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. 2001 Dec;159(4):1727–1740. doi: 10.1093/genetics/159.4.1727

Gene conversion within regulatory sequences generates maize r alleles with altered gene expression.

Y Li 1, J P Bernot 1, C Illingworth 1, W Lison 1, K M Bernot 1, W B Eggleston 1, K J Fogle 1, J E DiPaola 1, J Kermicle 1, M Alleman 1
PMCID: PMC1461907  PMID: 11779810

Abstract

The maize r locus encodes a transcription factor that regulates the developmental expression of the plant pigment anthocyanin. In an unusual example of gene regulatory diversity, the R-sc (Sc, strong seed color) and the R-p (P, plant color) alleles of r have nonoverlapping tissue specificity and nonhomologous 5' flanking sequences. Heterozygotes between wild-type P and Sc mutants with Ds6 transposable element inserts (r-sc:m::Ds6 or sc:m) produce colored seed derivatives (Sc+) during meiotic recombination. The sc:m alleles with Ds6 insertion in 3' regions of r produce crossover Sc+ derivatives. sc:m alleles with Ds6 elements inserted in 5' regions produce rare Sc+ derivatives borne on nonrecombinant chromosomes. Among 52 such noncrossover Sc+ derivatives, 18 are indistinguishable from the Sc progenitor in phenotype and DNA sequence [Scp(+) alleles]. The remaining 34 derivatives have strong Sc+ expression, including darkly pigmented aleurone, scutellum, coleoptile, and scutellar node [Scp(e) alleles]. The coleoptile and scutellar node phenotypes are unique from either progenitor but are similar to those of some naturally occurring r alleles. Both classes of Sc+ derivatives are explained by gene conversion between the promoter region of Sc:124 and a homologous region located proximal to P. The recombinational intermediate formed between sc:m alleles and P results in deletion of the Ds6 element alone or both Ds6 and a nearby unrelated transposable element-like sequence.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alleman M., Doctor J. Genomic imprinting in plants: observations and evolutionary implications. Plant Mol Biol. 2000 Jun;43(2-3):147–161. doi: 10.1023/a:1006419025155. [DOI] [PubMed] [Google Scholar]
  2. Alleman M., Kermicle J. L. Somatic variegation and germinal mutability reflect the position of transposable element Dissociation within the maize R gene. Genetics. 1993 Sep;135(1):189–203. doi: 10.1093/genetics/135.1.189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997 Sep 1;25(17):3389–3402. doi: 10.1093/nar/25.17.3389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. BRINK R. A. Paramutation at the R locus in maize. Cold Spring Harb Symp Quant Biol. 1958;23:379–391. doi: 10.1101/sqb.1958.023.01.036. [DOI] [PubMed] [Google Scholar]
  5. Bennetzen J. L., SanMiguel P., Chen M., Tikhonov A., Francki M., Avramova Z. Grass genomes. Proc Natl Acad Sci U S A. 1998 Mar 3;95(5):1975–1978. doi: 10.1073/pnas.95.5.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Borts R. H., Haber J. E. Length and distribution of meiotic gene conversion tracts and crossovers in Saccharomyces cerevisiae. Genetics. 1989 Sep;123(1):69–80. doi: 10.1093/genetics/123.1.69. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Borts R. H., Haber J. E. Meiotic recombination in yeast: alteration by multiple heterozygosities. Science. 1987 Sep 18;237(4821):1459–1465. doi: 10.1126/science.2820060. [DOI] [PubMed] [Google Scholar]
  8. Burr F. A., Burr B., Scheffler B. E., Blewitt M., Wienand U., Matz E. C. The maize repressor-like gene intensifier1 shares homology with the r1/b1 multigene family of transcription factors and exhibits missplicing. Plant Cell. 1996 Aug;8(8):1249–1259. doi: 10.1105/tpc.8.8.1249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chandler V. L., Eggleston W. B., Dorweiler J. E. Paramutation in maize. Plant Mol Biol. 2000 Jun;43(2-3):121–145. doi: 10.1023/a:1006499808317. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Chen J., Greenblatt I. M., Dellaporta S. L. Molecular analysis of Ac transposition and DNA replication. Genetics. 1992 Mar;130(3):665–676. doi: 10.1093/genetics/130.3.665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Chen W., Jinks-Robertson S. The role of the mismatch repair machinery in regulating mitotic and meiotic recombination between diverged sequences in yeast. Genetics. 1999 Apr;151(4):1299–1313. doi: 10.1093/genetics/151.4.1299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Civardi L., Xia Y., Edwards K. J., Schnable P. S., Nikolau B. J. The relationship between genetic and physical distances in the cloned a1-sh2 interval of the Zea mays L. genome. Proc Natl Acad Sci U S A. 1994 Aug 16;91(17):8268–8272. doi: 10.1073/pnas.91.17.8268. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Cooper D. M., Schimenti K. J., Schimenti J. C. Factors affecting ectopic gene conversion in mice. Mamm Genome. 1998 May;9(5):355–360. doi: 10.1007/s003359900769. [DOI] [PubMed] [Google Scholar]
  15. Dooner H. K., Belachew A. Transposition Pattern of the Maize Element Ac from the Bz-M2(ac) Allele. Genetics. 1989 Jun;122(2):447–457. doi: 10.1093/genetics/122.2.447. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Dooner H. K., Kermicle J. L. The Transposable Element Ds Affects the Pattern of Intragenic Recombination at the bz and R Loci in Maize. Genetics. 1986 May;113(1):135–143. doi: 10.1093/genetics/113.1.135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Dooner H. K., Robbins T. P., Jorgensen R. A. Genetic and developmental control of anthocyanin biosynthesis. Annu Rev Genet. 1991;25:173–199. doi: 10.1146/annurev.ge.25.120191.001133. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Goff S. A., Cone K. C., Chandler V. L. Functional analysis of the transcriptional activator encoded by the maize B gene: evidence for a direct functional interaction between two classes of regulatory proteins. Genes Dev. 1992 May;6(5):864–875. doi: 10.1101/gad.6.5.864. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Jackson J. A., Fink G. R. Gene conversion between duplicated genetic elements in yeast. Nature. 1981 Jul 23;292(5821):306–311. doi: 10.1038/292306a0. [DOI] [PubMed] [Google Scholar]
  22. Kermicle J. L., Eggleston W. B., Alleman M. Organization of paramutagenicity in R-stippled maize. Genetics. 1995 Sep;141(1):361–372. doi: 10.1093/genetics/141.1.361. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kermicle J. L. Somatic and meiotic instability of R-stippled, an aleurone spotting factor in maize. Genetics. 1970 Feb;64(2):247–258. doi: 10.1093/genetics/64.2.247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kupiec M., Petes T. D. Allelic and ectopic recombination between Ty elements in yeast. Genetics. 1988 Jul;119(3):549–559. doi: 10.1093/genetics/119.3.549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Lichten M., Borts R. H., Haber J. E. Meiotic gene conversion and crossing over between dispersed homologous sequences occurs frequently in Saccharomyces cerevisiae. Genetics. 1987 Feb;115(2):233–246. doi: 10.1093/genetics/115.2.233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Lin X., Kaul S., Rounsley S., Shea T. P., Benito M. I., Town C. D., Fujii C. Y., Mason T., Bowman C. L., Barnstead M. Sequence and analysis of chromosome 2 of the plant Arabidopsis thaliana. Nature. 1999 Dec 16;402(6763):761–768. doi: 10.1038/45471. [DOI] [PubMed] [Google Scholar]
  27. Liu Y., Alleman M., Wessler S. R. A Ds insertion alters the nuclear localization of the maize transcriptional activator R. Proc Natl Acad Sci U S A. 1996 Jul 23;93(15):7816–7820. doi: 10.1073/pnas.93.15.7816. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Liu Y., Wang L., Kermicle J. L., Wessler S. R. Molecular consequences of Ds insertion into and excision from the helix-loop-helix domain of the maize R gene. Genetics. 1998 Dec;150(4):1639–1648. doi: 10.1093/genetics/150.4.1639. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Ludwig S. R., Bowen B., Beach L., Wessler S. R. A regulatory gene as a novel visible marker for maize transformation. Science. 1990 Jan 26;247(4941):449–450. doi: 10.1126/science.247.4941.449. [DOI] [PubMed] [Google Scholar]
  30. 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]
  31. Ludwig S. R., Wessler S. R. Maize R gene family: tissue-specific helix-loop-helix proteins. Cell. 1990 Sep 7;62(5):849–851. doi: 10.1016/0092-8674(90)90259-h. [DOI] [PubMed] [Google Scholar]
  32. McCLINTOCK B. Chromosome organization and genic expression. Cold Spring Harb Symp Quant Biol. 1951;16:13–47. doi: 10.1101/sqb.1951.016.01.004. [DOI] [PubMed] [Google Scholar]
  33. McWhirter K S, Brink R A. Continuous Variation in Level of Paramutation at the R Locus in Maize. Genetics. 1962 Aug;47(8):1053–1074. doi: 10.1093/genetics/47.8.1053. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Modrich P., Lahue R. Mismatch repair in replication fidelity, genetic recombination, and cancer biology. Annu Rev Biochem. 1996;65:101–133. doi: 10.1146/annurev.bi.65.070196.000533. [DOI] [PubMed] [Google Scholar]
  35. Moreno M. A., Chen J., Greenblatt I., Dellaporta S. L. Reconstitutional mutagenesis of the maize P gene by short-range Ac transpositions. Genetics. 1992 Aug;131(4):939–956. doi: 10.1093/genetics/131.4.939. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Nag D. K., Petes T. D. Meiotic recombination between dispersed repeated genes is associated with heteroduplex formation. Mol Cell Biol. 1990 Aug;10(8):4420–4423. doi: 10.1128/mcb.10.8.4420. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Ochman H., Gerber A. S., Hartl D. L. Genetic applications of an inverse polymerase chain reaction. Genetics. 1988 Nov;120(3):621–623. doi: 10.1093/genetics/120.3.621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Okagaki R. J., Weil C. F. Analysis of recombination sites within the maize waxy locus. Genetics. 1997 Oct;147(2):815–821. doi: 10.1093/genetics/147.2.815. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. 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]
  40. Radicella J. P., Turks D., Chandler V. L. Cloning and nucleotide sequence of a cDNA encoding B-Peru, a regulatory protein of the anthocyanin pathway in maize. Plant Mol Biol. 1991 Jul;17(1):127–130. doi: 10.1007/BF00036813. [DOI] [PubMed] [Google Scholar]
  41. Robbins T. P., Walker E. L., Kermicle J. L., Alleman M., Dellaporta S. L. Meiotic instability of the R-r complex arising from displaced intragenic exchange and intrachromosomal rearrangement. Genetics. 1991 Sep;129(1):271–283. doi: 10.1093/genetics/129.1.271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. 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]
  43. Schmidt T. LINEs, SINEs and repetitive DNA: non-LTR retrotransposons in plant genomes. Plant Mol Biol. 1999 Aug;40(6):903–910. doi: 10.1023/a:1006212929794. [DOI] [PubMed] [Google Scholar]
  44. Schnable P. S., Hsia A. P., Nikolau B. J. Genetic recombination in plants. Curr Opin Plant Biol. 1998 Apr;1(2):123–129. doi: 10.1016/s1369-5266(98)80013-7. [DOI] [PubMed] [Google Scholar]
  45. Scott L., LaFoe D., Weil C. F. Adjacent sequences influence DNA repair accompanying transposon excision in maize. Genetics. 1996 Jan;142(1):237–246. doi: 10.1093/genetics/142.1.237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Steele D. F., Morris M. E., Jinks-Robertson S. Allelic and ectopic interactions in recombination-defective yeast strains. Genetics. 1991 Jan;127(1):53–60. doi: 10.1093/genetics/127.1.53. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Tikhonov A. P., SanMiguel P. J., Nakajima Y., Gorenstein N. M., Bennetzen J. L., Avramova Z. Colinearity and its exceptions in orthologous adh regions of maize and sorghum. Proc Natl Acad Sci U S A. 1999 Jun 22;96(13):7409–7414. doi: 10.1073/pnas.96.13.7409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. WEYERS W. H. Expression and stability of the marbled allele in maize. Genetics. 1961 Aug;46:1061–1067. doi: 10.1093/genetics/46.8.1061. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. 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]
  50. Xu X., Hsia A. P., Zhang L., Nikolau B. J., Schnable P. S. Meiotic recombination break points resolve at high rates at the 5' end of a maize coding sequence. Plant Cell. 1995 Dec;7(12):2151–2161. doi: 10.1105/tpc.7.12.2151. [DOI] [PMC free article] [PubMed] [Google Scholar]

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