Skip to main content
PMC home page
Genetics logoLink to Genetics
. 1995 Oct;141(2):709–719. doi: 10.1093/genetics/141.2.709

Allelic Interactions Heritably Alter the Activity of a Metastable Maize Pl Allele

J B Hollick 1, G I Patterson 1, E H Coe-Jr 1, K C Cone 1, V L Chandler 1
PMCID: PMC1206767  PMID: 8647404

Abstract

The maize pl locus encodes a transcriptional activator of anthocyanin biosynthetic genes. The Pl-Rhoades (Pl-Rh) allele confers robust purple anthocyanin pigment in several tissues. Spontaneous derivatives of Pl-Rh, termed Pl'-mahogany (Pl'-mah), arise that confer reduced pigment and are meiotically heritable. These derivatives influence other Pl-Rh alleles such that only Pl'-mah alleles are transmitted from a Pl-Rh/Pl'-mah heterozygote. Genetic crosses establish that chromosomal segregation distortion does not explain this exclusive transmission and suggest that Pl-Rh invariably changes to Pl'-mah when exposed to Pl'-mah. Such behavior is a hallmark of paramutation. Cosegregation experiments demonstrate that this paramutagenic activity is genetically linked to the pl locus. By visually quantifying pl action through successive crosses, we find that phenotypic expression is inversely related to paramutagenic strength. In addition, the paramutagenic state is metastable; reversion to a nonparamutagenic Pl-Rh state can occur. The behavior of Pl-Rh is unique, yet it shares characteristics with paramutation at two other maize loci, b and r. Previous analysis of b and r paramutation revealed extensive differences and led to suggestions of distinct molecular mechanisms. Consideration of the common features of all three systems reinvigorates the interpretation that the mechanistic processes of these three allelic interactions are similar.

Full Text

The Full Text of this article is available as a PDF (8.1 MB).

Selected References

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

  1. Ashman R B. Stippled Aleurone in Maize. Genetics. 1960 Jan;45(1):19–34. doi: 10.1093/genetics/45.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Brink R. A., Kermicle J. L., Ziebur N. K. Derepression in the female gametophyte in relation to paramutant R expression in maize endosperms, embryos, and seedlings. Genetics. 1970 Sep;66(1):87–96. doi: 10.1093/genetics/66.1.87. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brink R. A. Paramutation. Annu Rev Genet. 1973;7:129–152. doi: 10.1146/annurev.ge.07.120173.001021. [DOI] [PubMed] [Google Scholar]
  4. Brown D F, Brink R A. Paramutagenic Action of Paramutant R and R Alleles in Maize. Genetics. 1960 Oct;45(10):1313–1316. doi: 10.1093/genetics/45.10.1313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. 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]
  6. Cocciolone S. M., Cone K. C. Pl-Bh, an anthocyanin regulatory gene of maize that leads to variegated pigmentation. Genetics. 1993 Oct;135(2):575–588. doi: 10.1093/genetics/135.2.575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Coe E. H., Jr Heritable repression due to paramutation in maize. Science. 1968 Nov 22;162(3856):925–925. doi: 10.1126/science.162.3856.925. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Cone K. C., Cocciolone S. M., Moehlenkamp C. A., Weber T., Drummond B. J., Tagliani L. A., Bowen B. A., Perrot G. H. Role of the regulatory gene pl in the photocontrol of maize anthocyanin pigmentation. Plant Cell. 1993 Dec;5(12):1807–1816. doi: 10.1105/tpc.5.12.1807. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Consonni G., Geuna F., Gavazzi G., Tonelli C. Molecular homology among members of the R gene family in maize. Plant J. 1993 Feb;3(2):335–346. doi: 10.1111/j.1365-313x.1993.tb00185.x. [DOI] [PubMed] [Google Scholar]
  11. Das O. P., Messing J. Variegated phenotype and developmental methylation changes of a maize allele originating from epimutation. Genetics. 1994 Mar;136(3):1121–1141. doi: 10.1093/genetics/136.3.1121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dawe R. K., Freeling M. Clonal analysis of the cell lineages in the male flower of maize. Dev Biol. 1990 Nov;142(1):233–245. doi: 10.1016/0012-1606(90)90167-h. [DOI] [PubMed] [Google Scholar]
  13. Dooner H. K., Kermicle J. L. Structure of the R tandem duplication in maize. Genetics. 1971 Mar;67(3):427–436. doi: 10.1093/genetics/67.3.427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. 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]
  16. 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]
  17. 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]
  18. Johri M. M., Coe E. H., Jr Clonal analysis of corn plant development. I. The development of the tassel and the ear shoot. Dev Biol. 1983 May;97(1):154–172. doi: 10.1016/0012-1606(83)90073-8. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. 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]
  21. 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]
  22. 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]
  23. MIKULA B. C. Progressive conversion of R-locus expression in maize. Proc Natl Acad Sci U S A. 1961 Apr 15;47:566–571. doi: 10.1073/pnas.47.4.566. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. McWhirter K S, Brink R A. Paramutation in Maize during Endosperm Development. Genetics. 1963 Feb;48(2):189–203. doi: 10.1093/genetics/48.2.189. [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. Patterson G. I., Thorpe C. J., Chandler V. L. Paramutation, an allelic interaction, is associated with a stable and heritable reduction of transcription of the maize b regulatory gene. Genetics. 1993 Nov;135(3):881–894. doi: 10.1093/genetics/135.3.881. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Perrot G. H., Cone K. C. Nucleotide sequence of the maize R-S gene. Nucleic Acids Res. 1989 Oct 11;17(19):8003–8003. doi: 10.1093/nar/17.19.8003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. 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]
  31. 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]
  32. Sastry G. R., Cooper H. B., Jr, Brink R. A. Paramutation and somatic mosaicism in maize. Genetics. 1965 Aug;52(2):407–424. doi: 10.1093/genetics/52.2.407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Styles E. D., Brink R. A. The Metastable Nature of Paramutable R Alleles in Maize. IV. Parallel Enhancement of R Action in Heterozygotes with r and in Hemizygotes. Genetics. 1969 Apr;61(4):801–811. doi: 10.1093/genetics/61.4.801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Styles E. D., Brink R. A. The metastable nature of paramutable R alleles in maize. I. Heritable enhancement in level of standard R action. Genetics. 1966 Aug;54(2):433–439. doi: 10.1093/genetics/54.2.433. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES