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. 1992 Nov;132(3):813–822. doi: 10.1093/genetics/132.3.813

Active Mutator Elements Suppress the Knotted Phenotype and Increase Recombination at the Kn1-O Tandem Duplication

B Lowe 1, J Mathern 1, S Hake 1
PMCID: PMC1205217  PMID: 1334895

Abstract

The KNOTTED-1 (KN1) locus is defined by a number of dominant mutations that affect leaf development. The Kn1-O mutation is characterized by outpocketings of tissue along lateral veins of the maize leaf and by displacement of ligule tissue from the junction of the blade and sheath into the blade. Kn1-O results from a tandem duplication of 17 kb; each repeat includes the entire 8-kb KN1 transcription unit. Mutator (Mu) transposable elements inserted at the junction of the two repeats diminish the mutant phenotype. The Mu insertions affect the Kn1-O mutation in several distinctive ways. (1) Two of the three Mu elements, a Mu1 and a Mu8 element, diminish the mutant phenotype only when active as indicated by hypomethylation; when methylated or inactive, the phenotype is comparable to the Kn1-O progenitor. (2) Additional rearrangements have arisen in these derivatives that further reduce the mutant phenotype. (3) A 100-2000-fold increase in the loss of one repeat occurs in the presence of Mu elements as compared to Kn1-O without elements. The high frequency of loss only occurs when the Mu elements are hypomethylated. The frequency is also influenced by the specific allele carried at the same locus on the homologous chromosome. Reciprocal exchange of flanking markers does not accompany the loss events. Various recombination models that address the events occurring at Kn1-O are presented.

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Selected References

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  1. 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]
  2. 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]
  3. 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]
  4. Chandler V. L., Hardeman K. J. The Mu elements of Zea mays. Adv Genet. 1992;30:77–122. doi: 10.1016/s0065-2660(08)60319-3. [DOI] [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. 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]
  7. 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]
  8. Corces V. G., Geyer P. K. Interactions of retrotransposons with the host genome: the case of the gypsy element of Drosophila. Trends Genet. 1991 Mar;7(3):86–90. doi: 10.1016/0168-9525(91)90277-W. [DOI] [PubMed] [Google Scholar]
  9. Davis P. S., Shen M. W., Judd B. H. Asymmetrical pairings of transposons in and proximal to the white locus of Drosophila account for four classes of regularly occurring exchange products. Proc Natl Acad Sci U S A. 1987 Jan;84(1):174–178. doi: 10.1073/pnas.84.1.174. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dooner H. K., Kermicle J. L. Structure of the R tandem duplication in maize. Genetics. 1971 Mar;67(3):427–436. doi: 10.1093/genetics/67.3.427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Doseff A., Martienssen R., Sundaresan V. Somatic excision of the Mu1 transposable element of maize. Nucleic Acids Res. 1991 Feb 11;19(3):579–584. doi: 10.1093/nar/19.3.579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Fleenor D., Spell M., Robertson D., Wessler S. Nucleotide sequence of the maize Mutator element, Mu8. Nucleic Acids Res. 1990 Nov 25;18(22):6725–6725. doi: 10.1093/nar/18.22.6725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fogel S., Welch J. W., Maloney D. H. The molecular genetics of copper resistance in Saccharomyces cerevisiae--a paradigm for non-conventional yeasts. J Basic Microbiol. 1988;28(3):147–160. doi: 10.1002/jobm.3620280302. [DOI] [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. Hake S., Vollbrecht E., Freeling M. Cloning Knotted, the dominant morphological mutant in maize using Ds2 as a transposon tag. EMBO J. 1989 Jan;8(1):15–22. doi: 10.1002/j.1460-2075.1989.tb03343.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Jackson J. A., Fink G. R. Meiotic recombination between duplicated genetic elements in Saccharomyces cerevisiae. Genetics. 1985 Feb;109(2):303–332. doi: 10.1093/genetics/109.2.303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lim J. K. Intrachromosomal rearrangements mediated by hobo transposons in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1988 Dec;85(23):9153–9157. doi: 10.1073/pnas.85.23.9153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Maloney D. H., Fogel S. Gene conversion, unequal crossing-over and mispairing at a non-tandem duplication during meiosis of Saccharomyces cerevisiae. Curr Genet. 1987;12(1):1–7. doi: 10.1007/BF00420720. [DOI] [PubMed] [Google Scholar]
  21. Mangelsdorf P. C., Galinat W. C. THE TUNICATE LOCUS IN MAIZE DISSECTED AND RECONSTITUTED. Proc Natl Acad Sci U S A. 1964 Feb;51(2):147–150. doi: 10.1073/pnas.51.2.147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. 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]
  24. McGill C., Shafer B., Strathern J. Coconversion of flanking sequences with homothallic switching. Cell. 1989 May 5;57(3):459–467. doi: 10.1016/0092-8674(89)90921-5. [DOI] [PubMed] [Google Scholar]
  25. Montgomery E. A., Huang S. M., Langley C. H., Judd B. H. Chromosome rearrangement by ectopic recombination in Drosophila melanogaster: genome structure and evolution. Genetics. 1991 Dec;129(4):1085–1098. doi: 10.1093/genetics/129.4.1085. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Nicolas A., Treco D., Schultes N. P., Szostak J. W. An initiation site for meiotic gene conversion in the yeast Saccharomyces cerevisiae. Nature. 1989 Mar 2;338(6210):35–39. doi: 10.1038/338035a0. [DOI] [PubMed] [Google Scholar]
  27. Orr-Weaver T. L., Szostak J. W., Rothstein R. J. Yeast transformation: a model system for the study of recombination. Proc Natl Acad Sci U S A. 1981 Oct;78(10):6354–6358. doi: 10.1073/pnas.78.10.6354. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Petes T. D., Hill C. W. Recombination between repeated genes in microorganisms. Annu Rev Genet. 1988;22:147–168. doi: 10.1146/annurev.ge.22.120188.001051. [DOI] [PubMed] [Google Scholar]
  29. Robertson D. S., Stinard P. S. Genetic evidence of mutator-induced deletions in the short arm of chromosome 9 of maize. Genetics. 1987 Feb;115(2):353–361. doi: 10.1093/genetics/115.2.353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Saedler H., Nevers P. Transposition in plants: a molecular model. EMBO J. 1985 Mar;4(3):585–590. doi: 10.1002/j.1460-2075.1985.tb03670.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sturtevant A. H., Morgan T. H. REVERSE MUTATION OF THE BAR GENE CORRELATED WITH CROSSING OVER. Science. 1923 Jun 29;57(1487):746–747. doi: 10.1126/science.57.1487.746. [DOI] [PubMed] [Google Scholar]
  32. Szostak J. W., Orr-Weaver T. L., Rothstein R. J., Stahl F. W. The double-strand-break repair model for recombination. Cell. 1983 May;33(1):25–35. doi: 10.1016/0092-8674(83)90331-8. [DOI] [PubMed] [Google Scholar]
  33. Taylor L. P., Walbot V. A deletion adjacent to the maize transposable element Mu-1 accompanies loss of Adh1 expression. EMBO J. 1985 Apr;4(4):869–876. doi: 10.1002/j.1460-2075.1985.tb03712.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Veit B., Vollbrecht E., Mathern J., Hake S. A tandem duplication causes the Kn1-O allele of Knotted, a dominant morphological mutant of maize. Genetics. 1990 Jul;125(3):623–631. doi: 10.1093/genetics/125.3.623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Vollbrecht E., Veit B., Sinha N., Hake S. The developmental gene Knotted-1 is a member of a maize homeobox gene family. Nature. 1991 Mar 21;350(6315):241–243. doi: 10.1038/350241a0. [DOI] [PubMed] [Google Scholar]
  36. Welch J. W., Maloney D. H., Fogel S. Unequal crossing-over and gene conversion at the amplified CUP1 locus of yeast. Mol Gen Genet. 1990 Jul;222(2-3):304–310. doi: 10.1007/BF00633833. [DOI] [PubMed] [Google Scholar]

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