Hostname: page-component-76fb5796d-2lccl Total loading time: 0 Render date: 2024-04-25T17:25:20.629Z Has data issue: false hasContentIssue false
  • English
  • Français

The analysis of genetic recombination on the polaron hybrid DNA model

Published online by Cambridge University Press:  14 April 2009

H. L. K. Whitehouse  and
P. J. Hastings
H. L. K. Whitehouse
Affiliation:
Botany School, University of Cambridge
P. J. Hastings
Affiliation:
Botany School, University of Cambridge
Rights & Permissions [Opens in a new window]

Extract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

According to the polaron hybrid DNA model, the initial nucleotide-chain breakage leading to genetic recombination takes place only at the linkage points which define the ends of each polaron. The term dissociation cycle is proposed for the postulated series of events from primary breakage at a linkage point to the final breakdown of unpaired chains. At mutant sites, the mispairing in hybrid DNA may persist and give rise to post-meiotic segregation, or a correction process may operate by which molecular homozygosity is restored. This causes conversion, which may be evident as reciprocal or as non-reciprocal recombination.

The implications of this model are that a crossover occupies a segment of the chromosome, and that conversion is a process which takes place when a mutant site happens to lie within such a segment. Although crossovers appear to be initiated at fixed points outside or at the ends of the genes, they extend into the gene on one side or the other. The negative interference between recombination events over short intervals of the linkage map is attributed to the association between crossing-over and the conversion which is likely to occur at any mutant sites which happen to lie within the crossover. In the same way, non-crossover hybrid DNA can also lead to conversion, and hence to negative interference.

The relevant data on genetic recombination have been found to fit this model, and have led to the following main conclusions:

(1) The polaron may coincide with the cistron, or in some instances may possibly include more than one cistron. As a corollary to this, there appear to be two kinds of cistrons: unipolar, where all the recombination is initiated from the same end, and bipolar, where it is sometimes initiated from one end and sometimes from the other.

(2) In bipolar cistrons there is usually a preponderance of recombination initiated from one end over that from the other. In five genes where the orientation with respect to the centromere is known, two show a preponderance in favour of the proximal end and the other three in favour of the distal end. It seems possible that this asymmetry within the gene may reflect intrinsic differences in the frequencies with which the dissociation of the DNA molecules is initiated at different linkage points.

(3) The hypothesis of a fairly constant amount of newly-synthesized DNA per dissociation cycle, irrespective of how it is distributed along the four templates from a linkage point, leads to a number of predictions for which there is evidence in support. These concern the detailed pattern of crossover and non-crossover hybrid DNA within the gene.

(4) Specific differences in intragenic recombination are attributed to differences in the pattern of DNA synthesis. The predominantly non-reciprocal recombination found within cistrons of Neurospora crassa would be explained if synthesis extends unequally from the linkage point in the two chromatids. The higher frequency of reciprocal recombination found in Aspergillus nidulans is attributed to more equal extension.

(5) Differences between meiotic and mitotic intragenic recombination both in A. nidulans and in Saccharomyces cerevisiae are explained on the supposition that more DNA synthesis per dissociation cycle occurs at mitosis than at meiosis.

(6) Clustering of sites in maps of alleles based on recombination frequencies is attributed to a rather limited range of variation in the lengths of the newly synthesized nucleotide chains.

Type
Research Article
Information
Genetics Research , Volume 6 , Issue 1 , February 1965 , pp. 27 - 92
Copyright
Copyright © Cambridge University Press 1965

References

REFERENCES

Calef, E. (1957). Effect on linkage maps of selection of crossovers between closely linked markers. Heredity, 11, 265–279.CrossRefGoogle Scholar
Case, M. E. & Giles, N. H. (1958). Evidence from tetrad analysis for both normal and aberrant recombination between allelic mutants in Neurospora crassa. Proc. nat. Acad. Sci., Wash., 44, 378–390.CrossRefGoogle ScholarPubMed
Case, M. E. & Giles, N. H. (1959). Recombination mechanisms at the pan-2 locus in Neuro-apora crassa. Cold Spr. Harb. Symp. quant. Biol. 23, 119–135.CrossRefGoogle Scholar
Case, M. E. & Giles, N. H. (1960). Comparative complementation and genetic maps of the pan-2 locus in Neurospora crassa. Proc. nat. Acad. Sci., Wash., 46, 659–676.CrossRefGoogle ScholarPubMed
Cooke, F. (personal communication).Google Scholar
De Serres, F. J. (1956). Studies with purple adenine mutants in Neurospora crassa. I. Structural and functional complexity in the ad-3 region. Genetics, 41, 668–676.CrossRefGoogle ScholarPubMed
De Serres, F. J. (1960). Studies with purple adenine mutants in Neurospora crassa. IV. Lack of complementation between different ad-3A mutants in heterokaryons and pseudo wild types. Genetics, 45, 555–566.CrossRefGoogle Scholar
Freese, E. (1957 a). The correlation effect for a histidine locus of Neurospora crassa. Genetics, 42, 671–684.CrossRefGoogle ScholarPubMed
Freese, E. (1957 b). Über die Feinstruktur des Genoms im Beriech eines pab Locus von Neurospora crassa. Z. indukt. Abstamm.- u. VererbLehre, 88, 388–406.Google Scholar
Gajewski, W., Kruszewska, A., Makarewicz, A., Paszewski, A., Surzycki, S. & Bielawska, H. (1963). Conversion and crossing-over as recombination mechanisms in Ascobolus immersus. Proc. XI Int. Congr. Genet. 1, 11 (Abstr.) (Oxford).Google Scholar
Giles, N. H. (1952). Studies on the mechanism of reversion in biochemical mutants of Neurospora crassa. Cold Spr. Harb. Symp. quant. Biol. 16, 283–313.CrossRefGoogle Scholar
Giles, N. H. (1956). Forward and back mutation at specific loci in Neurospora. Brookhaven Symp. Biol. 8, 103–125.Google Scholar
Giles, N. H. (1964). Genetic fine structure in relation to function in Neurospora. Proc. XI Int. Congr. Genet. 2, (in press) (Oxford).Google Scholar
Giles, N. H., De Serres, F. J. & Barbour, E. (1957). Studies with purple adenine mutants in Neurospora crassa. II. Tetrad analyses from a cross of an ad-3A mutant with an ad-3B mutant. Genetics, 42, 608–617.CrossRefGoogle ScholarPubMed
Hastings, P. J. & Whitehouse, H. L. K. (1964). A polaron model of genetic recombination by the formation of hybrid DNA. Nature, Lond., 201, 1052–1054.CrossRefGoogle Scholar
Holliday, R. (1962). Mutation and replication in Ustilago maydis. Genet. Res. 3, 472–486.Google Scholar
Holliday, R. (1964). A mechanism for gene conversion in fungi. Genet. Res. (in press).CrossRefGoogle Scholar
Hotta, Y. & Stern, H. (1961). Transient phosphorylation of deoxyribosides and regulation of deoxyribonucleic acid synthesis. J. Biophys. Biochem. Cytol. 11, 311–319.CrossRefGoogle ScholarPubMed
Kakar, S. N. (1963). Allelic recombination and its relation to recombination of outside markers in yeast. Genetics, 48, 957–966.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, 697–706.CrossRefGoogle Scholar
Lissouba, P. (1961). Mise en évidence d'une unité génétique polarisée et essai d'analyse d'un cas d'interférence négative. Ann. sci. not. Bot. et Biol. végétale, ser. 12, 1, 641–720.Google Scholar
Lissouba, P. & Rizet, G. (1960). Sur l'existence d'une unité génétique polarisée ne subissant que des échanges non réciproques. C. R. Acad. Sci., Paris, 250, 3408–3410.Google Scholar
Lissouba, P., Mousseau, J., Rizet, G. & Rossignol, J. L. (1962). Fine structure of genes in the ascomycete Ascobolus immersus. Advanc. Genet. 11, 343–380.Google Scholar
Marmur, J. & Lane, D. (1960). Strand separation and specific recombination in deoxyribonucleic acids: biological studies. Proc. nat. Acad. Sci., Wash., 46, 453–461.Google Scholar
Martin-Smith, C. A. (1961). A genetic investigation of the ad 9 cistron of Aspergillus nidulans. Ph.D. Thesis, University of Glasgow.Google Scholar
Mitchell, M. B. (1955). Aberrant recombination of pyridoxine mutants of Neurospora. Proc. nat. Acad. Sci., Wash., 41, 215–220.Google Scholar
Mitchell, M. B. (1956). A consideration of aberrant recombination in Neurospora. C. R. Lab. Carlsberg, Ser. Physiol., 26, 285–298.Google Scholar
Murray, N. E. (1960). Complementation and recombination between methionine-2 alleles in Neurospora crassa. Heredity, 15, 207–217.Google Scholar
Murray, N. E. (1963). Polarized recombination and fine structure within the me-2 gene of Neurospora crassa. Genetics, 48, 1163–1183.CrossRefGoogle ScholarPubMed
Olive, L. S. (1956). Genetics of Sordaria fimicola. I. Ascospore color mutants. Amer. J. Bot. 43, 97–107.CrossRefGoogle Scholar
Olive, L. S. (1959). Aberrant tetrads in Sordaria fimicola. Proc. nat. Acad. Sci., Wash., 45, 727–732.CrossRefGoogle ScholarPubMed
Pateman, J. A. (1960). High negative interference at the am locus in Neurospora crassa. Genetics, 45, 839–846.Google Scholar
Pontecorvo, G. & Käfer, E. (1958). Genetic analysis based on mitotic recombination. Advanc. Genet. 9, 71–104.CrossRefGoogle ScholarPubMed
Pritchard, R. H. (1955). The linear arrangement of a series of alleles of Aspergillus nidulans. Heredity, 9, 343–371.CrossRefGoogle Scholar
Pritchard, R. H. (1960 a). Localized negative interference and its bearing on models of gene recombination. Genet. Sea. 1, 1–24.Google Scholar
Pritchard, R. H. (1960 b). 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, 155–180.Google Scholar
Putrament, A. (1964). Mitotic recombination in the paba-l cistron of Aspergillus nidulans. Genet. Res. (in press).CrossRefGoogle 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, 1369–1384.CrossRefGoogle ScholarPubMed
Rizet, G., Lissouba, P. & Mousseau, J. (1961). Sur l'interférence négative au sein d'une série d'allèles chez Ascobolus immersus. C. R. Soc. Biol., Paris, 154, 1967–1970.Google Scholar
Rizet, G. & Rossignol, J. L. (1964). Recombination within one locus of Ascobolus immersus. Proc. XI Int. Congr. Genet. 2 (in press) (Oxford).Google Scholar
Roman, H. & Jacob, F. (1959). A comparison of spontaneous and ultraviolet-induced allelic recombination with reference to the recombination of outside markers. Cold Spr. Harb. Symp. quant. Biol. 23, 155–160.Google Scholar
St Lawrence, P. (1956). The q locus of Neurospora crassa. Proc. nat. Acad. Sci., Wash., 42, 189–194.Google Scholar
Setlow, R. B. & Carrier, W. L. (1964). The disappearance of thymine dimers from DNA: an error-correcting mechanism. Proc. nat. Acad. Sci., Wash., 51, 226–231.CrossRefGoogle ScholarPubMed
Sherman, F. & Roman, H. (1963). Evidence for two types of allelic recombination in yeast. Genetics, 48, 253–261.CrossRefGoogle ScholarPubMed
Siddiqi, O. H. (1962). The fine genetic structure of the paba-l region of Aspergillus nidulans. Genet. Res. 3, 69–89.CrossRefGoogle Scholar
Stadler, D. R. (1956). A map of linkage group VI of Neurospora crassa. Genetics, 41, 528–543.CrossRefGoogle ScholarPubMed
Stadler, D. R. (1959 a). Gene conversion of cysteine mutants in Neurospora. Genetics, 44, 647–655.Google Scholar
Stadler, D. R. (1959 b). The relationship of gene conversion to crossing over in Neurospora crassa. Proc. nat. Acad. Sci., Wash., 45, 1625–1629.CrossRefGoogle Scholar
Stadler, D. R. & Towe, A. M. (1963). Recombination of allelic cysteine mutants in Neurospora. Genetics, 48, 1323–1344.Google Scholar
Strickland, W. N. (1961). Tetrad analysis of short chromosome regions of Neurospora crassa. Genetics, 46, 1125–1141.CrossRefGoogle ScholarPubMed
Suyama, Y., Munkres, 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, 293–311.CrossRefGoogle Scholar
Taylor, J. H., Haut, W. F. & Tung, J. (1962). Effects of fluorodeoxyuridine on DNA replication, chromosome breakage, and reunion. Proc. nat. Acad. Sci., Wash., 48, 190–198.Google Scholar
Whitehouse, H. L. K. (1963). A theory of crossing-over by means of hybrid deoxyribonucleic acid. Nature, Lond., 199, 1034–1040.CrossRefGoogle ScholarPubMed
Wilkie, D. & Lewis, D. (1963). The effect of ultraviolet light on recombination in yeast. Genetics, 48, 1701–1716.Google Scholar
Wimber, D. E. & Prensky, W. (1963). Autoradiography with meiotic chromosomes of the male newt (Triturus viridescens) using H3-thymidine. Genetics, 48, 1731–1738.CrossRefGoogle ScholarPubMed