Skip to main content
Log in

A maize QTL for silk maysin levels contains duplicated Myb-homologous genes which jointly regulate flavone biosynthesis

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

The maize p1 locus coincides with a major QTL (quantitative trait locus) determining levels of maysin, a C-glycosyl flavone that deters feeding by corn ear-worm. The p1 gene is tightly linked with a second gene, p2, and both genes encode similar Myb-domain proteins. We show here that maize cell cultures transformed with either the p1or p2 genes expressed under a constitutive promoter accumulate transcripts for flavonoid biosynthetic genes, and synthesize phenylpropanoids and C-glycosyl flavones related to maysin. Additionally, maize plants that are deleted for the p1 gene have reduced maysin levels and moderate silk-browning reaction, whereas plants with a deletion of both p1 and p2 have non-detectable silk maysin and non-browning silks. We conclude that both p1 and p2 induce maysin biosynthesis in silk, although the two genes differ in their expression and pigmentation effects in other tissues. These results show that a QTL for flavone biosynthesis actually comprises two tightly linked genes with related functions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Arabidopsis Genome Initiative 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796–815.

    Google Scholar 

  • Athma, P. and Peterson, T. 1991. Ac induces homologous recombination at the maize P locus. Genetics 128: 163–173.

    Google Scholar 

  • Bruce,W. Folkerts, O., Garnaat, C., Crasta, O., Roth, B. and Bowen, B. 2000. Expression profiling of the maize flavonoid pathway genes controlled by estradiol-inducible transcription factors CRC and P. Plant Cell 12: 65–79.

    Google Scholar 

  • Byrne, P.F., Darrah, L.L., Snook, M.E., Wiseman, B.R., Widstrom, N.W., Moellenbeck, D.J. and Barray, B.D. 1996a. Maize silkbrowning, maysin content, and antibiosis to the corn earworm, Helicoverpa zea (Boddie). Maydica 41: 13–18.

    Google Scholar 

  • Byrne, P., McMullen, M., Snook, M., Musket, T., Theuri, J., Widstrom, N., Wiseman, B. and Coe, E. 1996b. Quantitative trait loci and metabolic pathways: genetic control of the concentration of maysin, a corn earworm resistance factor, in maize silks. Proc. Natl. Acad. Sci. USA 93: 8820–8825.

    Google Scholar 

  • Byrne, P.F., McMullen, M.D., Wiseman, B.R., Snook, M.E., Musket, T.A., Theuri, J.M, Widstrom, N.W. and Coe, E.H. 1997. Identification of maize chromosome regions associated with antibiosis to corn earworm (Lepidoptera: Noctuidae) larvae. J. Econ. Entomol. 90: 1039–1045.

    Google Scholar 

  • Byrne, P.F., McMullen, M.D., Wiseman, B.R., Snook, M.E. Musket, T.A. 1998. Maize silk maysin concentration and corn earworm antibiosis: QTLs and genetic mechanisms. Crop Sci. 38: 461–471.

    Google Scholar 

  • Carroll, K., Guthrie, N., So, F., and Chanbers, A. 1998. Anticancer properties of flavonoids, with emphasis on citrus flavonoids. In: C.A. Rice-Evans and L. Packer (Eds.) Flavonoids in Health and Disease, Marcel Dekker, New York, pp. 437–447.

    Google Scholar 

  • Chopra, S., Athma, P. and Peterson, T. 1996. Alleles of the maize P gene with distinct tissue specificities encode myb-homologous proteins with C-terminal replacements. Plant Cell 8: 1149–1158.

    Google Scholar 

  • Chopra, S., Athma, P. and Peterson, T. 1998. A maize Myb-homolog is encoded by a stable multicopy gene complex. Mol. Gen. Genet. 260: 372–380.

    Google Scholar 

  • Christensen, A. and Quail, P. 1996. Ubiquitin promoter-based vectors for high-level expression of selectable and/or screenable marker genes in monocotyledonous plants. Transgen. Res. 5: 213–218.

    Google Scholar 

  • Cocciolone, S.M., Sidorenko, L.V., Chopra, S., Dixon, P.M. and Peterson T. 2000. Hierarchical patterns of transgene expression indicate involvement of developmental mechanisms in the regulation of the maize P1-rr promoter. Genetics 156: 839–846.

    Google Scholar 

  • Cocciolone, S.M., Chopra, S., Flint-Garcia, S.A., McMullen, M.D. and Peterson, T. 2001. Tissue-specific patterns of a maize Myb transcription factor are epigenetically regulated. Plant J. 27: 467–478.

    Google Scholar 

  • Cone, K.C., Cocciolone, S.M., Burr, F.A. and Burr, B. 1993. Maize anthocyanin regulatory gene Pl is a duplicate of C1 that functions in the plant. Plant Cell 5: 1795–1805.

    Google Scholar 

  • Deboo, G., Albertsen, M. and Taylor, L. 1995. Flavanone 3-hydroxylase transcripts and flavonol accumulation are temporally coordinate in maize anthers. Plant Cell 7: 703–713.

    Google Scholar 

  • Dooner, H.K., Robbins, T.P. and Jorgensen, R.A. 1991. Genetic and developmental control of anthocyanin biosynthesis. Annu. Rev. Genet. 25: 173–199.

    Google Scholar 

  • Force, A., Lynch, M., Pickett, F.B., Amores, A., Yan, Y.-l. and Postlethwait, J. 1999. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151: 1531–1545.

    Google Scholar 

  • Gordon-Kamm, W.J., Baszczynski, C.L., Bruce, W.B. and Tomes, D.T. 1999. Transgenic cereals - Zea mays (maize). In: I. K. Vasil (Ed.) Molecular Improvement of Cereal Crops, Kluwer Academic Publishers, Dordrecht, Netherlands, pp. 189–253.

    Google Scholar 

  • Grotewold, E., Athma, P. and Peterson, T. 1991. Alternatively spliced products of the maize P gene encode proteins with homology to the DNA-binding domain of myb-like transcription factors. Proc. Natl. Acad. Sci. USA 88: 4587–4591.

    Google Scholar 

  • Grotewold, E., Drummond, B. J., Bowen, B. and Peterson, T. 1994. The myb-homologous P gene controls phlobaphene pigmentation in maize floral organs by directly activating a flavonoid biosynthetic gene subset. Cell 76: 543–553.

    Google Scholar 

  • Grotewold, E., Chamberlin, M., Snook, M., Siame, B., Butler, L., Swenson, J., Maddock, S., Clair, G. and Bowen, B. 1998. Engineering secondary metabolism in maize cells by ectopic expression of transcription factors. Plant Cell 10: 721–740.

    Google Scholar 

  • Grotewold, E., Sainz, M.B., Tagliani, L., Hernandes, J.M., Bowen, B. and Chandler, V.L. 2000. Identification of the residues in the Myb domain of maize C1 that specify the interaction with the bHLH cofactor R. Proc. Natl. Acad. Sci. USA 97: 13579–13584.

    Google Scholar 

  • Guo, B.Z., Zhang, Z.J., Li, R.G., Widstrom, N.W., Snook, M.E., Lynch, R.E. and Plaisted, D. 2001. Restriction fragment length polymorphism markers associated with silk maysin, antibiosis to corn earworm (Lepidoptera: Noctuidae) larvae, in a dent and sweet corn cross. J. Econ. Entomol. 94: 564–571.

    Google Scholar 

  • Harborne, J.B. and Corner, J.J. 1961. Plant polyphenols: hydroxycinnamic acid-sugar derivatives. Biochem. J. 81: 242–250.

    Google Scholar 

  • Kermicle, J.L. 1980. Probing the component structure of a maize gene with transposable elements. Science 208: 1457–1459.

    Google Scholar 

  • Koes, R.E., Quattrocchio, F. and Mol, J.N. 1994. The flavonoid biosynthetic pathway in plants: function and evolution. BioEssays 16: 123–132.

    Google Scholar 

  • Lee, E.A., Byrne, P.F., McMullen, M.D., Snook, M.E., Wiseman, B.R., Widstrom, N.W. and Coe, E.H. 1998. Genetic mechanisms underlying apimaysin and maysin synthesis and corn earworm antibiosis in maize (Zea mays L.) Genetics 149: 1997–2006.

    Google Scholar 

  • Levings, C.S. and Stuber, C.W. 1971. A maize gene controlling silk browning in response to wounding. Genetics 69: 491–498.

    Google Scholar 

  • Lynch, M. and Force, A. 2000. The probability of duplicate gene preservation by subfunctionalization. Genetics 154: 459–473.

    Google Scholar 

  • Mo, Y., Nagel, C. and Taylor, L. 1992. Biochemical complementation of chalcone synthase mutants defines a role for flavonols in functional pollen. Proc. Natl. Acad. Sci. USA 89: 7213–7217.

    Google Scholar 

  • Mol., J., Grotewold, E. and Koes, R. 1998. How genes paint flowers and seeds. Trends Plant Sci. 3: 212–217.

    Google Scholar 

  • Moyano, E., Martinnez-Garcia, J. and Martin, C. 1996. Apparent redundancy in myb gene function provides gearing for the control of flavonoid biosynthesis in antirrhinum flowers. Plant Cell 8: 1519–1532.

    Google Scholar 

  • Napoli, C.A., Fahy, D., Wang, H.Y. and Taylor, L.P. 1999. White anther: a petunia mutant that abolishes pollen flavonol accumulation, induces male sterility, and is complemented by a chalcone synthase transgene. Plant Physiol. 120: 615–622.

    Google Scholar 

  • Nash, J., Luehrsen, K.R. and Walbot, V. 1990. Bronze-2 gene of maize: reconstruction of a wild-type allele and analysis of transcription and splicing. Plant Cell 2: 1039–1049.

    Google Scholar 

  • 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.

    Google Scholar 

  • Samman, S., Wall, P. and Cook, N. 1998. Flavonoids and coronary heart disease: dietary perspectives. In: C.A. Rice-Evans and L. Packer (Eds.) Flavonoids in Health and Disease, Marcel Dekker, New York, pp. 469–483.

    Google Scholar 

  • Schwarz-Sommer, Z., Shepherd, N., Tacke, E., Gierl, A., Rohde, W., Leclercq, L., Mattes, M., Berndtgen, R., Peterson, P.A., and Saedler, H. 1987. Influence of transposable elements on the structure and function of the A1 gene of Zea mays. EMBO J. 6: 287–294.

    Google Scholar 

  • Shih, C.Y., Dumbroff, E.B. and Thompson, J.E. 1989. Identification of a naturally occurring inhibitor of the conversion of 1-aminocyclopropane-1-carboxylic acid to ethylene by carnation microsomes. Plant Physiol. 89: 1053–1059.

    Google Scholar 

  • Sidorenko, L.V., Li, X., Cocciolone, S.M., Tagliani, L., Chopra, S., Bowen, B., Daniels, M. and Peterson, T. 2000. Complex structure of a maize Myb gene promoter: functional analysis in transgenic plants. Plant J. 22: 471–482.

    Google Scholar 

  • Snook, M.E., Widstrom, N.W. and Gueldner, R.C. 1989. Reversedphase high-performance liquid chromatographic procedure for the determination of maysin in corn silks. J. Chromatogr. 477: 439–447.

    Google Scholar 

  • Stafford, H.A. 1998. Teosinte to maize: some aspects of missing biochemical and physiological data concerning regulation of flavonoid pathways. Phytochemistry 49: 285–293.

    Google Scholar 

  • Styles, E.D. and Ceska, O. 1989. Pericarp flavonoids in genetic strains of Zea mays. Maydica 34: 227–237.

    Google Scholar 

  • van der Meer, I.M., Stam, M.E., van Tunen, A.J., Mol, J.N. and Stuitje, A.R. 1992. Antisense inhibition of flavonoid biosynthesis in petunia anthers results in male sterility. Plant Cell 4: 253–262.

    Google Scholar 

  • Villemur, R., Joyce, M., Haas, N.A., Goddard, R.H., Kopczak, S.D., Hussey, P.J., Snustad, D.P. and Silflow, C. 1992. α-Tubulin gene family of maize. Evidence for two ancient α-tubulin genes in plants. J. Mol. Biol. 227: 81–96.

    Google Scholar 

  • Wienand, U., Weydemann, U., Niesbach-Klosgen, U., Peterson, P. and Saedler, H. 1986. Molecular cloning of the c2 locus of Zea mays, the gene encoding chalcone synthase. Mol. Gen. Genet. 203: 202–207.

    Google Scholar 

  • Ylstra, B., Muskens, M. and van Tunen, A.J. 1996. Flavonols are not essential for fertilization in Arabidopsis thaliana. Plant Mol. Biol. 32: 1155–1158.

    Google Scholar 

  • Xiao, Y., Li, X. and Peterson T. 2000. Ac insertion site affects the frequency of transposon-induced homologous recombination at the maize P locus. Genetics 156: 2007–2017.

    Google Scholar 

  • Zhang, J. and Peterson, T. 1999. Genome rearrangements by nonlinear transposons in maize. Genetics 153: 1403–1410.

    Google Scholar 

  • Zhang, P., Chopra, S. and Peterson T. 2000. A segmental gene duplication generated differentially expressed Myb-homologous genes in maize. Plant Cell 12: 2311–2322.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Thomas Peterson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, P., Wang, Y., Zhang, J. et al. A maize QTL for silk maysin levels contains duplicated Myb-homologous genes which jointly regulate flavone biosynthesis. Plant Mol Biol 52, 1–15 (2003). https://doi.org/10.1023/A:1023942819106

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1023942819106

Navigation