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. 2003 Mar;163(3):1135–1146. doi: 10.1093/genetics/163.3.1135

The maize unstable factor for orange1 is a dominant epigenetic modifier of a tissue specifically silent allele of pericarp color1.

Surinder Chopra 1, Suzy M Cocciolone 1, Shaun Bushman 1, Vineet Sangar 1, Michael D McMullen 1, Thomas Peterson 1
PMCID: PMC1462483  PMID: 12663550

Abstract

We have characterized Unstable factor for orange1 (Ufo1), a dominant, allele-specific modifier of expression of the maize pericarp color1 (p1) gene. The p1 gene encodes an Myb-homologous transcriptional activator of genes required for biosynthesis of red phlobaphene pigments. The P1-wr allele specifies colorless kernel pericarp and red cobs, whereas Ufo1 modifies P1-wr expression to confer pigmentation in kernel pericarp, as well as vegetative tissues, which normally do not accumulate significant amounts of phlobaphene pigments. In the presence of Ufo1, P1-wr transcript levels and transcription rate are increased in kernel pericarp. The P1-wr allele contains approximately six p1 gene copies present in a hypermethylated and multicopy tandem array. In P1-wr Ufo1 plants, methylation of P1-wr DNA sequences is reduced, whereas the methylation state of other repetitive genomic sequences was not detectably affected. The phenotypes produced by the interaction of P1-wr and Ufo1 are unstable, exhibiting somatic mosaicism and variable penetrance. Moreover, the changes in P1-wr expression and methylation are not heritable: meiotic segregants that lack Ufo1 revert to the normal P1-wr expression and methylation patterns. These results demonstrate the existence of a class of modifiers of gene expression whose effects are associated with transient changes in DNA methylation of specific loci.

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Selected References

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  1. Amedeo P., Habu Y., Afsar K., Mittelsten Scheid O., Paszkowski J. Disruption of the plant gene MOM releases transcriptional silencing of methylated genes. Nature. 2000 May 11;405(6783):203–206. doi: 10.1038/35012108. [DOI] [PubMed] [Google Scholar]
  2. Ananiev E. V., Riera-Lizarazu O., Rines H. W., Phillips R. L. Oat-maize chromosome addition lines: a new system for mapping the maize genome. Proc Natl Acad Sci U S A. 1997 Apr 15;94(8):3524–3529. doi: 10.1073/pnas.94.8.3524. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Athma P., Peterson T. Ac induces homologous recombination at the maize P locus. Genetics. 1991 May;128(1):163–173. doi: 10.1093/genetics/128.1.163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bender J., Fink G. R. Epigenetic control of an endogenous gene family is revealed by a novel blue fluorescent mutant of Arabidopsis. Cell. 1995 Dec 1;83(5):725–734. doi: 10.1016/0092-8674(95)90185-x. [DOI] [PubMed] [Google Scholar]
  5. Campell B. R., Song Y., Posch T. E., Cullis C. A., Town C. D. Sequence and organization of 5S ribosomal RNA-encoding genes of Arabidopsis thaliana. Gene. 1992 Mar 15;112(2):225–228. doi: 10.1016/0378-1119(92)90380-8. [DOI] [PubMed] [Google Scholar]
  6. Chopra S., Athma P., Li X. G., Peterson T. A maize Myb homolog is encoded by a multicopy gene complex. Mol Gen Genet. 1998 Nov;260(4):372–380. doi: 10.1007/s004380050906. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Christensen A. H., Sharrock R. A., Quail P. H. Maize polyubiquitin genes: structure, thermal perturbation of expression and transcript splicing, and promoter activity following transfer to protoplasts by electroporation. Plant Mol Biol. 1992 Feb;18(4):675–689. doi: 10.1007/BF00020010. [DOI] [PubMed] [Google Scholar]
  9. Cocciolone S. M., Chopra S., Flint-Garcia S. A., McMullen M. D., Peterson T. Tissue-specific patterns of a maize Myb transcription factor are epigenetically regulated. Plant J. 2001 Sep;27(5):467–478. doi: 10.1046/j.1365-313x.2001.01124.x. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. 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]
  12. 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]
  13. Dorweiler J. E., Carey C. C., Kubo K. M., Hollick J. B., Kermicle J. L., Chandler V. L. mediator of paramutation1 is required for establishment and maintenance of paramutation at multiple maize loci. Plant Cell. 2000 Nov;12(11):2101–2118. doi: 10.1105/tpc.12.11.2101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Furner I. J., Sheikh M. A., Collett C. E. Gene silencing and homology-dependent gene silencing in Arabidopsis: genetic modifiers and DNA methylation. Genetics. 1998 Jun;149(2):651–662. doi: 10.1093/genetics/149.2.651. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Galbraith D. W., Harkins K. R., Maddox J. M., Ayres N. M., Sharma D. P., Firoozabady E. Rapid flow cytometric analysis of the cell cycle in intact plant tissues. Science. 1983 Jun 3;220(4601):1049–1051. doi: 10.1126/science.220.4601.1049. [DOI] [PubMed] [Google Scholar]
  16. Gardiner J. M., Coe E. H., Chao S. Cloning maize telomeres by complementation in Saccharomyces cerevisiae. Genome. 1996 Aug;39(4):736–748. doi: 10.1139/g96-093. [DOI] [PubMed] [Google Scholar]
  17. 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 Jun 1;88(11):4587–4591. doi: 10.1073/pnas.88.11.4587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. Hoekenga O. A., Muszynski M. G., Cone K. C. Developmental patterns of chromatin structure and DNA methylation responsible for epigenetic expression of a maize regulatory gene. Genetics. 2000 Aug;155(4):1889–1902. doi: 10.1093/genetics/155.4.1889. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hollick J. B., Patterson G. I., Asmundsson I. M., Chandler V. L. Paramutation alters regulatory control of the maize pl locus. Genetics. 2000 Apr;154(4):1827–1838. doi: 10.1093/genetics/154.4.1827. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Jeddeloh J. A., Stokes T. L., Richards E. J. Maintenance of genomic methylation requires a SWI2/SNF2-like protein. Nat Genet. 1999 May;22(1):94–97. doi: 10.1038/8803. [DOI] [PubMed] [Google Scholar]
  22. Kakutani T., Munakata K., Richards E. J., Hirochika H. Meiotically and mitotically stable inheritance of DNA hypomethylation induced by ddm1 mutation of Arabidopsis thaliana. Genetics. 1999 Feb;151(2):831–838. doi: 10.1093/genetics/151.2.831. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lechelt C., Peterson T., Laird A., Chen J., Dellaporta S. L., Dennis E., Peacock W. J., Starlinger P. Isolation and molecular analysis of the maize P locus. Mol Gen Genet. 1989 Oct;219(1-2):225–234. doi: 10.1007/BF00261181. [DOI] [PubMed] [Google Scholar]
  24. Lisch Damon, Carey Charles C., Dorweiler Jane E., Chandler Vicki L. A mutation that prevents paramutation in maize also reverses Mutator transposon methylation and silencing. Proc Natl Acad Sci U S A. 2002 Apr 16;99(9):6130–6135. doi: 10.1073/pnas.052152199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. Martienssen R. A., Richards E. J. DNA methylation in eukaryotes. Curr Opin Genet Dev. 1995 Apr;5(2):234–242. doi: 10.1016/0959-437x(95)80014-x. [DOI] [PubMed] [Google Scholar]
  27. Rea S., Eisenhaber F., O'Carroll D., Strahl B. D., Sun Z. W., Schmid M., Opravil S., Mechtler K., Ponting C. P., Allis C. D. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature. 2000 Aug 10;406(6796):593–599. doi: 10.1038/35020506. [DOI] [PubMed] [Google Scholar]
  28. Ronchi A., Petroni K., Tonelli C. The reduced expression of endogenous duplications (REED) in the maize R gene family is mediated by DNA methylation. EMBO J. 1995 Nov 1;14(21):5318–5328. doi: 10.1002/j.1460-2075.1995.tb00216.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Saghai-Maroof M. A., Soliman K. M., Jorgensen R. A., Allard R. W. Ribosomal DNA spacer-length polymorphisms in barley: mendelian inheritance, chromosomal location, and population dynamics. Proc Natl Acad Sci U S A. 1984 Dec;81(24):8014–8018. doi: 10.1073/pnas.81.24.8014. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Schwarz-Sommer Z., Shepherd N., Tacke E., Gierl A., Rohde W., Leclercq L., Mattes M., Berndtgen R., Peterson P. A., Saedler H. Influence of transposable elements on the structure and function of the A1 gene of Zea mays. EMBO J. 1987 Feb;6(2):287–294. doi: 10.1002/j.1460-2075.1987.tb04752.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sidorenko L. V., Li X., Cocciolone S. M., Chopra S., Tagliani L., Bowen B., Daniels M., Peterson T. Complex structure of a maize Myb gene promoter: functional analysis in transgenic plants. Plant J. 2000 Jun;22(6):471–482. doi: 10.1046/j.1365-313x.2000.00750.x. [DOI] [PubMed] [Google Scholar]
  32. Sidorenko L. V., Peterson T. Transgene-induced silencing identifies sequences involved in the establishment of paramutation of the maize p1 gene. Plant Cell. 2001 Feb;13(2):319–335. doi: 10.1105/tpc.13.2.319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Todd J. J., Vodkin L. O. Duplications That Suppress and Deletions That Restore Expression from a Chalcone Synthase Multigene Family. Plant Cell. 1996 Apr;8(4):687–699. doi: 10.1105/tpc.8.4.687. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Winkel-Shirley B. Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol. 2001 Jun;126(2):485–493. doi: 10.1104/pp.126.2.485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Ye F., Signer E. R. RIGS (repeat-induced gene silencing) in Arabidopsis is transcriptional and alters chromatin configuration. Proc Natl Acad Sci U S A. 1996 Oct 1;93(20):10881–10886. doi: 10.1073/pnas.93.20.10881. [DOI] [PMC free article] [PubMed] [Google Scholar]

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