Current Biology
Volume 31, Issue 21, 8 November 2021, Pages 4713-4726.e4
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Article
Evolution of crossover interference enables stable autopolyploidy by ensuring pairwise partner connections in Arabidopsis arenosa

https://doi.org/10.1016/j.cub.2021.08.028Get rights and content
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Highlights

  • In a neo-autotetraploid, aberrant crossover interference confers aberrant meiosis

  • In a stable autotetraploid, regular crossover interference confers regular meiosis

  • Crossover and synaptic patterns point to evolution of “supercharged” interference

  • Accordingly, evolution of stable autotetraploidy preadapts to higher ploidies

Summary

Polyploidy is a major driver of evolutionary change. Autopolyploids, which arise by within-species whole-genome duplication, carry multiple nearly identical copies of each chromosome. This presents an existential challenge to sexual reproduction. Meiotic chromosome segregation requires formation of DNA crossovers (COs) between two homologous chromosomes. How can this outcome be achieved when more than two essentially equivalent partners are available? We addressed this question by comparing diploid, neo-autotetraploid, and established autotetraploid Arabidopsis arenosa using new approaches for analysis of meiotic CO patterns in polyploids. We discover that crossover interference, the classical process responsible for patterning of COs in diploid meiosis, is defective in the neo-autotetraploid but robust in the established autotetraploid. The presented findings suggest that, initially, diploid-like interference fails to act effectively on multivalent pairing and accompanying pre-CO recombination interactions and that stable autopolyploid meiosis can emerge by evolution of a “supercharged” interference process, which can now act effectively on such configurations. Thus, the basic interference mechanism responsible for simplifying CO patterns along chromosomes in diploid meiosis has evolved the capability to also simplify CO patterns among chromosomes in autopolyploids, thereby promoting bivalent formation. We further show that evolution of stable autotetraploidy preadapts meiosis to higher ploidy, which in turn has interesting mechanistic and evolutionary implications.

Keywords

meiosis, chromosome pairing, polyploidy, crossover interference, Arabidopsis, Arabidopsis arenosa

Data and code availability

  • Microscopy data has been deposited at the ETH research collection and is publicly available as of the date of publication. The DOI is listed in the Key resources table. Primary component homolog measurements have been deposited at Mendeley and are publicly available as of the date of publication. The DOI is listed in the Key resources table.

  • All original code has been deposited at Zenodo and is publicly available as of the date of publication. DOIs are listed in the Key resources table.

  • Any additional information required to reanalyze the data reported in this paper is available from the lead contact upon request.

Cited by (0)

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Present address: Institute of Molecular Plant Biology, Department of Biology, ETH-Zürich, Universitätsstrasse 2, 8092 Zürich, Switzerland

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These authors contributed equally

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Twitter: @KBomblies

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Lead contact