Abstract
Flavonol 3-O-galactosyltransferase (F3GalTase) is a pollen-specific enzyme which glycosylates the flavonols required for germination in petunia. The highly restricted tissue-specific expression and substrate usage make F3GalTase unique among all other flavonoid glycosyltransferases (GTs) described to date, including the well characterized Bronze1 (Bz1) gene of maize. RFLP mapping, DNA gel blot, and sequence analyses showed that the single copy F3galtase gene has a different genomic organization than Bz1. Within the promoter of F3galtase are potential regulatory motifs which may confer pollen-specific gene expression and activation by Myb and bHLH transcription factors. However, we provide evidence that F3galtase is not regulated by An4, which encodes a Myb factor known to regulate anthocyanin accumulation in petunia anthers. An unexpected feature of the F3galtase promoter was the presence of large blocks of chloroplast and mitochondrial DNA. Gel blot analyses of genomic DNA from the progenitors of Petunia hybrida, as well as from Nicotiana tabacum, indicated that migration of organellar DNA into the F3galtase gene was an ancient event that occurred prior to speciation of the Solanaceae. Together with enzyme assays and HPLC analyses of pollen extracts from tobacco, tomato, and potato, these results confirmed that the unique F3galtase gene structure, enzyme activity, and pollen-specific flavonol glucosylgalactosides are conserved throughout the Solanaceae.
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References
Blanchard, J.L. and Schmidt, G.W. 1995. Pervasive migration of organellar DNA to the nucleus in plants. J. Mol. Evol. 41: 397–406.
Ceska, O. and Styles, E.D. 1984. Flavonoids from Zea mays pollen. Phytochemistry 23: 1822–1823.
Coe, E.H. Jr., McCormick, S.M. and Modena, S.A. 1981. White pollen in maize. J. Hered. 72: 318–320.
Eyal, Y., Curie, C. and McCormick, S. 1995. Pollen specificity elements reside in 30 bp of the proximal promoters of two pollen-expressed genes. Plant Cell. 7: 373–384.
Ford, C.M., Boss, P.K. and Høj, P.B. 1998. Cloning and characterization of Vitis vinifera UDP-glucose:flavonoid 3-Oglucosyltransferase, a homologue of the enzyme encoded by the maize bronze-1 locus that may primarily serve to glycosylate anthocyanidins in vivo. J. Biol. Chem. 273: 9224–9233.
Furtek, D., Schiefelbein, J.W., Johnston, F. and Nelson, O.E. Jr. 1988. Sequence comparison of three wild-type Bronze-1 alleles from Zea mays. Plant Mol. Biol. 11: 473–481.
Gerats, A.G.M., Vrijlandt, E., Wallroth, M. and Schram, A.W. 1985. The influence of the genes An1, An2, and An4 on the activity of the enzyme UDP-glucose:flavonoid 3-O-glucosyltransferase in flowers of Petunia hybrida. Biochem. Genet. 23: 591–598.
Huits, H.S., Gerats, A.G., Kreike, M.M., Mol, J.N., Koes, R.E. 1994. Genetic control of dihydroflavonol reductase gene expression in Petunia hybrida. Plant J. 6: 295–310.
Kapitonov, D. and Yu, R.K. 1999. Conserved domains of glycosyltransferases. Glycobiology 9: 961–978.
Lee, H.-S., Singh, A. and Kao, T.-h. 1992. Rnase X2, a pistilspecific ribonuclease from Petunia inflata, shares sequence similarity with solanaceous S proteins. Plant Mol. Biol. 20: 1131–1141.
Li, Y., Baldauf, S., Lim, E.-K. and Bowles, D.J. 2001. Phylogenetic analysis of the UDP-glycosyltransferase multigene family of Arabidopsis thaliana. J. Biol. Chem. 276: 4338–4343.
McKnight, S.L., Gavis, E.R., Kingsbury, R. and Axel, R. 1981. Analysis of transcriptional regulatory signals of the HSV thymidine kinase gene: identification of an upstream control region. Cell 25: 385–398.
Miller, K.D., Guyon, V., Evans, J.N.S., Shuttleworth, W.A. and Taylor, L.P. 1999. Purification, cloning, and heterologous expression of a catalytically efficient flavonol 3-O-galactosyltransferase expressed in the male gametophyte of Petunia hybrida. J. Biol. Chem. 274: 34011–34019
Mo, Y., Nagel, C. and Taylor, L.P. 1992. Biochemical complementation of chalcone synthase mutants defines a role for flavonols in functional pollen. Proc. Natl. Acad. Sci. USA. 89: 7213–7217.
Pollak, P.E., Hansen, K, Astwood, J.D. and Taylor, L.P. 1995. Conditional male fertility in maize. Sex. Plant Reprod. 8: 231–241.
Ralston, E.J., English, J.J. and Dooner, H.K. 1988. Sequence of three bronze alleles of maize and correlation with the genetic fine structure. Genetics 119: 185–197.
Sainz, M., Grotewold, E. and Chandler, V. 1997. Evidence for direct activation on an anthocyanin promoter by the maize C1 protein and comparison of DNA binding by related Myb-domain proteins. Plant Cell 9: 611–625.
Sink, K.C. 1984. Taxonomy. In: K.C. Sink (Ed.) Petunia. Springer-Verlag, Berlin, pp. 3–9.
Spelt, C., Quattrocchio, F., Mol, J.N.M. and Koes, R. 2000. anthocyanin1 of Petunia encodes a basic helix-loop-helix protein that directly activates transcription of structural anthocyanin genes. Plant Cell 12: 1619–1631.
Strommer, J., Gerats, A.G.M., Sanago, M. and Molnar S.J. 2000. A gene-based RFLP map of petunia. Theor. Appl. Genet. 100: 899–906.
Taylor, L.P. and Hepler, P.K. 1997. Pollen germination and tube growth. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48: 461–491.
Taylor, L.P. and Jorgensen, R. 1992. Conditional male fertility in chalcone synthase-deficient petunia. J. Hered. 83: 11–17.
Vogt, T, and Taylor, L.P. 1995. Flavonol 3-O-glycosyltransferases associated with petunia pollen produce gametophyte-specific flavonol diglycosides. Plant Physiol. 108: 903–911.
Vogt, T., Wollenweber, E. and Taylor L.P. 1995. The structural requirements of flavonols that induce pollen germination of conditionally male fertile Petunia. Phytochemistry 38: 589–592.
Vogt, T. and Jones, P. 2000. Glycosyltransferases in plant natural product synthesis: characterization of a supergene family. Trends Plant Sci. 5(9): 380–386.
Wise, R.P., Rohde, W. and Salamini, F. 1990. Nucleotide sequence of the Bronze-1 homologous gene from Hordeum vulgare. Plant Mol. Biol. 14: 277–279.
Woo, H.-H., Orbach, M.J., Hirsch, A.M. and Hawes, M.C. 1999. Meristem-localized inducible expression of a UDPglycosyltransferase gene is essential for growth and development in pea and alfalfa. Plant Cell. 11: 2303–2315.
Ylstra, B., Turaev, A., Benito Moreno, R.M., Stöger, E., van Tunen, A.J., Vicente, O., Mol, J.N.M. and Heberle-Bors, E. 1992. Flavonols stimulate development, germination and tube growth of tobacco pollen. Plant Physiol. 100: 902–907.
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Miller, K.D., Strommer, J. & Taylor, L.P. Conservation in divergent solanaceous species of the unique gene structure and enzyme activity of a gametophytically-expressed flavonol 3-O-galactosyltransferase1. Plant Mol Biol 48, 233–242 (2002). https://doi.org/10.1023/A:1013307231758
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DOI: https://doi.org/10.1023/A:1013307231758