Skip to main content
Genetics logoLink to Genetics
. 1998 Oct;150(2):891–897. doi: 10.1093/genetics/150.2.891

Epigenetic allelic states of a maize transcriptional regulatory locus exhibit overdominant gene action.

J B Hollick 1, V L Chandler 1
PMCID: PMC1460365  PMID: 9755217

Abstract

Using alleles of the maize purple plant locus (pl), which encodes a transcriptional regulator of anthocyanin pigment synthesis, we describe a case of single-locus heterosis, or overdominance, where the heterozygote displays a phenotype that is greater than either homozygote. The Pl-Rhoades (Pl-Rh) allele is subject to epigenetic changes in gene expression, resulting in quantitatively distinct expression states. Allelic states with low-expression levels, designated Pl'-mahogany (Pl'-mah), are dominant to the high-expression state of Pl-Rh. Pl'-mah states retain low-expression levels in subsequent generations when homozygous or heterozygous with Pl-Rh. However, Pl'-mah alleles frequently exhibit higher expression levels when heterozygous with other pl alleles; illustrating an overdominant allelic relationship. Higher expression levels are also observed when Pl'-mah is hemizygous. These results suggest that persistent allelic interactions between Pl'-mah and Pl-Rh are required to maintain the low-expression state and that other pl alleles are missing sequences required for this interaction. The Pl-Rh state can be sexually transmitted from Pl'-mah/pl heterozygotes, but not from Pl'-mah hemizygotes, suggesting that fixation of the high-expression state may involve synapsis. The existence of such allele-dependent regulatory mechanisms implicates a novel importance of allele polymorphisms in the genesis and maintenance of genetic variation.

Full Text

The Full Text of this article is available as a PDF (187.0 KB).

Selected References

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

  1. 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]
  2. Coe E. H. The properties, origin, and mechanism of conversion-type inheritance at the B locus in maize. Genetics. 1966 Jun;53(6):1035–1063. doi: 10.1093/genetics/53.6.1035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. East E M. Heterosis. Genetics. 1936 Jul;21(4):375–397. doi: 10.1093/genetics/21.4.375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Hollick J. B., Dorweiler J. E., Chandler V. L. Paramutation and related allelic interactions. Trends Genet. 1997 Aug;13(8):302–308. doi: 10.1016/s0168-9525(97)01184-0. [DOI] [PubMed] [Google Scholar]
  6. Hollick J. B., Patterson G. I., Coe E. H., Jr, Cone K. C., Chandler V. L. Allelic interactions heritably alter the activity of a metastable maize pl allele. Genetics. 1995 Oct;141(2):709–719. doi: 10.1093/genetics/141.2.709. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Jack J. W., Judd B. H. Allelic pairing and gene regulation: A model for the zeste-white interaction in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1979 Mar;76(3):1368–1372. doi: 10.1073/pnas.76.3.1368. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Jorgensen R. A. Cosuppression, flower color patterns, and metastable gene expression States. Science. 1995 May 5;268(5211):686–691. doi: 10.1126/science.268.5211.686. [DOI] [PubMed] [Google Scholar]
  9. Kassis J. A. Unusual properties of regulatory DNA from the Drosophila engrailed gene: three "pairing-sensitive" sites within a 1.6-kb region. Genetics. 1994 Mar;136(3):1025–1038. doi: 10.1093/genetics/136.3.1025. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Lewis E. B. Regulation of the genes of the bithorax complex in Drosophila. Cold Spring Harb Symp Quant Biol. 1985;50:155–164. doi: 10.1101/sqb.1985.050.01.021. [DOI] [PubMed] [Google Scholar]
  11. Metzlaff M., O'Dell M., Cluster P. D., Flavell R. B. RNA-mediated RNA degradation and chalcone synthase A silencing in petunia. Cell. 1997 Mar 21;88(6):845–854. doi: 10.1016/s0092-8674(00)81930-3. [DOI] [PubMed] [Google Scholar]
  12. Nap J. P., Conner A. J., Mlynárová L., Stiekema W. J., Jansen R. C. Dissection of a synthesized quantitative trait to characterize transgene interactions. Genetics. 1997 Sep;147(1):315–320. doi: 10.1093/genetics/147.1.315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. Roman H. Mitotic Nondisjunction in the Case of Interchanges Involving the B-Type Chromosome in Maize. Genetics. 1947 Jul;32(4):391–409. doi: 10.1093/genetics/32.4.391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Stuber C. W., Lincoln S. E., Wolff D. W., Helentjaris T., Lander E. S. Identification of genetic factors contributing to heterosis in a hybrid from two elite maize inbred lines using molecular markers. Genetics. 1992 Nov;132(3):823–839. doi: 10.1093/genetics/132.3.823. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Xiao J., Li J., Yuan L., Tanksley S. D. Dominance is the major genetic basis of heterosis in rice as revealed by QTL analysis using molecular markers. Genetics. 1995 Jun;140(2):745–754. doi: 10.1093/genetics/140.2.745. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES