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A mechanism for gene conversion in fungi

Published online by Cambridge University Press:  14 April 2009

Robin Holliday
Affiliation:
John Innes Institute, Bayfordbury, Hertford, Herts.
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A mechanism for gene conversion is proposed which overcomes many of the difficulties that any copy choice model encounters. It is suggested that along with general genetic pairing of homologous genomes at meiosis, effective pairing over short regions of the genetic material occurs at the molecular level by the separation of the strands of the DNA double helices, followed by the annealing of strands from two homologous chromatids. If the annealed region happens to span a heterozygous site, mispairing of bases will occur. Such a situation may be analogous to that in DNA which is damaged by mutagens; the same or similar repair mechanisms may operate, and these, by adjusting the base sequences in order to restore normal base pairing, would bring about gene conversion in the absence of any genetic replication. The model indicates how precise breakage and rejoining of chromatids could occur in the vicinity of the conversion, so that conversion would frequently be accompanied by the recombination of outside markers. The model also proposes that the distance between two mutant sites on a fine structure map depends not so much on the frequency of a recombinational event occurring between them, but rather on the degree of inhibition of the processes of genetic pairing by the mutants themselves.

The model will explain almost all the data in a formal way, and it has the advantage over copy choice mechanisms for gene conversion in (1) being compatible with semi-conservative replication of DNA, (2) not invoking DNA synthesis during or after genetic pairing, (3) providing a molecular mechanism for close specific pairing, (4) making it unnecessary to postulate sister strand exchange or a process akin to this, (5) suggesting why rates of gene conversion in opposite directions are sometimes unequal and (6) providing an explanation of the clustering of mutant sites, a basis for map expansion and for the apparently capricious departure of fine structure maps from additivity. Although the model proposed is a general rather than a specific one, it suggests that the process of conversion and intragenic recombination is more complex than is usually believed, since it depends on several interacting factors. Nevertheless, it is hoped that the introduction of a model with this complexity will help to stimulate specific experiments, and that these will provide definitive information which would never be obtained if simpler models of conversion and intragenic recombination were believed to explain the genetic data sufficiently well.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1964

References

REFERENCES

Balbinder, E. (1962). The fine structure of the loci try C and try D of Salmonella typhimurium. II. Studies of reversion patterns and the behaviour of specific alleles during recombination. Genetics, 47, 545559.CrossRefGoogle Scholar
Benzer, S. (1961). On the topography of the genetic fine structure. Proc. nat. Acad. Sci., Wash., 47, 403415.CrossRefGoogle ScholarPubMed
Case, M. E. & Giles, N. H. (1958). Recombination mechanisms at the pan-2 locus in Neurospora crassa. Cold Spr. Harb. Symp. quant. Biol. 23, 119135.CrossRefGoogle ScholarPubMed
Case, M. E. & Giles, N. H. (1963). In Methodology in Basic Genetics (Burdette, W. J., ed.). Pp. 221226. San Francisco: Holden-Day Inc.Google Scholar
Demerec, M., Goldman, I. & Lahr, E. L. (1958). Genetic recombination by transduction in Salmonella. Cold Spr. Harb. Symp. quant. Biol. 23, 5968.CrossRefGoogle ScholarPubMed
Edgar, R. S., Feynman, R. P., Klein, S., Lielausis, I. & Steinberg, C. M. (1962). Mapping experiments with r mutants of bacteriophate T4D. Genetics, 47, 179186.CrossRefGoogle Scholar
Fincham, J. R. S. & Day, P. R. (1963). Fungal Genetics. Oxford: Blackwell.Google Scholar
Fresco, J. R. & Alberts, B. M. (1960). The accomodation of noncomplementary bases in helical polyribonucleotides and deoxyribonucleic acids. Proc. nat. Acad. Sci., Wash., 46, 311321.CrossRefGoogle Scholar
Giles, N. H. (1958). Mutations at specific loci in Neurospora. Proc. X Int. Congr. Genet. 1, 261279.Google Scholar
Gutz, H. (1961). Distribution of X-ray and nitrous acid-induced mutations in the genetic fine structure of the ad-7 locus of Schizosaccharomyces pombe. Nature, Lond., 191, 11251126.CrossRefGoogle Scholar
Hartman, P. E., Loper, J. C. & Šerman, D. (1960). Fine structure mapping by complete transduction between histidine requiring Salmonella mutants. J. gen. Microbiol. 22, 323353.CrossRefGoogle ScholarPubMed
Hershey, A. D. (1958). The production of recombinants in phage crosses. Cold Spr. Harb. Symp. quant. Biol. 23, 1946.CrossRefGoogle ScholarPubMed
Hexter, W. M. (1963). Non-reciprocal events at the garnet locus in Drosphila melanogaster. Proc. nat. Acad. Sci., Wash., 50, 372379.CrossRefGoogle Scholar
Holliday, R. (1961). Induced mitotic crossing-over in Ustilago maydis. Genet. Res. 2, 231248.CrossRefGoogle Scholar
Holliday, R. (1962). Mutation and replication in Ustilago maydis. Genet. Res. 3, 472486.CrossRefGoogle Scholar
Holliday, R. (1964). The induction of mitotic recombination by mitomycin C in Ustilago and Saccharomyces. Genetics (in press).CrossRefGoogle ScholarPubMed
Ishikawa, T. (1962). Genetic studies of ad-8 mutants in Neurospora crassa. I. Genetic fine structure of the ad-8 locus. Genetics, 47, 11471161.CrossRefGoogle ScholarPubMed
Kellenburger, G., Zichichi, M. L. & Weigle, J. J. (1961). Exchange of DNA in the recombination of bacteriophage. Proc. not. Acad. Sci., Wash. 47, 869878.CrossRefGoogle Scholar
Kitani, Y., Olive, L. S. & El-Ani, A. S. (1961). Transreplication and crossing-over in Sordaria fimicola. Science, 134, 668669.CrossRefGoogle ScholarPubMed
Kitani, Y., Olive, L. S. & El-Ani, A. S. (1962). Genetics of Sordaria fimicola. V. Aberrant segregation at the g locus. Amer. J. Bot. 49, 697706.CrossRefGoogle Scholar
Leupold, U. (1961). Intragene Rekombination und allele Komplementierung. Arch. Klaus- Stift. VererbForsch. 36, 89117.Google Scholar
Lindegren, C. C. (1953). Gene conversion in Saccharomyces. J. Genet. 51, 625637.CrossRefGoogle Scholar
Lissouba, P., Mousseau, J., Rizet, G. & Rossignol, J. L. (1962). Fine structure of genes in the Ascomycete Ascobolus immersus. Advanc. Genet. 11, 343380.CrossRefGoogle Scholar
Margolin, P. (1963). Genetic fine structure of the leucine operon in Salmonella. Genetics, 48, 441457.CrossRefGoogle ScholarPubMed
Meselson, M. & Weigle, J. J. (1961). Chromosome breakage accompanying genetic recombination in bacteriophage. Proc. nat. Acad. Sci., Wash., 47, 857868.CrossRefGoogle Scholar
Mitchell, M. B. (1955). Aberrant recombination of pyridoxine mutants of Neurospora. Proc. nat. Acad. Sci., Wash., 41, 215220.CrossRefGoogle ScholarPubMed
Murray, N. E. (1963). Polarized recombination and fine structure within the me-2 gene of Neurospora crassa. Genetics, 48, 11631183.CrossRefGoogle ScholarPubMed
Nelson, O. E. (1962). The waxy locus in maize, I. Intra locus recombination frequency estimates by pollen and by conventional analyses. Genetics, 47, 737742.CrossRefGoogle Scholar
Perkins, D. D. (1962). The frequency in Neurospora tetrads of multiple exchanges within short intervals. Genet. Res. 3, 315327.CrossRefGoogle Scholar
Pontecorvo, G. (1958). Trends in Genetic Analysis. New York: Colombia University Press.Google Scholar
Pritchard, R. H. (1955). The linear arrangement of a series of alleles of Aspergillus nidulans. Heredity, 9, 343371.CrossRefGoogle Scholar
Pritchard, R. H. (1960 a). The bearing of recombination analysis at high resolution on genetic fine structure in Aspergillus nidulans and the mechanism of recombination in higher organisms. Symp. Soc. gen. Microbiol. 10, 155180.Google Scholar
Pritchard, R. H. (1960 b). Localized negative interference and its bearing on models of gene recombination. Genet. Res. 1, 124.CrossRefGoogle Scholar
Putrament, A. (1963). Mitotic recombination within the paba-1 region of Aspergillus nidulans. (Abstr.). Proc. 11th Int. Congr. Genet. 1, 14.Google Scholar
Ravin, A. W. & Iyer, V. N. (1962). Genetic mapping of DNA: influence of the mutated configuration on the frequency of recombination along the length of the molecule. Genetics, 47, 13691384.CrossRefGoogle ScholarPubMed
Rizet, G. & Rossignol, J. L. (1964). Recombination within one locus of Ascobolus immersus. (Abstr.) Proc. XI Int. Congr. Genet. 2, (in press).Google Scholar
Roman, H. L. (1956). Studies of gene mutation in Saccharomyces. Cold. Spr. Harb.Symp.quant. Biol. 21, 175183.CrossRefGoogle ScholarPubMed
Roman, H. L. (1958). Sur les recombinaisons non reciproques chez Saccharomyces cereviseae et sur les problèmes posés par ces phenomènes. Ann. Genet. 1, 1117.Google Scholar
Roman, H. L. (1963). Genic conversion in fungi. In Methodology in Basic Genetics (Burdette, W. J., ed.). Pp. 209221. San Francisco: Holden-Day Inc.Google Scholar
Roman, H. L. & Jacob, F. (1958). A comparison of spontaneous and ultraviolet-induced allelic recombination with reference to the recombination of outside markers. Cold Spr. Harb. Symp. quant. Biol. 23, 155160.CrossRefGoogle Scholar
St. Lawrence, P. (1956). The q locus of Neurospora crassa. Proc. nat. Acad. Sci., Wash., 42, 189194.CrossRefGoogle Scholar
Siddiqi, O. H. (1962). The fine genetic structure of the paba1 region of Aspergillus nidulans. Genet. Res. 3, 6989.CrossRefGoogle Scholar
Siddiqi, O. H. (1963). The incorporation of parental DNA into genetic recombinants of E. coli. Proc. nat. Acad. Sci., Wash., 49. 589592.CrossRefGoogle ScholarPubMed
Siddiqi, O. H. & Putrament, A. (1963). Polarized negative interference in the pabal region of Aspergillus nidulans. Genet. Res. 4, 1220.CrossRefGoogle Scholar
Smith, D. A. (1961). Some aspects of the genetics of methionineless mutants of Salmonella typhimurium. J. gen. Microbiol. 24, 335353.CrossRefGoogle Scholar
Sobels, F. H. (ed.). (1963). Repair from Genetic Radiation Damage. Oxford: Pergamon Press.Google Scholar
Stadler, D. R. (1963). Observations on the polaron model for genetic recombination. Heredity, 18, 233242.CrossRefGoogle ScholarPubMed
Stadler, D. B. & Towe, A. M. (1963). Recombination of allelic cysteine mutants in Neurospora. Genetica, 48, 13231344.CrossRefGoogle ScholarPubMed
Suyama, J., Munnkres, K. D. & Woodward, V. W. (1959). Genetic analysis of the pyr-3 locus of Neurospora crassa; the bearing of recombination and gene conversion upon intra-allelic linearity. Genetica, 30, 293311.CrossRefGoogle Scholar
Tessman, I. (1963). Genetic ultrafine structure of the T4r II region. (Abstr.). Proc. XI Int. Congr. Genet. 1, 10.Google Scholar
Whitehouse, H. L. K. (1963). A theory of crossing-over by means of hybrid deoxyribonucleic acid. Nature, Lond., 199, 10341040.CrossRefGoogle ScholarPubMed
Yanofsky, C. & Crawford, I. P. (1959). The effects of deletions, point mutations, reversions and suppressor mutations on the two components of the tryptophan synthetase of Escherichia coli. Proc. nat. Acad. Sci., Wash., 45, 10161026.CrossRefGoogle ScholarPubMed