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Polarity of meiotic gene conversion in fungi: Contrasting views

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Abstract

The frequency of meiotic gene conversion often varies linearly from one end of the gene to the other. This phenomenon has been called ‘polarity’. In this review, we will primarily discuss studies of polarity that have been done in the yeastSaccharomyces cerevisiae (ARG4 and HIS4 loci) and inAscobolus (b2 locus) with an emphasis on possible mechanisms. The genetic and physical data obtained at these ‘hotspots’ of recombination strongly suggests that the formation of a polarity gradient reflects both the frequency of heteroduplex formation and the processing of this recombination intermediate by mismatch-repair-dependent processes.

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References

  1. Arndt, K., Styles, C. S., and Fink, G. R., Multiple global regulators controlHIS4 transcription in yeast. Science237 (1987) 874–880.

    Article  CAS  PubMed  Google Scholar 

  2. Beacham, I. R., Schweitzer, B. W., Warwick, H. M., and Carbon, J., The nucleotide sequence of the yeastARG4 gene. Gene29 (1984) 271–279.

    Article  CAS  PubMed  Google Scholar 

  3. Cao, L., Alani, E., and Klechner, N., A pathway for generation and processing of double-strand breaks during meiotic recombination inSaccharomyces cerevisiae. Cell61 (1990) 1089–1101.

    Article  CAS  PubMed  Google Scholar 

  4. De Massy, B., and Nicolas, A., The controlin cis of the position and the amount of theARG4 meiotic double-strand break ofSaccharomyces cerevisiae. EMBOJ. 12 (1993) 1459–1466.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Detloff, P., Sieber, J., Petes, T. D., Repair of specific base pair mismatches formed during meiotic recombination in the yeastSaccharomyces cerevisiae. Molec. cell. Biol.11 (1991) 737–745.

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Detloff, P., White, M. A., and Petes, T. D., Analysis of a gene conversion gradient at theHIS4 locus inSaccharomyces cerevisiae. Genetics132 (1992) 113–123.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Devlin, C., Tice-Baldwin, K., Shore, D., and Arndt, K., RAP1 is required for BAS1/BAS2 and GCN4-dependent transcription of the yeastHIS4 gene. Molec. cell. Biol.11 (1991) 3462–3651.

    Google Scholar 

  8. Donahue, T. F., Farabaugh, P. J., and Fink, G. R., The nucleotide sequence of theHIS4 region of yeast. Gene18 (1982) 47–59.

    Article  CAS  PubMed  Google Scholar 

  9. Esposito, M. S., Postmeiotic segregation inSaccharomyces, Molec. gen. Genet.111 (1971) 297–299.

    Article  CAS  PubMed  Google Scholar 

  10. Fogel, S., and Hurst, D. D., Meiotic gene conversion in yeast tetrads and the theory of recombination. Genetics57 (1967) 455–481.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Fogel, S., Mortimer, R. K., and Lusnak, K., Mechanisms of meiotic gene conversion, or “wanderings on a foreign strand”, in: The Molecular Biology of the YeastSaccharomyces, vol. 1, pp. 289–339. Eds J. R. Broach, E. W. Jones, and J. N. Strathern. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York 1981.

    Google Scholar 

  12. Goyon, C., and Lichten, M., Timing of molecular events in meiosis inSaccharomyces cerevisae: stable heteroduplex DNA is formed late in meiotic prophase. Molec. Cell. Biol.13 (1993) 373–382.

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Hamza, H., Haedens, V., Mekki-Berrada, A., and Rossignol, J. L., Hybrid DNA formation during meiotic recombination. Proc. natl Acad. Sci. USA78 (1981) 7648–7651.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Hastings, P. J., and Whitehouse, H. L., K., A polaron model of genetic recombination by the formation of hybrid deoxyribonucleic acid. Nature201 (1960) 1052–1054.

    Article  Google Scholar 

  15. Hastings, P. J., Measurement of restoration and conversion: its meaning for the mismatch repair hypothesis of conversion. Cold Spring Harb. Symp. quant. Biol.49 (1984) 49–53.

    Article  CAS  PubMed  Google Scholar 

  16. Hastings, P. J., Conversion events in fungi, in: Genetic Recombination, pp. 397–428. Eds R. Kucherlapati and G. Smith. American Society for Microbiology, Washington, D. C. 1988.

    Google Scholar 

  17. Holiday, R., A mechanism for gene conversion in fungi. Genet. Res.5 (1964) 282–304.

    Article  Google Scholar 

  18. Jessop, A. P., and Catcheside, D. G., Interallelic recombination at thehis-1 locus inNeurospora crassa and its genetic control. Heredity20 (1965) 237–256.

    Article  CAS  PubMed  Google Scholar 

  19. Kalogeropoulos, A., and Rossignol, J.-L., Hybrid DNA tracts may start at different sites during meiotic recombination in geneb2 ofAscobolus. EMBO J.7 (1988) 253–259.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Kalogeropoulos, A., and Rossignol, J-L., Non random transition from asymmetrical to symmetrical hybrid DNA during meiotic recombination. Genome32 (1989) 414–419.

    Article  Google Scholar 

  21. Kitani, Y., and Olive, L. S., Genetics ofSordaria fimicola. VI. Gene conversion at theg locus in mutant x wild-type crosses. Genetics57 (1967) 767–782.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Lichten, M., Goyon, C., Schultes, N. P., Treco, D., Szostak, J. W., Haber, J. E., and Nicolas, A., Detection of heteroduplex DNA molecules among the products ofSaccharomyces cerevisiae meiosis. Proc. natl Acad. Sci. USA87 (1990) 7653–7657.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Lissouba, P., and Rizet, G., Sur l'existence d'une unite génétique polarisée ne subissant que des échanges non réciproques. C. R. Acad. Sci., Paris250 (1960) 3408–3410.

    CAS  PubMed  Google Scholar 

  24. Malone, R. E., Bullard, S., Lundquist, S., Kim, S., and Tarkowski, T., A meiotic gene conversion gradient opposite to the direction of transcription. Nature359 (1992) 154–155.

    Article  CAS  PubMed  Google Scholar 

  25. Meselson, M. S., and Radding, C. M., A general model for genetic recombination. Proc. natl Acad. Sci. USA72 (1975) 358–361.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Murray, N. E., Complementation and recombination between methionine-2 alleles inNeurospora crassa. Genetics48 (1960) 1163–1183.

    Article  Google Scholar 

  27. Murray, N. E., Polarized intragenic recombination in chromosome rearrangements ofNeurospora. Genetics58 (1968) 181–191.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Nag, D. K., White, M. A., and Petes, T. D., Palindromic sequences in heteroduplex DNA inhibit mismatch repair in yeast. Nature340 (1989) 95–98.

    Article  Google Scholar 

  29. Nag, D. K., and Petes, T. D., Genetic evidence for preferential strand transfer during meiotic recombination in yeast. Genetics125 (1990) 753–761.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Nag, D. K., and Petes, T. D., Physical detection of heteroduplexes during meiotic recombination in the yeastSaccharomyces cerevisiae. Molec cell. Biol.13 (1993) 2324–2331.

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Nagawa, F., and Fink, G. R., The relationship between the “TATA” sequence and transcription initiation sites at theHIS4 gene ofSaccharomyces cerevisiae. Proc. natl Acad. Sci. USA82 (1985) 8557–8561.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Nicolas, A., and Rossignol, J. L., Gene conversion: Point mutation heterozygosities lower heteroduplex formation. EMBO J.2 (1983) 2265–2270.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Nicolas, A., and Rossignol, J.-L., Intermediates in homologous recombination revealed by marker effects inAscobolus. Genome31 (1989) 528–535.

    Article  CAS  Google Scholar 

  34. Nicolas, A., Treco, D., Schultes, N. P., and Szostak, J. W., An initiation site for gene conversion in the yeastSaccharomyces cerevisiae. Nature338 (1989) 35–39.

    Article  CAS  PubMed  Google Scholar 

  35. Paquette, N., and Rossignol, J.-L., Gene conversion spectrum of 15 mutants giving post-meiotic segregation in theb2 locus ofAscobolus immersus. Molec. gen. Genet.163 (1978) 313–326.

    Article  Google Scholar 

  36. Pees, E., Genetic fine structure and polarized negative interference at the lys-51 (FL) locus ofAspergillus nidulans. Genetica38 (1967) 275–304.

    Article  Google Scholar 

  37. Petes, T. D., Malone, R. E., and Symmington, L. S., Recombination in yeast, in: The Molecular and Cellular Biology of the YeastSaccharomyces, vol. 1, pp. 407–521. Eds J. R. Broach, E. W. Jones, and J. R. Pringle. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York 1991.

    Google Scholar 

  38. Porter, S. E., White, M. A., and Petes, T. D., Genetic evidence that the meiotic recombination hotspot at theHIS4 locus ofSaccharomyces cerevisiae does not represent a site for a symmetrically-processed double-strand break. Genetics134 (1993) 5–19.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Radding, C. M., Homologous pairing and strand exchange in genetic recombination. A. Rev. of Genet.16 (1982) 405–437.

    Article  CAS  Google Scholar 

  40. Radman, M., Mismatch repair and genetic recombination, in: Genetic Recombination, pp. 169–192. Eds R. Kucherlapati and G. Smith. American Society for Microbiology, Washington, D.C. 1988.

    Google Scholar 

  41. Reenan, R. A. G., and Kolodner, R. D., Characterization of insertion mutations in theSaccharomyces cerevisiae MSH1 andMSH2 genes: evidence for separate mitochondrial and nuclear functions. Genetics132 (1992) 975–985.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Rocco, V., de Massy, B., and Nicolas A., TheSaccharomyces cerevisiae ARG4 initiator of meiotic gene conversion and its associated double-strand DNA breaks can be inhibited by transcriptional interference. Proc. natl Acad. Sci. USA89 (1992) 12068–12072.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Ross, L., Treco, D., Nicolas, A., Szostak, J. W., and Dawson D., Meiotic recombination on artificial chromosomes in yeast. Genetics131 (1992) 541–550.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Rossignol, J.-L., and Paquette, N., Disparity of gene conversion in frameshift mutants located in locusb2 ofAscobolus immersus. Proc. natl Acad. Sci. USA76 (1979) 2871–2875.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Rossignol, J.-L., and Haedens, V., Relationship between asymmetrical and symmetrical hybrid DNA formation during meiotic recombination. Curr. Genet.1 (1980) 185–191.

    Article  CAS  PubMed  Google Scholar 

  46. Rossignol, J.-L., Nicolas, A., Hamza, H., and Langin, T., Origin of gene conversion and reciprocal exchange inAscobolus. Cold Spring Harbor Symp. quant. Biol.49 (1984) 13–21.

    Article  CAS  PubMed  Google Scholar 

  47. Rossignol, J.-L., Nicolas, A., Hamza, H., and Kalogeropoulos, A., Recombination and gene conversion inAscobolus, in: The Recombination of Genetic Material, pp. 23–72. Ed. K. B. Low. Academic Press, Inc., New York 1988.

    Chapter  Google Scholar 

  48. Savage, E. A., and Hastings, P. J., Marker effects and the nature of the recombination event at thehis1 locus ofSaccharomyces cerevisiae. Curr. Genet.3 (1981) 37–47.

    Article  CAS  PubMed  Google Scholar 

  49. Schultes, N. P., and Szostak, J. W., Decreasing gradients of gene conversion on both sides of the initiation site for meiotic recombination at theARG4 locus in yeast. Genetics126 (1990) 813–822.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Sun, H., Treco, D., Schultes, N. P., and Szostak, J. W., Double-strand breaks at an initiation site for meiotic gene conversion. Nature338 (1989) 87–89.

    Article  CAS  PubMed  Google Scholar 

  51. Sun, H., Treco, D., and Szostak, J. W., Extensive 3′-overhanging, single-stranded DNA associated with the meiosis-specific double-strand breaks at theARG4 recombination initiation site. Cell64 (1991) 1155–1161.

    Article  CAS  PubMed  Google Scholar 

  52. Szostak, J. W., Orr-Weaver, T. L., Rothstein, R. J., and Stahl, F. W., The double-strand-break repair model for recombination. Cell33 (1983) 25–35.

    Article  CAS  PubMed  Google Scholar 

  53. Tice-Baldwin, K., Fink, G. R., and Arndt, K. T., BAS1 has a Myb motif and activatesHIS4 transcription only in combination with BAS2. Science246 (1989) 931–935.

    Article  CAS  PubMed  Google Scholar 

  54. Trueheart, J., Boeke, J. D., and Fink, G. R., Two genes required for cell fusion during yeast conjugation: evidence for a pheromone-induced surface protein. Molec. cell. Biol.7 (1987) 2316–2328.

    CAS  PubMed  PubMed Central  Google Scholar 

  55. White, J. H., Lusnak, K., and Fogel, S., Mismatch-specific post-meiotic segregation frequency in yeast suggests a heteroduplex recombination intermediate. Nature315 (1985) 350–352.

    Article  CAS  PubMed  Google Scholar 

  56. White, M. A., Wierdl, M., Detloff, P., and Petes, T. D., DNA-binding protein RAP1 stimulates meiotic recombination at theHIS4 locus in yeast. Proc. natl Acad. Sci. USA88 (1991) 9755–9759.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. White, M. A., Detloff, P., Strand, M., and Petes, T. D., A promoter deletion reduces the rate of mitotic, but not meiotic, recombination at theHIS4 locus in yeast. Curr. Genet.21 (1992) 109–116.

    Article  CAS  PubMed  Google Scholar 

  58. White, M. A., Dominska, M., and Petes, T. D., Transcription factors are required for the meiotic recombination hotspot at theHIS4 locus inSaccharomyces cerevisiae. Proc. natl Acad. Sci. USA90 (1993) 6621–6625.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Whitehouse, H., Genetic Recombination, John Wiley & Sons, Ltd., New York, 1982.

    Google Scholar 

  60. Williamson, M. S., Game, J. C., and Fogel, S., Meiotic gene conversion mutants inSaccharomyces cerevisiae: I. Isolation and characterization ofpms1-1 andpms1-2. Genetics110 (1985) 609–646.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Institut de Génétique et Microbiologie, Université Paris-Sud, Bât. 400, 91405, Orsay Cedex, France

    A. Nicolas

  2. Department of Biology, University of North Carolina, 27599-3280, Chapel Hill, North Carolina, USA

    T. D. Petes

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  1. A. Nicolas
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This article is dedicated to the memory of Seymour Fogel.

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Nicolas, A., Petes, T.D. Polarity of meiotic gene conversion in fungi: Contrasting views. Experientia 50, 242–252 (1994). https://doi.org/10.1007/BF01924007

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