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. 1998 Jun;149(2):1125–1138. doi: 10.1093/genetics/149.2.1125

The maize regulatory gene B-Peru contains a DNA rearrangement that specifies tissue-specific expression through both positive and negative promoter elements.

D A Selinger 1, D Lisch 1, V L Chandler 1
PMCID: PMC1460163  PMID: 9611220

Abstract

The B-Peru allele of the maize b regulatory gene is unusual relative to most b alleles in that it is expressed in the aleurone layer of the seed. It is also expressed in a subset of plant vegetative tissues. Transgenic maize plants containing the B-Peru gene with the first 710 bases of upstream sequence conferred the same levels of aleurone expression as nontransgenic B-Peru plants, but no pigment was made in vegetative tissues. Transient transformation assays in aleurone tissue localized the aleurone-specific promoter to the first 176 bases of the B-Peru upstream region and identified two critically important regions within this fragment. Mutation of either region alone reduced expression greater than fivefold. Surprisingly, the double mutation actually increased expression to twice the native promoter level. Our results suggest that these two critical sequences, which lie close together in the promoter, may form a negative regulatory element. Several lines of evidence suggest that the B-Peru promoter arose through the translocation of an existing aleurone-specific promoter to the b locus. Immediately upstream of the aleurone-specific promoter elements and in the opposite orientation to the b coding sequence is a pseudogene sequence with strong similarity to a known class of proteins. Our findings that novel aleurone-specific promoter sequences of the B-Peru transcription factor are found adjacent to part of another gene in a small insertion are quite unexpected and have interesting evolutionary implications.

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Selected References

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  1. Bodeau J. P., Walbot V. Regulated transcription of the maize Bronze-2 promoter in electroporated protoplasts requires the C1 and R gene products. Mol Gen Genet. 1992 Jun;233(3):379–387. doi: 10.1007/BF00265434. [DOI] [PubMed] [Google Scholar]
  2. Bodeau J. P., Walbot V. Structure and regulation of the maize Bronze2 promoter. Plant Mol Biol. 1996 Nov;32(4):599–609. doi: 10.1007/BF00020201. [DOI] [PubMed] [Google Scholar]
  3. Callis J., Fromm M., Walbot V. Introns increase gene expression in cultured maize cells. Genes Dev. 1987 Dec;1(10):1183–1200. doi: 10.1101/gad.1.10.1183. [DOI] [PubMed] [Google Scholar]
  4. Chandler V. L., Radicella J. P., Robbins T. P., Chen J., Turks D. Two regulatory genes of the maize anthocyanin pathway are homologous: isolation of B utilizing R genomic sequences. Plant Cell. 1989 Dec;1(12):1175–1183. doi: 10.1105/tpc.1.12.1175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chopra S., Athma P., Peterson T. Alleles of the maize P gene with distinct tissue specificities encode Myb-homologous proteins with C-terminal replacements. Plant Cell. 1996 Jul;8(7):1149–1158. doi: 10.1105/tpc.8.7.1149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cone K. C., Burr F. A., Burr B. Molecular analysis of the maize anthocyanin regulatory locus C1. Proc Natl Acad Sci U S A. 1986 Dec;83(24):9631–9635. doi: 10.1073/pnas.83.24.9631. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cone K. C., Cocciolone S. M., Burr F. A., Burr B. Maize anthocyanin regulatory gene pl is a duplicate of c1 that functions in the plant. Plant Cell. 1993 Dec;5(12):1795–1805. doi: 10.1105/tpc.5.12.1795. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Confalonieri F., Duguet M. A 200-amino acid ATPase module in search of a basic function. Bioessays. 1995 Jul;17(7):639–650. doi: 10.1002/bies.950170710. [DOI] [PubMed] [Google Scholar]
  9. Diamond M. I., Miner J. N., Yoshinaga S. K., Yamamoto K. R. Transcription factor interactions: selectors of positive or negative regulation from a single DNA element. Science. 1990 Sep 14;249(4974):1266–1272. doi: 10.1126/science.2119054. [DOI] [PubMed] [Google Scholar]
  10. Dorweiler J., Stec A., Kermicle J., Doebley J. Teosinte glume architecture 1: A Genetic Locus Controlling a Key Step in Maize Evolution. Science. 1993 Oct 8;262(5131):233–235. doi: 10.1126/science.262.5131.233. [DOI] [PubMed] [Google Scholar]
  11. Duncan I. The bithorax complex. Annu Rev Genet. 1987;21:285–319. doi: 10.1146/annurev.ge.21.120187.001441. [DOI] [PubMed] [Google Scholar]
  12. Eggleston W. B., Alleman M., Kermicle J. L. Molecular organization and germinal instability of R-stippled maize. Genetics. 1995 Sep;141(1):347–360. doi: 10.1093/genetics/141.1.347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Geyer P. K., Corces V. G. Separate regulatory elements are responsible for the complex pattern of tissue-specific and developmental transcription of the yellow locus in Drosophila melanogaster. Genes Dev. 1987 Nov;1(9):996–1004. doi: 10.1101/gad.1.9.996. [DOI] [PubMed] [Google Scholar]
  14. Goff S. A., Klein T. M., Roth B. A., Fromm M. E., Cone K. C., Radicella J. P., Chandler V. L. Transactivation of anthocyanin biosynthetic genes following transfer of B regulatory genes into maize tissues. EMBO J. 1990 Aug;9(8):2517–2522. doi: 10.1002/j.1460-2075.1990.tb07431.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Grotewold E., Drummond B. J., Bowen B., Peterson T. The myb-homologous P gene controls phlobaphene pigmentation in maize floral organs by directly activating a flavonoid biosynthetic gene subset. Cell. 1994 Feb 11;76(3):543–553. doi: 10.1016/0092-8674(94)90117-1. [DOI] [PubMed] [Google Scholar]
  16. Hanson M. A., Gaut B. S., Stec A. O., Fuerstenberg S. I., Goodman M. M., Coe E. H., Doebley J. F. Evolution of anthocyanin biosynthesis in maize kernels: the role of regulatory and enzymatic loci. Genetics. 1996 Jul;143(3):1395–1407. doi: 10.1093/genetics/143.3.1395. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Harris L. J., Currie K., Chandler V. L. Large tandem duplication associated with a Mu2 insertion in Zea mays B-Peru gene. Plant Mol Biol. 1994 Aug;25(5):817–828. doi: 10.1007/BF00028876. [DOI] [PubMed] [Google Scholar]
  18. Hattori T., Vasil V., Rosenkrans L., Hannah L. C., McCarty D. R., Vasil I. K. The Viviparous-1 gene and abscisic acid activate the C1 regulatory gene for anthocyanin biosynthesis during seed maturation in maize. Genes Dev. 1992 Apr;6(4):609–618. doi: 10.1101/gad.6.4.609. [DOI] [PubMed] [Google Scholar]
  19. Kao C. Y., Cocciolone S. M., Vasil I. K., McCarty D. R. Localization and interaction of the cis-acting elements for abscisic acid, VIVIPAROUS1, and light activation of the C1 gene of maize. Plant Cell. 1996 Jul;8(7):1171–1179. doi: 10.1105/tpc.8.7.1171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kel O. V., Romaschenko A. G., Kel A. E., Wingender E., Kolchanov N. A. A compilation of composite regulatory elements affecting gene transcription in vertebrates. Nucleic Acids Res. 1995 Oct 25;23(20):4097–4103. doi: 10.1093/nar/23.20.4097. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Klein T. M., Roth B. A., Fromm M. E. Regulation of anthocyanin biosynthetic genes introduced into intact maize tissues by microprojectiles. Proc Natl Acad Sci U S A. 1989 Sep;86(17):6681–6685. doi: 10.1073/pnas.86.17.6681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kloeckener-Gruissem B., Freeling M. Transposon-induced promoter scrambling: a mechanism for the evolution of new alleles. Proc Natl Acad Sci U S A. 1995 Mar 14;92(6):1836–1840. doi: 10.1073/pnas.92.6.1836. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lorenz W. W., McCann R. O., Longiaru M., Cormier M. J. Isolation and expression of a cDNA encoding Renilla reniformis luciferase. Proc Natl Acad Sci U S A. 1991 May 15;88(10):4438–4442. doi: 10.1073/pnas.88.10.4438. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Ludwig S. R., Habera L. F., Dellaporta S. L., Wessler S. R. 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 Sep;86(18):7092–7096. doi: 10.1073/pnas.86.18.7092. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Matzke M. A., Matzke AJM. How and Why Do Plants Inactivate Homologous (Trans)genes? Plant Physiol. 1995 Mar;107(3):679–685. doi: 10.1104/pp.107.3.679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Patterson G. I., Kubo K. M., Shroyer T., Chandler V. L. Sequences required for paramutation of the maize b gene map to a region containing the promoter and upstream sequences. Genetics. 1995 Aug;140(4):1389–1406. doi: 10.1093/genetics/140.4.1389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Radicella J. P., Brown D., Tolar L. A., Chandler V. L. Allelic diversity of the maize B regulatory gene: different leader and promoter sequences of two B alleles determine distinct tissue specificities of anthocyanin production. Genes Dev. 1992 Nov;6(11):2152–2164. doi: 10.1101/gad.6.11.2152. [DOI] [PubMed] [Google Scholar]
  28. Roth B. A., Goff S. A., Klein T. M., Fromm M. E. C1- and R-dependent expression of the maize Bz1 gene requires sequences with homology to mammalian myb and myc binding sites. Plant Cell. 1991 Mar;3(3):317–325. doi: 10.1105/tpc.3.3.317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Sainz M. B., Goff S. A., Chandler V. L. Extensive mutagenesis of a transcriptional activation domain identifies single hydrophobic and acidic amino acids important for activation in vivo. Mol Cell Biol. 1997 Jan;17(1):115–122. doi: 10.1128/mcb.17.1.115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. SanMiguel P., Tikhonov A., Jin Y. K., Motchoulskaia N., Zakharov D., Melake-Berhan A., Springer P. S., Edwards K. J., Lee M., Avramova Z. Nested retrotransposons in the intergenic regions of the maize genome. Science. 1996 Nov 1;274(5288):765–768. doi: 10.1126/science.274.5288.765. [DOI] [PubMed] [Google Scholar]
  31. Tuerck J. A., Fromm M. E. Elements of the maize A1 promoter required for transactivation by the anthocyanin B/C1 or phlobaphene P regulatory genes. Plant Cell. 1994 Nov;6(11):1655–1663. doi: 10.1105/tpc.6.11.1655. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Walker E. L., Robbins T. P., Bureau T. E., Kermicle J., Dellaporta S. L. Transposon-mediated chromosomal rearrangements and gene duplications in the formation of the maize R-r complex. EMBO J. 1995 May 15;14(10):2350–2363. doi: 10.1002/j.1460-2075.1995.tb07230.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. White S. E., Habera L. F., Wessler S. R. Retrotransposons in the flanking regions of normal plant genes: a role for copia-like elements in the evolution of gene structure and expression. Proc Natl Acad Sci U S A. 1994 Dec 6;91(25):11792–11796. doi: 10.1073/pnas.91.25.11792. [DOI] [PMC free article] [PubMed] [Google Scholar]

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