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. 2003 Oct;165(2):781–797. doi: 10.1093/genetics/165.2.781

Mu killer causes the heritable inactivation of the Mutator family of transposable elements in Zea mays.

R Keith Slotkin 1, Michael Freeling 1, Damon Lisch 1
PMCID: PMC1462800  PMID: 14573488

Abstract

Mutations in a number of genes responsible for the maintenance of transposon silencing have been reported. However, the initiation of epigenetic silencing of transposable elements is poorly characterized. Here, we report the identification of a single dominant locus, Mu killer (Muk), that acts to silence MuDR, the autonomous regulatory transposon of the Mutator family of transposable elements in maize. Muk results in the methylation of MuDR TIRs and is competent to silence one or several active MuDR elements. Silencing by Muk is not dependent on the position of the MuDR element and occurs gradually during plant development. Transcript levels of the MuDR transposase, mudrA, decrease substantially when Muk is present. The other transcript encoded by MuDR, mudrB, also fails to accumulate in the poly(A) RNA fraction when MuDR and Muk are combined. Additionally, plants undergoing MuDR silencing produce small, mudrA-homologous approximately 26-nt RNAs, suggesting a role for RNA-directed DNA methylation in MuDR silencing. MuDR elements silenced by Muk remain silenced even in plants that do not inherit Muk, suggesting that Muk is required for the initiation of MuDR silencing but not for its maintenance.

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Selected References

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  1. Bennetzen J. L. The Mutator transposable element system of maize. Curr Top Microbiol Immunol. 1996;204:195–229. doi: 10.1007/978-3-642-79795-8_9. [DOI] [PubMed] [Google Scholar]
  2. Chandler V., Rivin C., Walbot V. Stable non-mutator stocks of maize have sequences homologous to the Mu1 transposable element. Genetics. 1986 Nov;114(3):1007–1021. doi: 10.1093/genetics/114.3.1007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Chomet P., Lisch D., Hardeman K. J., Chandler V. L., Freeling M. Identification of a regulatory transposon that controls the Mutator transposable element system in maize. Genetics. 1991 Sep;129(1):261–270. doi: 10.1093/genetics/129.1.261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cuypers H., Dash S., Peterson P. A., Saedler H., Gierl A. The defective En-I102 element encodes a product reducing the mutability of the En/Spm transposable element system of Zea mays. EMBO J. 1988 Oct;7(10):2953–2960. doi: 10.1002/j.1460-2075.1988.tb03157.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. 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]
  6. Hamilton A. J., Baulcombe D. C. A species of small antisense RNA in posttranscriptional gene silencing in plants. Science. 1999 Oct 29;286(5441):950–952. doi: 10.1126/science.286.5441.950. [DOI] [PubMed] [Google Scholar]
  7. Hamilton Andrew, Voinnet Olivier, Chappell Louise, Baulcombe David. Two classes of short interfering RNA in RNA silencing. EMBO J. 2002 Sep 2;21(17):4671–4679. doi: 10.1093/emboj/cdf464. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hershberger R. J., Benito M. I., Hardeman K. J., Warren C., Chandler V. L., Walbot V. Characterization of the major transcripts encoded by the regulatory MuDR transposable element of maize. Genetics. 1995 Jul;140(3):1087–1098. doi: 10.1093/genetics/140.3.1087. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hirochika H., Okamoto H., Kakutani T. Silencing of retrotransposons in arabidopsis and reactivation by the ddm1 mutation. Plant Cell. 2000 Mar;12(3):357–369. doi: 10.1105/tpc.12.3.357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Huang Y., Carmichael G. G. Role of polyadenylation in nucleocytoplasmic transport of mRNA. Mol Cell Biol. 1996 Apr;16(4):1534–1542. doi: 10.1128/mcb.16.4.1534. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Jeong Br Byeong-ryool, Wu-Scharf Dancia, Zhang Chaomei, Cerutti Heriberto. Suppressors of transcriptional transgenic silencing in Chlamydomonas are sensitive to DNA-damaging agents and reactivate transposable elements. Proc Natl Acad Sci U S A. 2002 Jan 8;99(2):1076–1081. doi: 10.1073/pnas.022392999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kakutani T., Jeddeloh J. A., Flowers S. K., Munakata K., Richards E. J. Developmental abnormalities and epimutations associated with DNA hypomethylation mutations. Proc Natl Acad Sci U S A. 1996 Oct 29;93(22):12406–12411. doi: 10.1073/pnas.93.22.12406. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. Ketting R. F., Haverkamp T. H., van Luenen H. G., Plasterk R. H. Mut-7 of C. elegans, required for transposon silencing and RNA interference, is a homolog of Werner syndrome helicase and RNaseD. Cell. 1999 Oct 15;99(2):133–141. doi: 10.1016/s0092-8674(00)81645-1. [DOI] [PubMed] [Google Scholar]
  15. Kumar A., Bennetzen J. L. Plant retrotransposons. Annu Rev Genet. 1999;33:479–532. doi: 10.1146/annurev.genet.33.1.479. [DOI] [PubMed] [Google Scholar]
  16. Lee C. C., Beall E. L., Rio D. C. DNA binding by the KP repressor protein inhibits P-element transposase activity in vitro. EMBO J. 1998 Jul 15;17(14):4166–4174. doi: 10.1093/emboj/17.14.4166. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lisch D., Chomet P., Freeling M. Genetic characterization of the Mutator system in maize: behavior and regulation of Mu transposons in a minimal line. Genetics. 1995 Apr;139(4):1777–1796. doi: 10.1093/genetics/139.4.1777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lisch D., Girard L., Donlin M., Freeling M. Functional analysis of deletion derivatives of the maize transposon MuDR delineates roles for the MURA and MURB proteins. Genetics. 1999 Jan;151(1):331–341. doi: 10.1093/genetics/151.1.331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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]
  20. Lisch Damon. Mutator transposons. Trends Plant Sci. 2002 Nov;7(11):498–504. doi: 10.1016/s1360-1385(02)02347-6. [DOI] [PubMed] [Google Scholar]
  21. Miura A., Yonebayashi S., Watanabe K., Toyama T., Shimada H., Kakutani T. Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis. Nature. 2001 May 10;411(6834):212–214. doi: 10.1038/35075612. [DOI] [PubMed] [Google Scholar]
  22. Moreno M. A., Harper L. C., Krueger R. W., Dellaporta S. L., Freeling M. liguleless1 encodes a nuclear-localized protein required for induction of ligules and auricles during maize leaf organogenesis. Genes Dev. 1997 Mar 1;11(5):616–628. doi: 10.1101/gad.11.5.616. [DOI] [PubMed] [Google Scholar]
  23. Rudenko G. N., Walbot V. Expression and post-transcriptional regulation of maize transposable element MuDR and its derivatives. Plant Cell. 2001 Mar;13(3):553–570. doi: 10.1105/tpc.13.3.553. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Rudenko George N., Ono Akemi, Walbot Virginia. Initiation of silencing of maize MuDR/Mu transposable elements. Plant J. 2003 Mar;33(6):1013–1025. doi: 10.1046/j.1365-313x.2003.01683.x. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. Singer T., Yordan C., Martienssen R. A. Robertson's Mutator transposons in A. thaliana are regulated by the chromatin-remodeling gene Decrease in DNA Methylation (DDM1). Genes Dev. 2001 Mar 1;15(5):591–602. doi: 10.1101/gad.193701. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Tabara H., Sarkissian M., Kelly W. G., Fleenor J., Grishok A., Timmons L., Fire A., Mello C. C. The rde-1 gene, RNA interference, and transposon silencing in C. elegans. Cell. 1999 Oct 15;99(2):123–132. doi: 10.1016/s0092-8674(00)81644-x. [DOI] [PubMed] [Google Scholar]
  28. Tijsterman Marcel, Okihara Kristy L., Thijssen Karen, Plasterk Ronald H. A. PPW-1, a PAZ/PIWI protein required for efficient germline RNAi, is defective in a natural isolate of C. elegans. Curr Biol. 2002 Sep 3;12(17):1535–1540. doi: 10.1016/s0960-9822(02)01110-7. [DOI] [PubMed] [Google Scholar]
  29. Vielle-Calzada J. P., Thomas J., Spillane C., Coluccio A., Hoeppner M. A., Grossniklaus U. Maintenance of genomic imprinting at the Arabidopsis medea locus requires zygotic DDM1 activity. Genes Dev. 1999 Nov 15;13(22):2971–2982. doi: 10.1101/gad.13.22.2971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Wu-Scharf D., Jeong B., Zhang C., Cerutti H. Transgene and transposon silencing in Chlamydomonas reinhardtii by a DEAH-box RNA helicase. Science. 2000 Nov 10;290(5494):1159–1162. doi: 10.1126/science.290.5494.1159. [DOI] [PubMed] [Google Scholar]
  31. Zhang Chaomei, Wu-Scharf Dancia, Jeong Byeong-ryool, Cerutti Heriberto. A WD40-repeat containing protein, similar to a fungal co-repressor, is required for transcriptional gene silencing in Chlamydomonas. Plant J. 2002 Jul;31(1):25–36. doi: 10.1046/j.1365-313x.2002.01331.x. [DOI] [PubMed] [Google Scholar]

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