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Analysis of the meiotic recombination frequency in transgenic tomato hybrids expressing recA and NLS-recA-licBM3 genes

  • Plant Genetics
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Abstract

To study and induce meiotic recombination in plants, we generated and analyzed transgenic tomato hybrids F1-RecA and F1-NLS-recA-LicBM3 expressing, respectively, the recA gene of Escherichia coli and the NLS-recA-licBM3 gene. It was found that the recA and NLS-recA-licBM3 genes are inherited through the maternal and paternal lineages, they have no selective influence on the pollen and are contained in tomato F1-RecA and F1-NLS-RecA-LicBM3 hybrids outside the second chromosome in the hemizygous state. The comparative analysis of the meiotic recombination frequency (rf) in the progenies of the transgenic and nontransgenic hybrids showed that only the expression of the recA gene of E. coli in cells of the F1-RecA plants produced a 1.2–1.5-fold increase in the frequency of recombination between some linked marker genes of the second chromosome of tomato.

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References

  1. Zhuchenko, A.A., Adaptivnaya sistema selektsii rastenii (ekologo-geneticheskie osnovy) (Adaptive System of Plant Breeding (Ecological and Genetic Bases)), Moscow: Agroruss, 2001.

    Google Scholar 

  2. Bogdanov, Yu.F. and Kolomiets, O.L., Sinaptonemnyi kompleks—indikator dinamiki meioza i izmenchivosti khromosom (Synaptonemal Complex—an Indicator of Meiosis Dynamics and Chromosome Variation), Moscow: KMK, 2007.

    Google Scholar 

  3. Falque, M., Anderson, L.K., Stack, S.M., et al., Two Types of Meiotic Crossovers Coexist in Maize, Plant Cell, 2009, vol. 21, pp. 3915–3925.

    Article  PubMed  CAS  Google Scholar 

  4. Hollingsworth, N.M. and Brill, S.J., The Mus81 Solution to Resolution: Generating Meiotic Crossovers without Holliday Junctions, Genes Dev., 2004, vol. 18, pp. 117–125.

    Article  PubMed  CAS  Google Scholar 

  5. Mezard, C., Vignard, J., Drouaud, J., and Mercier, R., The Road to Crossovers: Plants Have Their Say, Trends Genet., 2007, vol. 23, pp. 91–99.

    Article  PubMed  CAS  Google Scholar 

  6. Froenicke, L., Anderson, L.K., Wienberg, J., and Ashley, T., Male Mouse Recombination Maps for Each Autosome Identified by Chromosome Painting, Am. J. Hum. Genet., 2002, vol. 71, pp. 1353–1368.

    Article  PubMed  CAS  Google Scholar 

  7. Broman, K.W., Rowe, L.B., Churchill, G.A., and Paigen, K., Crossover Interference in the Mouse, Genetics, 2002, vol. 160, pp. 1123–1131.

    PubMed  Google Scholar 

  8. Falque, M., Mercier, R., Mezard, C., et al., Patterns of Recombination and MLH1 Foci Density along Mouse Chromosomes: Modeling Effects of Interference and Obligate Chiasma, Genetics, 2007, vol. 176, pp. 1453–1467.

    Article  PubMed  CAS  Google Scholar 

  9. Santos, T., Hunter, N., Lee, C., et al., The Mus81/Mms4 Endonuclease Acts Independently of Double-Holliday Junction Resolution to Promote a Distinct Subset of Crossovers during Meiosis in Budding Yeast, Genetics, 2003, vol. 164, pp. 81–94.

    PubMed  Google Scholar 

  10. Lhuissier, F.G., Offenberg, H.H., Wittich, P.E., et al., The Mismatch Repair Protein MLH1 Marks a Subset of Strongly Interfering Crossovers in Tomato, Plant Cell, 2007, vol. 19, pp. 862–876.

    Article  PubMed  CAS  Google Scholar 

  11. Zalevsky, J., MacQueen, A.J., Duffy, J.B., et al., Crossing over during Caenorhabditis elegans Meiosis Requires a Conserved MutS-Based Pathway That Is Partially Dispensable in Budding Yeast, Genetics, 1999, vol. 153, pp. 1271–1283.

    PubMed  CAS  Google Scholar 

  12. Hillers, K.J. and Villeneuve, A.M., Chromosome-Wide Control of Meiotic Crossing over in C. elegans, Curr. Biol., 2003, vol. 13, pp. 1641–1647.

    Article  PubMed  CAS  Google Scholar 

  13. Munz, P., An Analysis of Interference in the Fission Yeast Schizosaccharomyces pombe, Genetics, 1994, vol. 137, pp. 701–707.

    PubMed  CAS  Google Scholar 

  14. Anderson, L.K. and Stack, S.M., Meiotic Recombination in Plants, Curr. Genomics, 2002, vol. 3, pp. 507–525.

    Article  CAS  Google Scholar 

  15. Drouaud, J., Camilleri, C., Bourguignon, P.Y., et al., Variation in Crossing-Over Rates across Chromosome 4 of Arabidopsis thaliana Reveals the Presence of Meiotic Recombination “Hot Spots”, Genome Res., 2006, vol. 16, no. 1, pp. 106–114.

    Article  PubMed  CAS  Google Scholar 

  16. Mezard, C., Meiotic Recombination Hotspots in Plants, Biochem. Soc. Trans., 2006, vol. 34, no. 4, pp. 531–534.

    Article  PubMed  CAS  Google Scholar 

  17. Rick, C.M., Recombination, Genetics, 1969, vol. 62, pp. 753–768.

    PubMed  CAS  Google Scholar 

  18. Chetelat, R.T., Meglic, V., and Cisneros, P., A Genetic Map of Tomato Based on BC(1) Lycopersicon esculentum × Solanum lycopersicoides Reveals Overall Synteny but Suppressed Recombination between These Homeologous Genomes, Genetics, 2000, vol. 154, pp. 857–867.

    PubMed  CAS  Google Scholar 

  19. Wijnker, E. and de Jong, H., Managing Meiotic Recombination in Plant Breeding, Trends Plant Sci., 2008, vol. 13, no. 12, pp. 640–646.

    Article  PubMed  CAS  Google Scholar 

  20. Gavrilenko, T.A., Temperature Effect on Recombination in Tomatoes, Tsitol. Genet., 1984, vol. 18, no. 5, pp. 347–352.

    Google Scholar 

  21. Sall, T., Flink, J., and Bengtsson, B.O., Genetic Control of Recombination in Barley: Variation in Recombination Frequency Measured with Inversion Heterozygotes, Hereditas, 1990, vol. 112, pp. 157–170.

    Article  Google Scholar 

  22. Sanchez-Moran, E., Armstrong, S.J., Santos, J.L., et al., Variation in Chiasma Frequency among Eight Accessions of Arabidopsis thaliana, Genetics, 2002, vol. 162, pp. 1415–1422.

    PubMed  CAS  Google Scholar 

  23. Drouaud, J., Mercier, R., Chelysheva, L., et al., Sex-Specific Crossover Distributions and Variations in Interference Level along Arabidopsis thaliana Chromosome 4, PLoS Genet., 2007, vol. 3, no. 6, pp. 1096–1107.

    Article  CAS  Google Scholar 

  24. Petkov, P.M., Broman, K.W., Szatkiewicz, J.P., and Paigen, K., Crossover Interference Underlies Sex Differences in Recombination Rates, Trends Genet., 2007, vol. 23, pp. 539–542.

    Article  PubMed  CAS  Google Scholar 

  25. Ma, H., A Molecular Portrait of Arabidopsis Meiosis, The Arabidopsis Book, 2006, pp. 1–39.

  26. Mercier, R. and Grelon, M., Meiosis in Plants: Ten Years of Gene Discovery, Cytogenet. Genome Res., 2008, vol. 120, pp. 281–290.

    Article  PubMed  CAS  Google Scholar 

  27. Masson, J.E. and Paszkowski, J., Arabidopsis thaliana Mutants Altered in Homologous Recombination, Proc. Natl. Acad. Sci. USA, 1997, vol. 94, pp. 11731–11735.

    Article  PubMed  CAS  Google Scholar 

  28. Komakhin, R.A., Komakhina, V.V., and Zhuchenko, A.A., The Creation of Genetic Constructions Containing Bacterial Gene resA E. coli for Recombination Induction in Plants, S-kh. Biol., 2007, no. 3, pp. 25–32.

  29. Emmanuel, E., Yehuda, E., Melamed-Bessudo, C., et al., The Role of AtMSH2 in Homologous Recombination in Arabidopsis thaliana, EMBO Rep., 2006, vol. 7, no. 1, pp. 100–1005.

    Article  PubMed  CAS  Google Scholar 

  30. Hunter, N., Chambers, S.R., Louis, E.J., and Borts, R.H., The Mismatch Repair System Contributes to Meiotic Sterility in an Interspecific Yeast Hybrid, EMBO J., 1996, vol. 15, pp. 1726–1733.

    PubMed  CAS  Google Scholar 

  31. Leonard, J.M., Bollmann, S.R., and Hays, J.B., Reduction of Stability of Arabidopsis Genomic and Transgenic DNA-Repeat Sequences (Microsatellites) by Inactivation of AtMSH2 Mismatch-Repair Function, Plant Physiol., 2003, vol. 133, no. 1, pp. 328–338.

    Article  PubMed  CAS  Google Scholar 

  32. Hoffman, P.D., Leonard, J.M., Lindberg, G.E., et al., Rapid Accumulation of Mutations during Seed-to-Seed Propagation of Mismatch-Repair-Defective Arabidopsis, Genes Dev., 2004, vol. 18, no. 21, pp. 2676–2685.

    Article  PubMed  CAS  Google Scholar 

  33. Reiss, B., Klemm, M., Kosak, H., and Schell, J., RecA Protein Stimulates Homologous Recombination in Plants, Proc. Natl. Acad. Sci. USA, 1996, vol. 93, no. 7, pp. 3094–3098.

    Article  PubMed  CAS  Google Scholar 

  34. Reiss, B., Schubert, I., Kopchen, K., et al., RecA Stimulates Sister Chromatid Exchange and the Fidelity of Double-Strand Break Repair, but not Gene Targeting, in Plants Transformed by Agrobacterium, Proc. Natl. Acad. Sci. USA, 2000, vol. 97, no. 7, pp. 3358–3363.

    Article  PubMed  CAS  Google Scholar 

  35. Lantsov, V.A., RecA Homologous DNA Transferase: Functional Activities and a Search for Homology by Recombining DNA Molecules, Mol. Biol., 2007, vol. 41, no. 3, pp. 417–426.

    Article  Google Scholar 

  36. Komakhin, R.A., Komakhina, V.V., Milyukova, N.A., et al., Transgenic Tomato Plants Expressing resA and NLS-resA-lisVM3 Genes as a Model for Studying Meiotic Recombination, Russ. J. Genet., 2010, vol. 46, no. 12, pp. 1440–1448.

    Article  CAS  Google Scholar 

  37. Bocharnikova, N.I. and Kozlova, V.M., Mutantnye formy tomatov (Mutant Forms of Tomatoes), Chisinau: Shtiintsa, 1992.

    Google Scholar 

  38. Dospekhov, B.A., Metodika polevogo opyta (Methods of Field Experiment), Moscow: Kolos, 1973.

    Google Scholar 

  39. Orlova, N.N., Geneticheskii analiz (Genetic Analysis), Moscow: Mosk. Gos. Univ., 1991.

    Google Scholar 

  40. Yunusov, Z.R., Solov’ev, A.A., Mikhailenko, S.N., et al., Transgenes Effect on Meiotic Recombination in Higher Eukaryotes by Example of Tomato Plants, S-kh. Biol., 2009, no. 3, pp. 52–59.

  41. Strel’nikova, S.R., Frequency Chiasm Evaluation in Wild Species, Mutant Forms, and F1 Hybrids of Tomatoes, Cand. Sci. (Biol.) Dissertation, Moscow: Moscow Timiryazev Agric. Acad., 2001, p. 111.

    Google Scholar 

  42. Bocharnikova, N.I., Ushchapovskii, I.V., and Kazantsev, E.F., Influence of Genotypic Environment on the Crossing-Over Frequency in Tomato Plants, Genetika (Moscow), 1991, vol. 27, no. 2, pp. 361–363.

    Google Scholar 

  43. Kharrasova, L.K., Effect of Growth Conditions on Recombination Frequency in Tomato, Dokl. Timiryazev S-kh. Akad., 2001, no. 273, pp. 33–36.

  44. Zhuchenko, A.A., Korol’, A.B., Vizir, I.Yu., et al., Sex Differences in Crossover Frequency for Tomato and Arabidopsis, Genetika (Moscow), 1988, vol. 24, no. 9, pp. 1593–1601.

    Google Scholar 

  45. Bocharnikova, N.I., Specificity of Formation of Genetic Variation in the Genus Lycopersicon Tourn. and Its Significance for Breeding, Doctoral (Agric.) Dissertation, Moscow: All-Russ. Res. Inst. Sel. Seed Farming Vegetable Cultures Ross. Acad. Agric., 2007, p. 294.

    Google Scholar 

  46. Bakhlanova, I.V., Dudkina, A.V., Baitin, D.M., et al., Modulating Cellular Recombination Potential through Alterations in RecA Structure and Regulation, Mol. Microbiol., 2010, vol. 78, no. 6, pp. 1523–1538.

    Article  PubMed  CAS  Google Scholar 

  47. Li, W., Chen, C., Markmann-Mulisch, U., et al., The Arabidopsis AtRAD51 Gene Is Dispensable for Vegetative Development but Required for Meiosis, Proc. Natl. Acad. Sci. USA, 1997, vol. 101, no. 29, pp. 10596–10601.

    Article  Google Scholar 

  48. Baumann, P. and West, S.C., Role of the Human RAD51 Protein in Homologous Recombination and Double-Strand-Break Repair, Trends Biochem. Sci., 1998, vol. 23, no. 7, pp. 248–251.

    Article  Google Scholar 

  49. Kawabata, M., Kawabata, T., and Nishibori, M., Role of RecA/RAD51 Family Proteins in Mammals, Acta Med. Okayama, 2005, vol. 59, no. 1, pp. 1–9.

    PubMed  CAS  Google Scholar 

  50. Brenneman, M.A., Weiss, A.E., Nickoloff, J.A., and Chen, D.J., Xrcc3 Is Required for Efficient Repair of Chromosome Breaks by Homologous Recombination, Mutat. Res., 2000, vol. 459, no. 2, pp. 89–97.

    PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. All-Russia Research Institute of Agricultural Biotechnology, Russian Academy of Agricultural Sciences, Moscow, 127550, Russia

    R. A. Komakhin, V. V. Komakhina & N. A. Milyukova

  2. Department of Genetics and Biotechnology, Russian State Agrarian University-MTAA, Moscow, 127550, Russia

    N. A. Milyukova

  3. Vavilov Institute of General Genetics, Russian Academy of Sciences, Moscow, 119991, Russia

    A. A. Zhuchenko

Authors
  1. R. A. Komakhin
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  2. V. V. Komakhina
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  3. N. A. Milyukova
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  4. A. A. Zhuchenko
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Correspondence to R. A. Komakhin.

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Original Russian Text © R.A. Komakhin, V.V. Komakhina, N.A. Milyukova, A.A. Zhuchenko, 2012, published in Genetika, 2012, Vol. 48, No. 1, pp. 30–39.

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Komakhin, R.A., Komakhina, V.V., Milyukova, N.A. et al. Analysis of the meiotic recombination frequency in transgenic tomato hybrids expressing recA and NLS-recA-licBM3 genes. Russ J Genet 48, 23–31 (2012). https://doi.org/10.1134/S1022795411110093

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  • DOI: https://doi.org/10.1134/S1022795411110093

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