exploring and Analyzing Large-Scale Biological Data Sets. PLoS ONE, 2, e718. doi:
68. Yamamoto, Y.Y., Deng, X. and Matsui, M. (2001) CIP4, a new COP1 target, is a nucleus-localized positive regulator of Arabidopsis photmorphogenesis. Plant Cell, 13, 399-411.
69. 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.