A bHLH regulatory gene in the common morning glory, Ipomoea purpurea, controls anthocyanin biosynthesis in flowers, proanthocyanidin and phytomelanin pigmentation in seeds, and seed trichome formation

Plant Journal

Volumn 49, Issue 4, 2007, Pages 641-654

  Park, Kyeung Il ^a   Ishikawa, Naoko ^a   Morita, Yasumasa ^a   Choi, Jeong Doo ^a,b   Hoshino, Atsushi ^a   Iida, Shigeru ^a  

^a NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

^b Gyeongbuk Institute for Bio industry   (South Korea)

Author keywords

Anthocyanin pigmentation; bHLH transcriptional regulator; Ipomoea purpurea; Phytomelanin accumulation; Proanthocyanidin biosynthesis; Trichome formation

Indexed keywords

BIOSYNTHESIS; GENES; PIGMENTS; PROTEINS; SEED;

ANTHOCYANIN PIGMENTATION; BHLH TRANSCRIPTIONAL REGULATOR; IPOMOEA PURPUREA; PHYTOMELANIN ACCUMULATION; PROANTHOCYANIDIN BIOSYNTHESIS; TRICHOME FORMATION;

PLANTS (BOTANY);

ANTHOCYANIN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; MELANIN; PIGMENT; PROANTHOCYANIDIN; VEGETABLE PROTEIN;

ARTICLE; BIOLOGICAL MODEL; BIOSYNTHESIS; FLOWER; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; IPOMOEA; METABOLISM; MOLECULAR GENETICS; MUTATION; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PLANT SEED; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANTHOCYANINS; BASE SEQUENCE; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BLOTTING, NORTHERN; FLOWERS; GENE EXPRESSION REGULATION, PLANT; IPOMOEA; MELANINS; MODELS, BIOLOGICAL; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; MUTATION; PIGMENTS, BIOLOGICAL; PLANT PROTEINS; PROANTHOCYANIDINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEEDS;

BIOSYNTHESIS; GENES; PIGMENT; PLANTS; PROTEINS; SEEDS;

IPOMOEA; IPOMOEA PURPUREA; PETUNIA;

EID: 33846935526     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2006.02988.x     Document Type: Article

References (62)

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. Alfenito, M.R., Souer, E., Goodman, C.D., Buell, R., Mol, J., Koes, R. and Walbot, V. (1998) Functional complementation of anthocyanin sequestration in the vacuole by widely divergent glutathione S-transferases. Plant Cell, 10, 1135-1149.
3. Austin, D.F. and Huáman, Z. (1996) A synopsis of Ipomoea (Convolvulaceae) in the Americas. Taxon, 45, 3-38.
4. Belostotsky, D.A. and Rose, A.B. (2005) Plant gene expression in the age of systems biology: integrating transcriptional and posttranscriptional events. Trends Plant Sci. 10, 347-353.
5. 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.
6. Chang, S.M., Lu, Y. and Rausher, M.D. (2005) Neutral evolution of the nonbinding region of the anthocyanin regulatory gene Ipmyb1 in Ipomoea. Genetics, 170, 1967-1978.
7. Chopra, S., Hoshino, A., Boddu, J. and Iida, S. (2006) Flavonoid pigments as tools in molecular genetics. In The Science of Flavonoids (Glotewold, E., ed.). New York: Springer, pp. 147-173.
8. Clegg, M.T. and Durbin, M.L. (2003) Tracing floral adaptations from ecology to molecules. Nature Rev. Genet. 4, 206-215.
9. Debeaujon, I., Léon-Kloosterziel, K.M. and Koornneef, M. (2000) Influence of the testa on seed dormancy, germination, and longevity in Arabidopsis. Plant Physiol. 122, 403-413.
10. 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.
11. Downie, A.B., Zhang, D., Dirk, L.M.A., Thacker, R.R., Pfeiffer, J.A., Drake, J.L., Levy, A.A., Butterfield, D.A., Buxton, J.W. and Snyder, J.C. (2003) Communication between the maternal testa and the embryo and/or endosperm affect testa attributes in tomato. Plant Physiol. 133, 145-160.
12. Durbin, M.L., McCaig, B. and Clegg, M.T. (2000) Molecular evolution of the chalcone synthase multigene family in the morning glory genome. Plant Mol. Biol. 42, 79-92.
13. Durbin, M.L., Denton, A.L. and Clegg, M.T. (2001) Dynamics of mobile element activity in chalcone synthase loci in the common morning glory (Ipomoea purpurea). Proc. Natl Acad. Sci. USA, 98, 5084-5089.
14. Ennos, R.A. and Clegg, M.T. (1983) Flower color variation in the morning glory, Ipomoea purpurea. J. Hered. 74, 247-250.
15. Fogarty, R.V. and Tobin, J.M. (1996) Fungal melanins and their interactions with metals. Enzyme Microbial Technol. 19, 311-317.
16. Fukada-Tanaka, S., Hoshino, A., Hisatomi, Y., Habu, Y., Hasebe, M. and Iida, S. (1997) Identification of new chalcone synthase genes for flower pigmentation in the Japanese and common morning glories. Plant Cell Physiol. 38, 754-758.
17. Fukada-Tanaka, S., Inagaki, Y., Yamaguchi, T., Saito, N. and Iida, S. (2000) Colour-enhancing protein in blue petals. Nature, 407, 581.
18. Habu, Y., Hisatomi, Y. and Iida, S. (1998) Molecular characterization of the mutable flaked allele for flower variegation in the common morning glory. Plant J. 16, 371-376.
19. Harki, E., Talou, T. and Dargent, R. (1997) Purification, characterisation and analysis of melanin extracted from Tuber melanosporum Vitt. Food Chem. 58, 69-73.
20. Hisatomi, Y., Yoneda, Y., Kasahara, K., Inagaki, Y. and Iida, S. (1997) DNA rearrangements at the region of the dihydroflavonol 4-reductase gene for flower pigmentation and incomplete dominance in morning glory carrying the mutable flaked mutation. Theor. Appl. Genet. 95, 509-515.
21. Hoshino, A., Abe, Y., Saito, N., Inagaki, Y. and Iida, S. (1997) The gene encoding flavanone 3-hydroxylase is expressed normally in the pale yellow flowers of the Japanese morning glory carrying the speckled mutation which produce neither flavonol nor anthocyanin but accumulate chalcone, aurone and flavanone. Plant Cell Physiol. 38, 970-974.
22. Hoshino, A., Johzuka-Hisatomi, Y. and Iida, S. (2001) Gene duplication and mobile genetic elements in the morning glories. Gene, 265, 1-10.
23. Hoshino, A., Morita, Y., Choi, J.D., Saito, N., Toki, K., Tanaka, Y. and Iida, S. (2003) Spontaneous mutations of the flavonoid 3prime;-hydroxylase gene conferring reddish flowers in the three morning glory species. Plant Cell Physiol. 44, 990-1001.
24. Iida, S., Hoshino, A., Johzuka-Hisatomi, Y., Habu, Y. and Inagaki, Y. (1999) Floricultural traits and transposable elements in the Japanese and common morning glories. Ann. NY Acad. Sci. 870, 265-274.
25. Iida, S., Morita, Y., Choi, J.D., Park, K.I. and Hoshino, A. (2004) Genetics and epigenetics in flower pigmentation associated with transposable elements in morning glories. Adv. Biophys. 38, 141-159.
26. Imai, Y. (1927) The genetics of Pharbitis purpurea. J. Coll. Agric. Imp. Univ. Tokyo, 9, 199-222.
27. Irani, N.G., Hernandez, J.M. and Grotewold, E. (2003) Regulation of anthocyanin pigmentation. Recent Adv. Phytochem. 37, 59-78.
28. Ishikawa, N., Johzuka-Hisatomi, Y., Sugita, K., Ebinuma, H. and Iida, S. (2002) The transposon Tip100 from the common morning glory is an autonomous element that can transpose in tobacco plants. Mol. Genet. Genomics, 266, 732-739.
29. Johzuka-Hisatomi, Y., Hoshino, A., Mori, T., Habu, Y. and Iida, S. (1999) Characterization of the chalcone synthase genes expressed in flowers of the common and Japanese morning glories. Genes Genet. Syst. 74, 141-147.
30. Kim, H.J. and Triplett, B.A. (2001) Cotton fiber growth in planta and in vitro. Models for plant cell elongation and cell wall biogenesis. Plant Physiol. 127, 1361-1366.
31. 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.
32. Kondo, T., Kawai, T., Tamura, H. and Goto, T. (1987) Structure determination of heavenly blue anthocyanin, a complex monomeric anthocyanin from the morning glory Ipomoea tricolor, by means of the negative NOE method. Tetrahedron Lett. 28, 2273-2276.
33. Larkin, J.C., Brown, M.L. and Schiefelbein, J. (2003) How do cells know what they want to be when they grow up? Lessons from epidermal pattering in Arabidopsis. Annu. Rev. Plant Biol. 54, 403-430.
34. Lu, T.S., Saito, N., Yokoi, M., Shigihara, A. and Honda, T. (1992) Acylated peonidin glycosides in the violet-blue cultivars of Pharbitis nil. Phytochemistry, 31, 659-663.
35. Marles, M.A.S., Ray, H. and Gruber, M.Y. (2003) New perspectives on proanthocyanidin biochemistry and molecular regulation. Phytochemistry, 64, 367-383.
36. Martin, C. and Gerats, T. (1993) Control of pigment biosynthesis genes during petal development. Plant Cell, 5, 1253-1264.
37. 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.
38. Mol, J., Grotewold, E. and Koes, R. (1998) How genes paint flowers and seeds. Trends Plant Sci. 3, 212-217.
39. Morita, Y., Hoshino, A., Kikuchi, Y. et al. (2005) Japanese morning glory dusky mutants displaying reddish-brown or purplish-gray flowers are deficient in a novel glycosylation enzyme for anthocyanin biosynthesis, UDP-glucose:anthocyanidin 3-O-glucoside-2″-O- glucosyltransferase, due to 4-bp insertions in the gene. Plant J. 42, 353-363.
40. Morita, Y., Saitoh, M., Hoshino, A., Nitasaka, E. and Iida, S. (2006) Isolation of cDNAs for R2R3-MYB, bHLH, and WDR transcriptional regulators and identification of c and ca mutations conferring white flowers in the Japanese morning glory. Plant Cell Physiol. 47, 457-470.
41. 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.
42. 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.
43. Nicolaus, R.A. and Piattelli, M. (1965) Progress in the chemistry of natural black pigments. Rend. Acc. Sci. Fis. Mat. 32, 83-97.
44. + antiporter gene InNHX2 and comparison of InNHX2 with InNHX1, which is responsible for blue flower coloration by increasing the vacuolar pH in the Japanese morning glory. Plant Cell Physiol. 46, 259-267.
45. Pandey, A.K., Wilcox, L.W., Sack, F.D. and Stuessy, F. (1989) Development of the phytomelanin layer in fruits of Ageratum conyzoides (Compositae). Am. J. Bot. 76, 739-746.
46. Park, K.I., Choi, J.D., Hoshino, A., Morita, Y. and Iida, S. (2004) An intragenic tandem duplication in a transcriptional regulatory gene for anthocyanin biosynthesis confers pale-colored flowers and seeds with fine spots in Ipomoea tricolor. Plant J. 38, 840-849.
47. Quattrocchio, F., Wing, J.F., van der Woude, K., Mol, J.N.M. and Koes, R. (1998) Analysis of bHLH and MYB domain proteins: species-specific regulatory differences are caused by divergent evolution of target anthocyanin genes. Plant J. 13, 475-488.
48. Quattrocchio, F., Wing, J., van der Woude, K., Souer, E., de Vetten, N., Mol, J. and Koes, R. (1999) Molecular analysis of the anthocyanin2 gene of petunia and its role in the evolution of flower color. Plant Cell, 11, 1433-1444.
49. Ramsay, N.A. and Glover, B.J. (2005) MYB-bHLH-WD40 protein complex and the evolution of cellular diversity. Trends Plant Sci. 10, 63-70.
50. Saito, N., Tatsuzawa, F., Yoda, K., Yokoi, M., Kasahara, K., Iida, S., Shigihara, A. and Honda, T. (1995) Acylated cyanidin glycosides in the violet-blue flowers of Ipomoea purpurea. Phytochemistry, 40, 1283-1289.
51. Sava, V.M., Yang, S.-M., Hong, M.-Y., Yang, P.-C. and Huang, G.S. (2001) Isolation and characterization of melanic pigments derived from tea and tea polyphenols. Food Chem. 73, 177-184.
52. Schwinn, K.E. and Davies, K.M. (2004) Flavonoids. In Plant Pigments and Their Manipulation (Davies, K., ed.). Oxford: Blackwell Publishing Ltd, pp. 92-149.
53. Shiokawa, K., Inagaki, Y., Morita, H., Hsu, T.-J., Iida, S. and Noguchi, H. (2000) The functional expression of the CHS-D and CHS-E genes of the common morning glory (Ipomoea purpurea) in Escherichia coli and characterization of their gene products. Plant Biotechnol. 17, 203-210.
54. Spelt, C., Quattrocchio, F., Mol, J. and Koes, R. (2002) ANTHOCYANIN1 of petunia controls pigment synthesis, vacuolar pH, and seed coat development by genetically distinct mechanisms. Plant Cell, 14, 2121-2135.
55. Tanner, G. (2004) Condensed tannins. Annu. Plant Rev. 14, 150-184.
56. 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, 1337-1349.
57. Wang, S., Wang, J.-W., Yu, N., Li, C.-H., Luo, B., Gou, J.-Y., Wang, L.-J. and Chen, X.-Y. (2004) Control of plant trichome development by a cotton fiber MYB gene. Plant Cell, 16, 2323-2334.
58. White, L.N. (1981) Heirlooms and Genetics: 100 Years of Vegetables and Flowers. Cambridge, NY: Cambridge Seed Packet.
59. Xie, D.-Y., Sharma, S.B., Pavia, N.L., Ferreira, D. and Dixon, R.A. (2003) Role of anthocyanidin reductase, encoded by BANYULS in plant flavonoid biosynthesis. Science, 299, 396-399.
60. + exchanger and flower coloration. Plant Cell Physiol. 42, 451-461.
61. Yoshida, K., Kondo, T., Okazaki, Y. and Katou, K. (1995) Cause of blue petal colour. Nature, 373, 291.
62. Zhang, F., Gonzalez, A., Zhao, M., Payne, C.T. and Lloyd, A. (2003) A network of redundant bHLH proteins functions in all TTG1-dependent pathways of Arabidopsis. Development, 130, 4859-4869.