Analysis of a Mutator Activity Necessary for Germline Transposition and Excision of Tc1 Transposable Elements in Caenorhabditis Elegans

Overview

Journal Genetics

Publisher Oxford University Press

Specialty Genetics

Date 1988 Oct 1

PMID 2848746

Citations 42

Authors

I Mori

D G Moerman

R H Waterston

Affiliations

Soon will be listed here.

Abstract

The Tc1 transposable element family of the nematode Caenorhabditis elegans consists primarily of 1.6-kb size elements. This uniformity of size is in contrast to P in Drosophila and Ac/Ds in maize. Germline transposition and excision of Tc1 are detectable in the Bergerac (BO) strain, but not in the commonly used Bristol (N2) strain. A previous study suggested that multiple genetic components are responsible for the germline Tc1 activity of the BO strain. To analyze further this mutator activity, we derived hybrid strains between the BO strain and the N2 strain. One of the hybrid strains exhibits a single locus of mutator activity, designated mut-4, which maps to LGI. Two additional mutators, mut-5 II and mut-6 IV, arose spontaneously in mut-4 harboring strains. This spontaneous appearance of mutator activity at new sites suggests that the mutator itself transposes. The single mutator-harboring strains with low Tc1 copy number generated in this study should be useful in investigations of the molecular basis of mutator activity. As a first step toward this goal, we examined the Tc1 elements in these low copy number strains for elements consistently co-segregating with mutator activity. Three possible candidates were identified: none was larger than 1.6 kb.

Citing Articles

Genome-wide association and environmental suppression of the mortal germline phenotype of wild C. elegans.

Frezal L, Saglio M, Zhang G, Noble L, Richaud A, Felix M EMBO Rep. 2023; 24(12):e58116.

PMID: 37983674 PMC: 10702804. DOI: 10.15252/embr.202358116.

Bergerac strains of Caenorhabditis elegans revisited: expansion of Tc1 elements imposes a significant genomic and fitness cost.

Daigle A, Deiss T, Melde R, Bergthorsson U, Katju V G3 (Bethesda). 2022; 12(11).

PMID: 35977391 PMC: 9635669. DOI: 10.1093/g3journal/jkac214.

CRL4 regulates recombination and synaptonemal complex aggregation in the Caenorhabditis elegans germline.

Alleva B, Clausen S, Koury E, Hefel A, Smolikove S PLoS Genet. 2019; 15(11):e1008486.

PMID: 31738749 PMC: 6886871. DOI: 10.1371/journal.pgen.1008486.

Polymerase Θ is a key driver of genome evolution and of CRISPR/Cas9-mediated mutagenesis.

van Schendel R, Roerink S, Portegijs V, van den Heuvel S, Tijsterman M Nat Commun. 2015; 6:7394.

PMID: 26077599 PMC: 4490562. DOI: 10.1038/ncomms8394.

Forward and reverse mutagenesis in C. elegans.

Kutscher L, Shaham S WormBook. 2014; :1-26.

PMID: 24449699 PMC: 4078664. DOI: 10.1895/wormbook.1.167.1.

References

Alleman M, Freeling M . The Mu transposable elements of maize: evidence for transposition and copy number regulation during development. Genetics. 1986; 112(1):107-19. PMC: 1202684. DOI: 10.1093/genetics/112.1.107. View

Simmons M, Bucholz L . Transposase titration in Drosophila melanogaster: a model of cytotype in the P-M system of hybrid dysgenesis. Proc Natl Acad Sci U S A. 1985; 82(23):8119-23. PMC: 391454. DOI: 10.1073/pnas.82.23.8119. View

Rigby P, Dieckmann M, Rhodes C, Berg P . Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977; 113(1):237-51. DOI: 10.1016/0022-2836(77)90052-3. View

Moerman D, Benian G, Barstead R, Schriefer L, Waterston R . Identification and intracellular localization of the unc-22 gene product of Caenorhabditis elegans. Genes Dev. 1988; 2(1):93-105. DOI: 10.1101/gad.2.1.93. View

Sakoyama Y, Todo T, Ishiwa-Chigusa S, Honjo T, Kondo S . Structures of defective P transposable elements prevalent in natural Q and Q-derived M strains of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1985; 82(18):6236-9. PMC: 391027. DOI: 10.1073/pnas.82.18.6236. View

Moerman D, Baillie D . Genetic Organization in CAENORHABDITIS ELEGANS: Fine-Structure Analysis of the unc-22 Gene. Genetics. 1979; 91(1):95-103. PMC: 1213933. DOI: 10.1093/genetics/91.1.95. View

Laski F, Rio D, Rubin G . Tissue specificity of Drosophila P element transposition is regulated at the level of mRNA splicing. Cell. 1986; 44(1):7-19. DOI: 10.1016/0092-8674(86)90480-0. View

Green M, Slatko B . Genetic instability in Drosophila melanogaster dosage and mutator activity of an MR chromosome. Mutat Res. 1979; 62(3):529-31. DOI: 10.1016/0027-5107(79)90048-4. View

Emmons S, Roberts S, Ruan K . Evidence in a nematode for regulation of transposon excision by tissue-specific factors. Mol Gen Genet. 1986; 202(3):410-5. DOI: 10.1007/BF00333270. View

10.

Brenner S . The genetics of Caenorhabditis elegans. Genetics. 1974; 77(1):71-94. PMC: 1213120. DOI: 10.1093/genetics/77.1.71. View

11.

Daniels S, Clark S, Kidwell M, Chovnick A . Genetic transformation of Drosophila melanogaster with an autonomous P element: phenotypic and molecular analyses of long-established transformed lines. Genetics. 1987; 115(4):711-23. PMC: 1203104. DOI: 10.1093/genetics/115.4.711. View

12.

Kiff J, Moerman D, Schriefer L, Waterston R . Transposon-induced deletions in unc-22 of C. elegans associated with almost normal gene activity. Nature. 1988; 331(6157):631-3. DOI: 10.1038/331631a0. View

13.

Emmons S, Yesner L . High-frequency excision of transposable element Tc 1 in the nematode Caenorhabditis elegans is limited to somatic cells. Cell. 1984; 36(3):599-605. DOI: 10.1016/0092-8674(84)90339-8. View

14.

Collins J, Saari B, Anderson P . Activation of a transposable element in the germ line but not the soma of Caenorhabditis elegans. Nature. 1987; 328(6132):726-8. DOI: 10.1038/328726a0. View

15.

Kidwell M . Hybrid dysgenesis in Drosophila melanogaster: nature and inheritance of P element regulation. Genetics. 1985; 111(2):337-50. PMC: 1202647. DOI: 10.1093/genetics/111.2.337. View

16.

Green M . Genetic instability in Drosophila melanogaster: the genetics of an MR element that makes complete P insertion mutations. Proc Natl Acad Sci U S A. 1986; 83(4):1036-40. PMC: 323005. DOI: 10.1073/pnas.83.4.1036. View

17.

Craigie R, Arndt-Jovin D, Mizuuchi K . A defined system for the DNA strand-transfer reaction at the initiation of bacteriophage Mu transposition: protein and DNA substrate requirements. Proc Natl Acad Sci U S A. 1985; 82(22):7570-4. PMC: 391374. DOI: 10.1073/pnas.82.22.7570. View

18.

McCLINTOCK B . The origin and behavior of mutable loci in maize. Proc Natl Acad Sci U S A. 1950; 36(6):344-55. PMC: 1063197. DOI: 10.1073/pnas.36.6.344. View

19.

Southern E . Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975; 98(3):503-17. DOI: 10.1016/s0022-2836(75)80083-0. View

20.

Rose A, Harris L, Mawji N, Morris W . Tc1(Hin): a form of the transposable element Tc1 in Caenorhabditis elegans. Can J Biochem Cell Biol. 1985; 63(7):752-6. DOI: 10.1139/o85-094. View