Skip to main content
Genetics logoLink to Genetics
. 1994 Mar;136(3):1157–1170. doi: 10.1093/genetics/136.3.1157

Coordinate Suppression of Mutations Caused by Robertson's Mutator Transposons in Maize

R Martienssen 1, A Baron 1
PMCID: PMC1205871  PMID: 8005422

Abstract

Transposable elements from the Robertson's Mutator family are highly active insertional mutagens in maize. However, mutations caused by the insertion of responder (non-autonomous) elements frequently depend on the presence of active regulator (autonomous) elements for their phenotypic effects. The hcf106::Mu1 mutation has been previously shown to depend on Mu activity in this way. The dominant Lesion-mimic 28 mutation also requires Mu activity for its phenotypic effects. We have used double mutants to show that the loss of Mu activity results in the coordinate suppression of both mutant phenotypes. This loss can occur somatically resulting in large clones of cells that have a wild-type phenotype. Autonomous and non-autonomous Mutator elements within these clones are insensitive to digestion with methylation-sensitive enzymes, suggesting extensive methylation of CG and non-CG cytosine residues. Our data are consistent with the sectors being caused by the cycling of MuDR regulatory elements between active and inactive phases. The pattern of sectors suggests that they are clonal and that they are derived from the apical cells of the vegetative shoot meristem. We propose that these cells are more likely to undergo epigenetic loss of Mu activity because of their longer cell division cycle during shoot growth. Coordinate suppression of unlinked mutations can be used to perform mosaic analysis in maize.

Full Text

The Full Text of this article is available as a PDF (19.2 MB).

Selected References

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

  1. Barkan A., Martienssen R. A. Inactivation of maize transposon Mu suppresses a mutant phenotype by activating an outward-reading promoter near the end of Mu1. Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3502–3506. doi: 10.1073/pnas.88.8.3502. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Barkan A., Miles D., Taylor W. C. Chloroplast gene expression in nuclear, photosynthetic mutants of maize. EMBO J. 1986 Jul;5(7):1421–1427. doi: 10.1002/j.1460-2075.1986.tb04378.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bestor T., Laudano A., Mattaliano R., Ingram V. Cloning and sequencing of a cDNA encoding DNA methyltransferase of mouse cells. The carboxyl-terminal domain of the mammalian enzymes is related to bacterial restriction methyltransferases. J Mol Biol. 1988 Oct 20;203(4):971–983. doi: 10.1016/0022-2836(88)90122-2. [DOI] [PubMed] [Google Scholar]
  4. Brown J., Sundaresan V. Genetic study of the loss and restoration of Mutator transposon activity in maize: evidence against dominant-negative regulator associated with loss of activity. Genetics. 1992 Apr;130(4):889–898. doi: 10.1093/genetics/130.4.889. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chandler V. L., Walbot V. DNA modification of a maize transposable element correlates with loss of activity. Proc Natl Acad Sci U S A. 1986 Mar;83(6):1767–1771. doi: 10.1073/pnas.83.6.1767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. Frey M., Reinecke J., Grant S., Saedler H., Gierl A. Excision of the En/Spm transposable element of Zea mays requires two element-encoded proteins. EMBO J. 1990 Dec;9(12):4037–4044. doi: 10.1002/j.1460-2075.1990.tb07625.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gierl A. How maize transposable elements escape negative selection. Trends Genet. 1990 May;6(5):155–158. doi: 10.1016/0168-9525(90)90150-5. [DOI] [PubMed] [Google Scholar]
  9. Hahn S., Buratowski S., Sharp P. A., Guarente L. Isolation of the gene encoding the yeast TATA binding protein TFIID: a gene identical to the SPT15 suppressor of Ty element insertions. Cell. 1989 Sep 22;58(6):1173–1181. doi: 10.1016/0092-8674(89)90515-1. [DOI] [PubMed] [Google Scholar]
  10. Hake S. Unraveling the knots in plant development. Trends Genet. 1992 Mar;8(3):109–114. doi: 10.1016/0168-9525(92)90199-e. [DOI] [PubMed] [Google Scholar]
  11. Hershberger R. J., Warren C. A., Walbot V. Mutator activity in maize correlates with the presence and expression of the Mu transposable element Mu9. Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):10198–10202. doi: 10.1073/pnas.88.22.10198. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Holliday R. The inheritance of epigenetic defects. Science. 1987 Oct 9;238(4824):163–170. doi: 10.1126/science.3310230. [DOI] [PubMed] [Google Scholar]
  13. Hunt M. D., Newton K. J. The NCS3 mutation: genetic evidence for the expression of ribosomal protein genes in Zea mays mitochondria. EMBO J. 1991 May;10(5):1045–1052. doi: 10.1002/j.1460-2075.1991.tb08043.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Jackson M. S., Black D. M., Dover G. A. Amplification of KP elements associated with the repression of hybrid dysgenesis in Drosophila melanogaster. Genetics. 1988 Dec;120(4):1003–1013. doi: 10.1093/genetics/120.4.1003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lowe B., Mathern J., Hake S. Active Mutator elements suppress the knotted phenotype and increase recombination at the Kn1-O tandem duplication. Genetics. 1992 Nov;132(3):813–822. doi: 10.1093/genetics/132.3.813. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Martienssen R. A., Barkan A., Freeling M., Taylor W. C. Molecular cloning of a maize gene involved in photosynthetic membrane organization that is regulated by Robertson's Mutator. EMBO J. 1989 Jun;8(6):1633–1639. doi: 10.1002/j.1460-2075.1989.tb03553.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Martienssen R., Barkan A., Taylor W. C., Freeling M. Somatically heritable switches in the DNA modification of Mu transposable elements monitored with a suppressible mutant in maize. Genes Dev. 1990 Mar;4(3):331–343. doi: 10.1101/gad.4.3.331. [DOI] [PubMed] [Google Scholar]
  18. Masson P., Surosky R., Kingsbury J. A., Fedoroff N. V. Genetic and molecular analysis of the Spm-dependent a-m2 alleles of the maize a locus. Genetics. 1987 Sep;117(1):117–137. doi: 10.1093/genetics/117.1.117. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. McClintock B. The Production of Homozygous Deficient Tissues with Mutant Characteristics by Means of the Aberrant Mitotic Behavior of Ring-Shaped Chromosomes. Genetics. 1938 Jul;23(4):315–376. doi: 10.1093/genetics/23.4.315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Misra S., Rio D. C. Cytotype control of Drosophila P element transposition: the 66 kd protein is a repressor of transposase activity. Cell. 1990 Jul 27;62(2):269–284. doi: 10.1016/0092-8674(90)90365-l. [DOI] [PubMed] [Google Scholar]
  21. Parkhurst S. M., Harrison D. A., Remington M. P., Spana C., Kelley R. L., Coyne R. S., Corces V. G. The Drosophila su(Hw) gene, which controls the phenotypic effect of the gypsy transposable element, encodes a putative DNA-binding protein. Genes Dev. 1988 Oct;2(10):1205–1215. doi: 10.1101/gad.2.10.1205. [DOI] [PubMed] [Google Scholar]
  22. Peterson P. A. Phase variation of regulatory elements in maize. Genetics. 1966 Jul;54(1):249–266. doi: 10.1093/genetics/54.1.249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Poethig R. S. Phase change and the regulation of shoot morphogenesis in plants. Science. 1990 Nov 16;250(4983):923–930. doi: 10.1126/science.250.4983.923. [DOI] [PubMed] [Google Scholar]
  24. Robertson D. S. Genetic studies on the loss of mu mutator activity in maize. Genetics. 1986 Jul;113(3):765–773. doi: 10.1093/genetics/113.3.765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Robertson D. S. The timing of mu activity in maize. Genetics. 1980 Apr;94(4):969–978. doi: 10.1093/genetics/94.4.969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Rutledge B. J., Mortin M. A., Schwarz E., Thierry-Mieg D., Meselson M. Genetic interactions of modifier genes and modifiable alleles in Drosophila melanogaster. Genetics. 1988 Jun;119(2):391–397. doi: 10.1093/genetics/119.2.391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Schläppi M., Smith D., Fedoroff N. TnpA trans-activates methylated maize Suppressor-mutator transposable elements in transgenic tobacco. Genetics. 1993 Apr;133(4):1009–1021. doi: 10.1093/genetics/133.4.1009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. 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]
  29. Selker E. U. DNA methylation and chromatin structure: a view from below. Trends Biochem Sci. 1990 Mar;15(3):103–107. doi: 10.1016/0968-0004(90)90193-f. [DOI] [PubMed] [Google Scholar]
  30. Walbot V. Inheritance of mutator activity in Zea mays as assayed by somatic instability of the bz2-mu1 allele. Genetics. 1986 Dec;114(4):1293–1312. doi: 10.1093/genetics/114.4.1293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Walbot V. Reactivation of Mutator transposable elements of maize by ultraviolet light. Mol Gen Genet. 1992 Sep;234(3):353–360. doi: 10.1007/BF00538694. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES