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Tetrad analysis in plants and fungi finds large differences in gene conversion rates but no GC bias

Nature Ecology & Evolution volume 2, pages 164–173 (2018)Cite this article

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Abstract

GC-favouring gene conversion enables fixation of deleterious alleles, disturbs tests of natural selection and potentially explains both the evolution of recombination as well as the commonly reported intragenomic correlation between G+C content and recombination rate. In addition, gene conversion disturbs linkage disequilibrium, potentially affecting the ability to detect causative variants. However, the importance and generality of these effects is unresolved, not simply because direct analyses are technically challenging but also because previous within- and between-species discrepant results can be hard to appraise owing to methodological differences. Here we report results of methodologically uniform whole-genome sequencing of all tetrad products in Saccharomyces, Neurospora, Chlamydomonas and Arabidopsis. The proportion of polymorphic markers converted varies over three orders of magnitude between species (from 2% of markers converted in yeast to only ~0.005% in the two plants) with at least 87.5% of the variance in per tetrad conversion rates being between species. This is largely due to differences in recombination rate and median tract length. Despite three of the species showing a positive GC-recombination correlation, there is no significant net AT→GC conversion bias in any of the species, despite relatively high resolution in the two taxa (Saccharomyces and Neurospora) with relatively common gene conversion. The absence of a GC bias means that: (1) there should be no presumption that gene conversion is GC biased, or (2) that a GC-recombination correlation necessarily implies biased gene conversion, (3) K a/K s tests should be unaffected in these species and (4) it is unlikely that gene conversion explains the evolution of recombination.

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Fig. 1: Schematic of experiment design.
Fig. 2: Outcomes of DSBR and SDSA pathways in meiotic recombination.
Fig. 3: Estimation of tract length for gene-conversion events.

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (91731308, 91631104 and 31671322 to S.Y. or D.T.) and the European Research Council (Advanced grant ERC-2014-ADG 669207 to L.D.H.). We are indebted to D. Liu for advice on Chlamydomonas experiments. We thank S. Li, C. Tian and W. Sun for providing the Neurospora strains that were used in this study.

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  1. Haoxuan Liu, Ju Huang and Xiaoguang Sun contributed equally to this work.

Authors and Affiliations

  1. State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University, Nanjing, China

    Haoxuan Liu, Ju Huang, Xiaoguang Sun, Yingwen Hu, Luyao Yu, Dacheng Tian & Sihai Yang

  2. Institute for Research on Cancer and Aging, Nice (IRCAN), CNRS UMR7284, INSERM U1081, University of Nice Sophia Antipolis, Nice, France

    Jing Li & Gianni Liti

  3. The Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, Bath, UK

    Laurence D. Hurst

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Contributions

S.Y., L.D.H., D.T. and H.L. designed the experiments. H.L., J.H., X.S., J.L., Y.H., L.Y., S.Y, L.D.H. and G.L. performed the experiments and analysed the data. L.D.H., H.L., S.Y. and D.T. wrote the paper.

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Correspondence to Laurence D. Hurst or Sihai Yang.

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Supplementary discussion; supplementary figures 1–11; supplementary tables 1–7.

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Liu, H., Huang, J., Sun, X. et al. Tetrad analysis in plants and fungi finds large differences in gene conversion rates but no GC bias. Nat Ecol Evol 2, 164–173 (2018). https://doi.org/10.1038/s41559-017-0372-7

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