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Unleashing meiotic crossovers in hybrid plants

  1. Raphael Merciera,2
  1. aInstitut Jean-Pierre Bourgin (IJPB), Institut National de la Recherche Agronomique, AgroParisTech, CNRS, Université Paris-Saclay, 78000 Versailles, France;
  2. bUniversité Paris-Sud, Université Paris-Saclay, 91405 Orsay, France
  1. Edited by R. Scott Hawley, Stowers Institute for Medical Research, Kansas City, MO, and approved October 31, 2017 (received for review July 23, 2017)

Significance

In eukaryotes, meiotic recombination shuffles genetic information at each generation, making each offspring unique. In addition to its key role in heredity and evolution, this gene reshuffling is central in plant and animal breeding, which relies on the ability to combine desired alleles. However, the number of recombination events by generation is low, limiting the power of breeding programs. Here we showed that meiotic recombination can be massively increased in hybrid plants, up to almost eightfold. This opens the possibility of manipulating recombination to enhance the efficiency of plant breeding programs, which is important as we face the double challenge of ensuring food security while preserving natural resources.

Abstract

Meiotic crossovers shuffle parental genetic information, providing novel combinations of alleles on which natural or artificial selection can act. However, crossover events are relatively rare, typically one to three exchange points per chromosome pair. Recent work has identified three pathways limiting meiotic crossovers in Arabidopsis thaliana that rely on the activity of FANCM [Crismani W, et al. (2012) Science 336:1588–1590], RECQ4 [Séguéla-Arnaud M, et al. (2015) Proc Natl Acad Sci USA 112:4713–4718], and FIGL1 [Girard C, et al. (2015) PLoS Genet 11:e1005369]. Here we analyzed recombination in plants in which one, two, or all three of these pathways were disrupted in both pure line and hybrid contexts. The greatest effect was observed when combining recq4 and figl1 mutations, which increased the hybrid genetic map length from 389 to 3,037 cM. This corresponds to an unprecedented 7.8-fold increase in crossover frequency. Disrupting the three pathways did not further increase recombination, suggesting that some upper limit had been reached. The increase in crossovers is not uniform along chromosomes and rises from centromere to telomere. Finally, although in wild type recombination is much higher in male meiosis than in female meiosis (490 cM vs. 290 cM), female recombination is higher than male recombination in recq4 figl1 (3,200 cM vs. 2,720 cM), suggesting that the factors that make wild-type female meiosis less recombinogenic than male wild-type meiosis do not apply in the mutant context. The massive increase in recombination observed in recq4 figl1 hybrids opens the possibility of manipulating recombination to enhance plant breeding efficiency.

Footnotes

  • ?1J.B.F. and M.S.-A. contributed equally to this work.

  • ?2To whom correspondence should be addressed. Email: raphael.mercier{at}inra.fr.
  • Author contributions: R.M. designed research; J.B.F., M.S.-A., and C.L. performed research; J.B.F., M.S.-A., A.H.L., and R.M. analyzed data; and J.B.F. and R.M. wrote the paper.

  • Conflict of interest statement: Patents have been deposited by INRA on the use of RECQ4, FIGL1, and FANCM to manipulate meiotic recombination (EP3149027, EP3016506, and EP2755995).

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.danielhellerman.com/lookup/suppl/doi:10.1073/pnas.1713078114/-/DCSupplemental.

Published under the PNAS license.

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