Skip to main content
SpringerLink
Log in

Gene inactivation triggered by recognition between DNA repeats

  • Multi-Author Reviews
  • Published:
Experientia Aims and scope Submit manuscript

Abstract

This chapter focuses on phenomena of gene inactivation resulting from the presence of repeated gene copies within the genome of plants and fungi, and on their possible relationships to homologous DNA-DNA interactions. Emphasis is given to two related premeiotic processes: Methylation Induced Premeiotically (MIP) and Repeat-Induced Point mutation (RIP) which take place in the fungiAscobolus immersus andNeurospora crassa, respectively. The relationships between these processes and genetic recombination are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Almeida, A., Kokalj-Vokac, N., Lefrançois, D., Viegas-Pequignot, E., Jeanpierre, E., Dutrillaux, B., and Malfoy, B., Hypomethylation of classical satellite DNA and chromosome instability in lymphoblastoid cell lines. Human Genet.91 (1993) 538–546.

    Article  CAS  Google Scholar 

  2. Assaad, F. F., Tucker, K. L., and Signer, E. R., Epigenetic repeat-induced gene silencing (RIGS) inArabidopsis. Plant molec. Biol.22 (1993) 1067–1085.

    Article  CAS  Google Scholar 

  3. Barry, C., Faugeron, G., and Rossignol, J.-L., Methylation induced premeiotically inAscobolus: Coextension with DNA repeat lengths and effect on transcript elongation. Proc. natl Acad. Sci. USA90 (1993) 4557–4561.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Brink, R. A., Paramutation, A. Rev. Genet7 (1973) 129–152.

    Article  CAS  Google Scholar 

  5. Cambareri, E. B., Jensen, B. C., Schabtach, E., and Selker, E. U., Repeat-induced G-C to A-T mutations inNeurospora. Science244 (1989) 1571–1575.

    Article  CAS  PubMed  Google Scholar 

  6. Cambareri, E. B., Singer, M. J., and Selker, E. U., Recurrence of repeat-induced point mutation (RIP) inNeurospora crassa. Genetics127 (1991) 699–710.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Coppin-Raynal, E., Picard, M. and Arnaise, S., Transformation by integration inPodospora anserina III. Replacement of a chromosome segment by a two-step process. Molec. gen. Genet.219 (1989) 270–276.

    Article  CAS  PubMed  Google Scholar 

  8. Emerson, S., Mechanisms of inheritance. 1. Mendelian, in: The Fungi: An Advanced Treatise, vol. 2, pp. 513–566. Eds G. C. Ainsworthe and A. S. Sussman. Academic Press, New York 1966.

    Google Scholar 

  9. Faugeron, G., Rhounim, L., Barry, C., Goyon, C., Grégoire, A., and Rossignol, J.-L., MIP: de novo methylation and silencing of repeated genes inAscobolus immersus, in: Molecular Biology of Filamentous Fungi, pp. 191–199. Eds U. Stahl and P. Tudzinski. VCH, Weinheim 1992.

    Google Scholar 

  10. Faugeron, G., Rhounim, L., and Rossignol, J.-L., How does the cell count the number of ectopic copies of a gene in the premeiotic inactivation process acting inAscobolus immersus: Genetics124 (1990) 585–591.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Fincham, J. R. S., Connerton, I. F., Notarianni, E., and Harrington, K., Premeiotic disruption of duplicated and triplicated copies of theNeurospora crassa am (glutamate dehydrogenase) gene. Curr. Genet.15 (1989) 327–334.

    Article  CAS  PubMed  Google Scholar 

  12. Foss, E. J., Garrett, P. W., Kinsey, J. A., and Selker, E. U., Specificity of repeat-induced point mutation (RIP) inNeurospora: Sensitivity of non-Neurospora sequences, a natural diverged tandem duplication, and unique DNA adjacent to a duplicated region. Genetics127 (1991) 711–717.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Freedman, T., and Pukkila, P. J., De novo methylation of repeated sequences inCoprinus cinereus. Genetics135 (1993) 357–366.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Goyon, C., and Faugeron, G., Targeted transformation ofAscobolus immersus and de novo methylation of the resulting duplicated DNA sequences. Molec. cell. Biol.9 (1989) 2818–2827.

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Grayburn, W. S., and Selker, E. U., A natural case of RIP: Degeneration of DNA sequence in an ancestral tandem duplication. Molec. cell. Biol.9 (1989) 4416–4421.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Haber, J. E., Leung, W.-Y., Borts, R. H., and Lichten, M., The frequency of meiotic recombination in yeast is independent of the number and position of homologous donor sequences: implications for chromosome pairing. Proc. natl. Acad. Sci. USA88 (1991) 1120–1124.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Hart, C. M., Fischer, B., Neuhaus, J. M., and Meins, F. Jr., Regulated inactivation of homologous gene expression in transgenicNicotiana sylvestris plants containing a defenserelated tobacco chitinase gene. Molec. gen. Genet.235 (1992) 179–188.

    Article  CAS  PubMed  Google Scholar 

  18. Hawley, R. S., and Arbel, T., Yeast genetics and the fall of the classical view of meiosis. Cell72 (1993) 301–303.

    Article  CAS  PubMed  Google Scholar 

  19. Henikoff, S., Position effect variegation after 60 years. Trends Genet.6 (1992) 422–426.

    Article  Google Scholar 

  20. Hobbs, S. L. A., Kpodar, P., and Delong, C. M. O., The effect of T-DNA copy number position and methylation on reporter gene expression in tobacco transformants. Plant molec. Biol.15 (1990) 851–864.

    Article  CAS  Google Scholar 

  21. Hsieh, C.-L., and Lieber, M. R., CpG methylated minichromosomes become inaccessible for V(D)J recombination after undergoing replication. EMBO J.11 (1992) 315–325.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Jinks-Robertson, S., Michelitch, M. M., and Ramcharan, S., Substrate length requirements for efficient mitotic recombination inSaccharomyces cerevisiae. Molec. cell. Biol.13 (1993) 3937–3950.

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Jorgensen, R., Altered gene expression in plants due to trans interactions between homologous genes. Trends Biotech.8 (1990) 340–344.

    Article  CAS  Google Scholar 

  24. Jorgensen, R., Silencing of plant genes by homologous transgenes. AgBiotech News Inform.4 (1992) 265N-273N.

    Google Scholar 

  25. Jorgensen, R., The germinal inheritance of epigenetic information in plants. Phil. Trans. R. Soc. B.335 (1993) 173–181.

    Google Scholar 

  26. Kleckner, N., Padmore, R., and Bishop, D. K., Meiotic chromosome metabolism: One view. Cold Spring Harb. quant. Biol. (1991) 729–743.

  27. Kricker, M. C., Drake, J. W., and Radman, M., Duplication-targeted DNA methylation and mutagenesis in the evolution of eukaryotic chromosomes. Proc. natl Acad. Sci. USA89 (1992) 1075–1079.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Kunter, J. M., and Mol, J. N. M., Trans inactivation of gene expression in plants. Curr. Opin. Biotech.4 (1993) 166–171.

    Article  Google Scholar 

  29. Le Chevanton, L., Leblon, G., and Lebilcot, S., Duplications created by transformation inSordaria macrospora are not inactivated during meiosis. Molec. gen. Genet.218 (1989) 390–396.

    Article  PubMed  Google Scholar 

  30. Linn, F., Heidman, I., Seadler, H., and Meyer, P., Epigenetic changes in the expression of the maize A1 gene inPetunia hybrida: role of numbers of integrated gene copies and state of methylation. Molec. gen. Genet.222 (1990) 329–336.

    Article  CAS  PubMed  Google Scholar 

  31. Liskay, R. M., Letsou, A., and Stacheleck, J. L., Homology requirement for efficient gene conversion between duplicated chromosomal sequences in mammalian cells. Genetics115 (1987) 161–167.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Matzke, M. A., and Matzke, A. J. M., Gene interactions and epigenetic variation in transgenic plants. Devl Genet.11 (1990) 214–223.

    Article  CAS  Google Scholar 

  33. Matzke, M. A., and Matzke, A. J. M., Differential inactivation and methylation of a transgene in plants by two suppressor loci containing homologous sequences. Plant molec. Biol.16 (1991) 821–830.

    Article  CAS  Google Scholar 

  34. Matzke, A. J. M., and Matzke, M. A., Epigenetic variation as a consequence of homology-dependent gene interactions in transgenic plants. Devl Biol.4 (1993) 83–89.

    Article  Google Scholar 

  35. Matzke, M., and Matzke, A. J. M., Genomic imprinting in plants: parental effects and trans-inactivation phenomena. Annu. Rev. Plant Physiol. Plant molec. Biol.44 (1993) 53–76.

    Article  CAS  Google Scholar 

  36. Matzke, M., Matzke, A. J. M., and Mittelsten Scheid, O., Inactivation of repeated genes — DNA-DNA interaction?, in: Homologous Recombination and Gene Silencing in Plants. Ed. J. Paszkowski. Kluwer Academy Publishers, 1994, in press.

  37. Matzke, M. A., Neuhuber, F., and Matzke, A. J. M., A variety of epistatic interactions can occur between partially homologous transgene loci brought together by sexual crossing. Molec. gen. Genet.236 (1993) 379–386.

    Article  CAS  PubMed  Google Scholar 

  38. Matzke, M. A., Primig, M., Trnovsky, J., and Matzke, A. J. M., Reversible methylation and inactivation of marker genes in sequentially transformed tobacco plants. EMBO J.8 (1989) 643–649.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Meyer, P., Heidman, I., and Niedenhof, I., Differences in DNA methylation are associated with a paramutation phenomenon in transgenic petunia. Plant J.4 (1993) 89–100.

    Article  CAS  PubMed  Google Scholar 

  40. Mittelsten Scheid, O., Paszkowski, J., and Potrykus, I., Reversible inactivation of a transgene inAradopsis thaliana. Molec. Gen. Genet.228 (1991) 104–112.

    Article  CAS  PubMed  Google Scholar 

  41. Napoli, C., Lemieux, C., and Jorgensen, R., Introduction of a chimeric chalcone synthase gene intoPetunia results in reversible co-suppression of homologous genes in trans. Plant Cell2 (1990) 279–289.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Padmore, R., Cao, L., and Kleckner, N., Temporal comparison of recombination and synaptonemal complex formation during meiosis inS. cerevisiae. Cell66 (1991) 1239–1256.

    Article  CAS  PubMed  Google Scholar 

  43. Pandit, N. N., and Russo, V. E. A., Reversible inactivation of a foreign gene,hph, during the asexual cycle inNeurospora crassa transformants. Molec. gen. Genet.234 (1992) 412–422.

    Article  CAS  PubMed  Google Scholar 

  44. Perkins, D. D., and Barry, E. G., The cytogenetics ofNeurospora. Adv. Genet.19 (1977) 133–284.

    Article  CAS  PubMed  Google Scholar 

  45. Perkins, D. D., Metzenberg, R. L., Raju, N. B., Selker, E. U., and Barry, E. G., Reversal of aNeurospora translocation by crossing over involving displaced rDNA, and methylation of the rDNA segments that result from recombination. Genetics114 (1986) 791–817.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Picard, M., Debuchy, R., Julien, J., and Brygoo, Y., Transformation by integration inPodospora anserina II Targeting to the resident locus with cosmids and instability of the transformants. Molec. gen. Genet.210 (1987) 129–134.

    Article  CAS  Google Scholar 

  47. Pirrotta, V., Transvection and long-distance regulation. BioEssays12 (1990) 409–414.

    Article  CAS  PubMed  Google Scholar 

  48. Rhounim, L., Rossignol, J.-L., and Faugeron, G., Epimutation of repeated genes inAscobolus immersus. EMBO J.11 (1992) 4451–4457.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Rideout III, W. M., Coetzee, G. A., Olumi, A. F., and Jones, P. A., 5-Methylcytosine as an endogenous mutagen in the human LDL receptor and p53 genes. Science249 (1990) 1288–1290.

    Article  CAS  PubMed  Google Scholar 

  50. Romano, N., and Macino, G., Quelling: transient inactivation of gene expression inNeurospora crassa by tranformation with homologous sequences. Molec. Microbiol.6 (1992) 3343–3353.

    Article  CAS  Google Scholar 

  51. Scherthan, H., Loidl, J., Schuster, T., and Schweizer, D., Meiotic chromosome condensation and pairing inSaccharomyces cerevisiae studied by chromosome painting. Chromosoma101 (1992) 590–595.

    Article  CAS  PubMed  Google Scholar 

  52. Selker, E. U., Premeiotic instability of repeated sequences inNeurospora crassa. A. Rev. Genet.24 (1990) 579–613.

    Article  CAS  Google Scholar 

  53. Selker, E. U., Control of DNA methylation in fungi, in: DNA Methylation: Molecular Biology and Biological Significance, pp. 212–217. Eds J. P. Jost and H. P. Saluz, Birkhäuser Verlag, Basel 1993.

    Chapter  Google Scholar 

  54. Selker, E. U., Cambareri, E. B., Jensen, B. C., and Haack, K. R., Rearrangement of duplicated DNA in specialized cells ofNeurospora. Cell51 (1987) 741–752.

    Article  CAS  PubMed  Google Scholar 

  55. Selker, E. U., and Garrett, P. W., DNA sequence duplications trigger gene inactivation inNeurospora crassa. Proc. natl Acad. Sci. USA85 (1988) 6870–6874.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Selker, E. U., Jensen, B. C., and Richardson, G. A., A portable signal causing faithful DNA methylation de novo inNeurospora crassa. Science238 (1987) 48–53.

    Article  CAS  PubMed  Google Scholar 

  57. Selker, E. U., and Stevens, J. N., DNA methylation at asymmetric sites is associated with numerous transition mutations. Proc. natl Acad. Sci. USA82 (1985) 8114–8118.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Selker, E. U., Stevens, J. N., and Metzenberg, R. L., Rapid evolutionary decay of a novel pair of 5S rRNA genes, in: Molecular Genetics of Filamentous Fungi, pp. 309–319. Ed. W. E. Timberlake, A. R. Liss Inc., New York 1985.

    Google Scholar 

  59. Shapiro, R., and Klein, R. S., The deamination of cytidine and cytosine by acidic buffer solutions. Mutagenic implications. Biochemistry5 (1966) 2358–2362.

    Article  CAS  PubMed  Google Scholar 

  60. Shen, P., and Huang, H. V., Homologous recombination inEscherichia coli: dependence on substrate length and homology. Genetics112 (1986) 441–457.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Shen, J. C., Rideout, W. M. III, and Jones, P. A., High frequency mutagenesis by a DNA methyltransferase. Cell71 (1992) 1073–1080.

    Article  CAS  PubMed  Google Scholar 

  62. Stadler, D., Macleod, H., and Dillon, D., Spontaneous mutation at themtr locus ofNeurospora: the spectrum of mutant types. Genetics129 (1991) 39–45.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Smith, C. J. S., Watson, C. F., Bird, C. R., Ray, J., Schuch, W., and Gierson, D., Expression of a truncated tomato polygalacturonase gene inhibits expression of the endogenous gene in transgenic plants. Molec. gen. Genet.224 (1990) 477–481.

    Article  CAS  PubMed  Google Scholar 

  64. Sun, H., Treco, D., Nicolas, A., and Szostak, J. W., Doublestrand breaks at an initiation site for meiotic gene conversion. Nature338 (1989) 87–90.

    Article  CAS  PubMed  Google Scholar 

  65. Sun, H., Treco, D., and Szostak, J. W., Extensive 3′-over-hanging single-sranded DNA associated with the meiosis specific double-strand breaks at the ARG4 recombination initiation site. Cell64 (1991) 1155–1161.

    Article  CAS  PubMed  Google Scholar 

  66. Szostak, J. W., Orr-Weaver, R., Rothstein, R., and Stahl, F. W., The double-strand break model for recombination. Cell33 (1983) 25–35.

    Article  CAS  PubMed  Google Scholar 

  67. Toledo, F., Le Roscouet, D., Buttin, G., and Debatisse, M., Co-amplified markers alternate in megabase long chromosomal inverted repeats and cluster independently in interphase nuclei at early steps of mammalian gene amplification. EMBO J.11 (1992) 2665–2673.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. van der Krol, A. R., Mur, L. A., Beld, M., Mol, J. N. M., and Stuitje, A. R., Flavanoid genes inPetunia: addition of a limited number of gene copies may lead to a suppression of gene expression. Plant Cell2 (1990) 291–299.

    PubMed  PubMed Central  Google Scholar 

  69. Vaucheret, H., Identification of a general silencer for 19S and 35S promoters in a transgenic tobacco plant: 90 bp of homology in the promoter sequence are sufficient for trans-inactivation. C. R. Acad. Sci. Paris, Sciences de la vie/Life Sciences316 (1993) 1471–1483.

    CAS  Google Scholar 

  70. Waldmann, A. S., and Liskay, R. M., Differential effects of base-pair mismatch on intrachromosomal versus extra chromosomal recombination in mouse cells. Proc. natl Acad. Sci. USA84 (1987) 5340–5344.

    Article  Google Scholar 

  71. Zenvirth, D., Arbel, T., Sherman, A., Goldway, M., Klein, S., and Simchen, G., Multiple sites for double-strand breaks in whole meiotic chromosomes ofSaccharomyces cerevisiae. EMBO J.11 (1992) 3441–3447.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut de Génétique et Microbiologie, CNRS URA 1354, Université Paris-Sud, Bât. 400, F-91405, Orsay Cedex, France

    J. -L. Rossignol & G. Faugeron

Authors
  1. J. -L. Rossignol
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. G. Faugeron
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rossignol, J.L., Faugeron, G. Gene inactivation triggered by recognition between DNA repeats. Experientia 50, 307–317 (1994). https://doi.org/10.1007/BF01924014

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01924014

Key words

Search

Navigation