Evidence for Direct Activation of an Anthocyanin Promoter by the Maize C1 Protein and Comparison of DNA Binding by Related Myb Domain Proteins

Overview

Journal Plant Cell

Publisher Oxford University Press

Specialties Biology
Cell Biology

Date 1997 Apr 1

PMID 9144964

Citations 82

Authors

M B Sainz

E Grotewold

V L CHANDLER

Affiliations

Soon will be listed here.

Abstract

The enzyme-encoding genes of two classes of maize flavonoid pigments, anthocyanins and phlobaphenes, are differentially regulated by distinct transcription factors. Anthocyanin biosynthetic gene activation requires the Myb domain C1 protein and the basic helix-loop-helix B or R proteins. In the phlobaphene pathway, a subset of C1-regulated genes, including a1, are activated by the Myb domain P protein independently of B/R. We show sequence-specific binding to the a1 promoter by C1 in the absence of B. Activation is decreased by mutations in the C1 DNA binding domain or in a1 sequences bound by C1, providing direct evidence for activation of the anthocyanin biosynthetic genes by C1. The two C1 binding sites in the a1 promoter are also bound by P. One site is bound with higher affinity by P relative to C1, whereas the other site is bound with similar lower affinity by both proteins. Interestingly, either site is sufficient for C1 plus B/R or P activation in vivo, demonstrating that differences in DNA binding affinities between P and C1 are insufficient to explain the differential requirement for B. Results of DNA binding site-selection experiments suggest that C1 has a broader DNA binding specificity than does P, which may help C1 to activate a more diverse set of promoters.

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References

Patterson G, Thorpe C, CHANDLER V . Paramutation, an allelic interaction, is associated with a stable and heritable reduction of transcription of the maize b regulatory gene. Genetics. 1993; 135(3):881-94. PMC: 1205727. DOI: 10.1093/genetics/135.3.881. View

Roth B, Goff S, Klein T, Fromm M . C1- and R-dependent expression of the maize Bz1 gene requires sequences with homology to mammalian myb and myc binding sites. Plant Cell. 1991; 3(3):317-25. PMC: 160002. DOI: 10.1105/tpc.3.3.317. View

Pollock R, Treisman R . A sensitive method for the determination of protein-DNA binding specificities. Nucleic Acids Res. 1990; 18(21):6197-204. PMC: 332481. DOI: 10.1093/nar/18.21.6197. View

Shieh M, Wessler S, Raikhel N . Nuclear targeting of the maize R protein requires two nuclear localization sequences. Plant Physiol. 1993; 101(2):353-61. PMC: 160579. DOI: 10.1104/pp.101.2.353. View

Williams C, Grotewold E . Differences between plant and animal Myb domains are fundamental for DNA binding activity, and chimeric Myb domains have novel DNA binding specificities. J Biol Chem. 1997; 272(1):563-71. DOI: 10.1074/jbc.272.1.563. View

Ludwig S, Habera L, Dellaporta S, Wessler S . Lc, a member of the maize R gene family responsible for tissue-specific anthocyanin production, encodes a protein similar to transcriptional activators and contains the myc-homology region. Proc Natl Acad Sci U S A. 1989; 86(18):7092-6. PMC: 298000. DOI: 10.1073/pnas.86.18.7092. View

Paz-Ares J, Ghosal D, Saedler H . Molecular analysis of the C1-I allele from Zea mays: a dominant mutant of the regulatory C1 locus. EMBO J. 1990; 9(2):315-21. PMC: 551668. DOI: 10.1002/j.1460-2075.1990.tb08113.x. View

Howe K, Reakes C, Watson R . Characterization of the sequence-specific interaction of mouse c-myb protein with DNA. EMBO J. 1990; 9(1):161-9. PMC: 551642. DOI: 10.1002/j.1460-2075.1990.tb08092.x. View

Cone K, Cocciolone S, Burr F, Burr B . Maize anthocyanin regulatory gene pl is a duplicate of c1 that functions in the plant. Plant Cell. 1993; 5(12):1795-805. PMC: 160405. DOI: 10.1105/tpc.5.12.1795. View

10.

Goff S, Klein T, Roth B, Fromm M, Cone K, Radicella J . Transactivation of anthocyanin biosynthetic genes following transfer of B regulatory genes into maize tissues. EMBO J. 1990; 9(8):2517-22. PMC: 552281. DOI: 10.1002/j.1460-2075.1990.tb07431.x. View

11.

Grotewold E, Athma P, Peterson T . 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 U S A. 1991; 88(11):4587-91. PMC: 51710. DOI: 10.1073/pnas.88.11.4587. View

12.

Dooner H, Robbins T, Jorgensen R . Genetic and developmental control of anthocyanin biosynthesis. Annu Rev Genet. 1991; 25:173-99. DOI: 10.1146/annurev.ge.25.120191.001133. View

13.

Lois R, Dietrich A, Hahlbrock K, Schulz W . A phenylalanine ammonia-lyase gene from parsley: structure, regulation and identification of elicitor and light responsive cis-acting elements. EMBO J. 1989; 8(6):1641-8. PMC: 401003. DOI: 10.1002/j.1460-2075.1989.tb03554.x. View

14.

Klein T, Roth B, Fromm M . Regulation of anthocyanin biosynthetic genes introduced into intact maize tissues by microprojectiles. Proc Natl Acad Sci U S A. 1989; 86(17):6681-5. PMC: 297909. DOI: 10.1073/pnas.86.17.6681. View

15.

Callis J, Fromm M, Walbot V . Introns increase gene expression in cultured maize cells. Genes Dev. 1987; 1(10):1183-200. DOI: 10.1101/gad.1.10.1183. View

16.

Abate C, Luk D, Gentz R, Rauscher 3rd F, Curran T . Expression and purification of the leucine zipper and DNA-binding domains of Fos and Jun: both Fos and Jun contact DNA directly. Proc Natl Acad Sci U S A. 1990; 87(3):1032-6. PMC: 53404. DOI: 10.1073/pnas.87.3.1032. View

17.

Weintraub H, Davis R, Tapscott S, Thayer M, Krause M, Benezra R . The myoD gene family: nodal point during specification of the muscle cell lineage. Science. 1991; 251(4995):761-6. DOI: 10.1126/science.1846704. View

18.

Sablowski R, Moyano E, Culianez-Macia F, Schuch W, Martin C, Bevan M . A flower-specific Myb protein activates transcription of phenylpropanoid biosynthetic genes. EMBO J. 1994; 13(1):128-37. PMC: 394786. DOI: 10.1002/j.1460-2075.1994.tb06242.x. View

19.

Bodeau J, Walbot V . Regulated transcription of the maize Bronze-2 promoter in electroporated protoplasts requires the C1 and R gene products. Mol Gen Genet. 1992; 233(3):379-87. DOI: 10.1007/BF00265434. View

20.

Gill G, Ptashne M . Mutants of GAL4 protein altered in an activation function. Cell. 1987; 51(1):121-6. DOI: 10.1016/0092-8674(87)90016-x. View