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. 1999 Jul;11(7):1319–1336. doi: 10.1105/tpc.11.7.1319

Epigenetic interactions among three dTph1 transposons in two homologous chromosomes activate a new excision-repair mechanism in petunia.

A van Houwelingen 1, E Souer 1, J Mol 1, R Koes 1
PMCID: PMC144270  PMID: 10402432

Abstract

Unstable anthocyanin3 (an3) alleles of petunia with insertions of the Activator/Dissociation-like transposon dTph1 fall into two classes that differ in their genetic behavior. Excision of the (single) dTph1 insertion from class 1 an3 alleles results in the formation of a footprint, similar to the "classical" mechanism observed for excisions of maize and snapdragon transposons. By contrast, dTph1 excision and gap repair in class 2 an3 alleles occurs via a newly discovered mechanism that does not generate a footprint at the empty donor site. This novel mechanism depends on the presence of two additional dTph1 elements: one located in cis, 30 bp upstream of the an3 translation start in the same an3 allele, and a homologous copy, which is located in trans in the homologous an3 allele. Absence of the latter dTph1 element causes a heritable suppression of dTph1 excision-repair from the homologous an3 allele by the novel mechanism, which to some extent resembles paramutation. Thus, an epigenetic interaction among three dTph1 copies activates a novel recombination mechanism that eliminates a transposon insertion.

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Selected References

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

  1. Agrawal A., Eastman Q. M., Schatz D. G. Transposition mediated by RAG1 and RAG2 and its implications for the evolution of the immune system. Nature. 1998 Aug 20;394(6695):744–751. doi: 10.1038/29457. [DOI] [PubMed] [Google Scholar]
  2. Alfenito M. R., Souer E., Goodman C. D., Buell R., Mol J., Koes R., Walbot V. Functional complementation of anthocyanin sequestration in the vacuole by widely divergent glutathione S-transferases. Plant Cell. 1998 Jul;10(7):1135–1149. doi: 10.1105/tpc.10.7.1135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Banks J. A., Masson P., Fedoroff N. Molecular mechanisms in the developmental regulation of the maize Suppressor-mutator transposable element. Genes Dev. 1988 Nov;2(11):1364–1380. doi: 10.1101/gad.2.11.1364. [DOI] [PubMed] [Google Scholar]
  4. Baran G., Echt C., Bureau T., Wessler S. Molecular analysis of the maize wx-B3 allele indicates that precise excision of the transposable Ac element is rare. Genetics. 1992 Feb;130(2):377–384. doi: 10.1093/genetics/130.2.377. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Brink R. A., Styles E. D., Axtell J. D. Paramutation: directed genetic change. Paramutation occurs in somatic cells and heritably alters the functional state of a locus. Science. 1968 Jan 12;159(3811):161–170. doi: 10.1126/science.159.3811.161. [DOI] [PubMed] [Google Scholar]
  6. Brutnell T. P., Dellaporta S. L. Somatic inactivation and reactivation of Ac associated with changes in cytosine methylation and transposase expression. Genetics. 1994 Sep;138(1):213–225. doi: 10.1093/genetics/138.1.213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brutnell T. P., May B. P., Dellaporta S. L. The Ac-st2 element of maize exhibits a positive dosage effect and epigenetic regulation. Genetics. 1997 Oct;147(2):823–834. doi: 10.1093/genetics/147.2.823. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Coen E. S., Carpenter R., Martin C. Transposable elements generate novel spatial patterns of gene expression in Antirrhinum majus. Cell. 1986 Oct 24;47(2):285–296. doi: 10.1016/0092-8674(86)90451-4. [DOI] [PubMed] [Google Scholar]
  10. Craig N. L. Unity in transposition reactions. Science. 1995 Oct 13;270(5234):253–254. doi: 10.1126/science.270.5234.253. [DOI] [PubMed] [Google Scholar]
  11. Engels W. R., Johnson-Schlitz D. M., Eggleston W. B., Sved J. High-frequency P element loss in Drosophila is homolog dependent. Cell. 1990 Aug 10;62(3):515–525. doi: 10.1016/0092-8674(90)90016-8. [DOI] [PubMed] [Google Scholar]
  12. Fedoroff N., Schläppi M., Raina R. Epigenetic regulation of the maize Spm transposon. Bioessays. 1995 Apr;17(4):291–297. doi: 10.1002/bies.950170405. [DOI] [PubMed] [Google Scholar]
  13. Fedoroff N. The heritable activation of cryptic Suppressor-mutator elements by an active element. Genetics. 1989 Mar;121(3):591–608. doi: 10.1093/genetics/121.3.591. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gerats A. G., Huits H., Vrijlandt E., Maraña C., Souer E., Beld M. Molecular characterization of a nonautonomous transposable element (dTph1) of petunia. Plant Cell. 1990 Nov;2(11):1121–1128. doi: 10.1105/tpc.2.11.1121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gloor G. B., Nassif N. A., Johnson-Schlitz D. M., Preston C. R., Engels W. R. Targeted gene replacement in Drosophila via P element-induced gap repair. Science. 1991 Sep 6;253(5024):1110–1117. doi: 10.1126/science.1653452. [DOI] [PubMed] [Google Scholar]
  16. Henikoff S., Matzke M. A. Exploring and explaining epigenetic effects. Trends Genet. 1997 Aug;13(8):293–295. doi: 10.1016/s0168-9525(97)01219-5. [DOI] [PubMed] [Google Scholar]
  17. Hiom K., Melek M., Gellert M. DNA transposition by the RAG1 and RAG2 proteins: a possible source of oncogenic translocations. Cell. 1998 Aug 21;94(4):463–470. doi: 10.1016/s0092-8674(00)81587-1. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. 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]
  20. Hsia A. P., Schnable P. S. DNA sequence analyses support the role of interrupted gap repair in the origin of internal deletions of the maize transposon, MuDR. Genetics. 1996 Feb;142(2):603–618. doi: 10.1093/genetics/142.2.603. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Johnson-Schlitz D. M., Engels W. R. P-element-induced interallelic gene conversion of insertions and deletions in Drosophila melanogaster. Mol Cell Biol. 1993 Nov;13(11):7006–7018. doi: 10.1128/mcb.13.11.7006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kennedy A. K., Guhathakurta A., Kleckner N., Haniford D. B. Tn10 transposition via a DNA hairpin intermediate. Cell. 1998 Oct 2;95(1):125–134. doi: 10.1016/s0092-8674(00)81788-2. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. Koes R., Souer E., van Houwelingen A., Mur L., Spelt C., Quattrocchio F., Wing J., Oppedijk B., Ahmed S., Maes T. Targeted gene inactivation in petunia by PCR-based selection of transposon insertion mutants. Proc Natl Acad Sci U S A. 1995 Aug 29;92(18):8149–8153. doi: 10.1073/pnas.92.18.8149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Krebbers E, Hehl R, Piotrowiak R, Lönnig W E, Sommer H, Saedler H. Molecular analysis of paramutant plants of Antirrhinum majus and the involvement of transposable elements. Mol Gen Genet. 1987 Oct;209(3):499–507. doi: 10.1007/BF00331156. [DOI] [PubMed] [Google Scholar]
  26. Kroon J., Souer E., de Graaff A., Xue Y., Mol J., Koes R. Cloning and structural analysis of the anthocyanin pigmentation locus Rt of Petunia hybrida: characterization of insertion sequences in two mutant alleles. Plant J. 1994 Jan;5(1):69–80. doi: 10.1046/j.1365-313x.1994.5010069.x. [DOI] [PubMed] [Google Scholar]
  27. Lewin B. The mystique of epigenetics. Cell. 1998 May 1;93(3):301–303. doi: 10.1016/s0092-8674(00)81154-x. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. 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]
  30. Mathern J., Hake S. Mu element-generated gene conversions in maize attenuate the dominant knotted phenotype. Genetics. 1997 Sep;147(1):305–314. doi: 10.1093/genetics/147.1.305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Oettinger M. A., Schatz D. G., Gorka C., Baltimore D. RAG-1 and RAG-2, adjacent genes that synergistically activate V(D)J recombination. Science. 1990 Jun 22;248(4962):1517–1523. doi: 10.1126/science.2360047. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Plasterk R. H. The origin of footprints of the Tc1 transposon of Caenorhabditis elegans. EMBO J. 1991 Jul;10(7):1919–1925. doi: 10.1002/j.1460-2075.1991.tb07718.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Quattrocchio F., Wing J. F., Leppen HTC., Mol JNM., Koes R. E. Regulatory Genes Controlling Anthocyanin Pigmentation Are Functionally Conserved among Plant Species and Have Distinct Sets of Target Genes. Plant Cell. 1993 Nov;5(11):1497–1512. doi: 10.1105/tpc.5.11.1497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Rinehart T. A., Dean C., Weil C. F. Comparative analysis of non-random DNA repair following Ac transposon excision in maize and Arabidopsis. Plant J. 1997 Dec;12(6):1419–1427. doi: 10.1046/j.1365-313x.1997.12061419.x. [DOI] [PubMed] [Google Scholar]
  36. Rommens C. M., van Haaren M. J., Nijkamp H. J., Hille J. Differential repair of excision gaps generated by transposable elements of the 'Ac family'. Bioessays. 1993 Aug;15(8):507–512. doi: 10.1002/bies.950150803. [DOI] [PubMed] [Google Scholar]
  37. Roth D. B., Craig N. L. VDJ recombination: a transposase goes to work. Cell. 1998 Aug 21;94(4):411–414. doi: 10.1016/s0092-8674(00)81580-9. [DOI] [PubMed] [Google Scholar]
  38. Schläppi M., Raina R., Fedoroff N. Epigenetic regulation of the maize Spm transposable element: novel activation of a methylated promoter by TnpA. Cell. 1994 May 6;77(3):427–437. doi: 10.1016/0092-8674(94)90157-0. [DOI] [PubMed] [Google Scholar]
  39. Schwartz D. Gene-controlled cytosine demethylation in the promoter region of the Ac transposable element in maize. Proc Natl Acad Sci U S A. 1989 Apr;86(8):2789–2793. doi: 10.1073/pnas.86.8.2789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. 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]
  41. Souer E., Quattrocchio F., de Vetten N., Mol J., Koes R. A general method to isolate genes tagged by a high copy number transposable element. Plant J. 1995 Apr;7(4):677–685. doi: 10.1046/j.1365-313x.1995.7040677.x. [DOI] [PubMed] [Google Scholar]
  42. Souer E., van Houwelingen A., Kloos D., Mol J., Koes R. The no apical meristem gene of Petunia is required for pattern formation in embryos and flowers and is expressed at meristem and primordia boundaries. Cell. 1996 Apr 19;85(2):159–170. doi: 10.1016/s0092-8674(00)81093-4. [DOI] [PubMed] [Google Scholar]
  43. Souer E., van der Krol A., Kloos D., Spelt C., Bliek M., Mol J., Koes R. Genetic control of branching pattern and floral identity during Petunia inflorescence development. Development. 1998 Feb;125(4):733–742. doi: 10.1242/dev.125.4.733. [DOI] [PubMed] [Google Scholar]
  44. de Vetten N., Quattrocchio F., Mol J., Koes R. The an11 locus controlling flower pigmentation in petunia encodes a novel WD-repeat protein conserved in yeast, plants, and animals. Genes Dev. 1997 Jun 1;11(11):1422–1434. doi: 10.1101/gad.11.11.1422. [DOI] [PubMed] [Google Scholar]
  45. van Gent D. C., McBlane J. F., Ramsden D. A., Sadofsky M. J., Hesse J. E., Gellert M. Initiation of V(D)J recombination in a cell-free system. Cell. 1995 Jun 16;81(6):925–934. doi: 10.1016/0092-8674(95)90012-8. [DOI] [PubMed] [Google Scholar]
  46. van Gent D. C., Mizuuchi K., Gellert M. Similarities between initiation of V(D)J recombination and retroviral integration. Science. 1996 Mar 15;271(5255):1592–1594. doi: 10.1126/science.271.5255.1592. [DOI] [PubMed] [Google Scholar]
  47. van Houwelingen A., Souer E., Spelt K., Kloos D., Mol J., Koes R. Analysis of flower pigmentation mutants generated by random transposon mutagenesis in Petunia hybrida. Plant J. 1998 Jan;13(1):39–50. doi: 10.1046/j.1365-313x.1998.00005.x. [DOI] [PubMed] [Google Scholar]

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