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A novel allele of ASY3 is associated with greater meiotic stability in autotetraploid Arabidopsis lyrata

Seear, Paul J.; France, Martin G.; Gregory, Catherine L.; Heavens, Darren; Schmickl, Roswitha; Yant, Levi; Higgins, James D.

A novel allele of ASY3 is associated with greater meiotic stability in autotetraploid Arabidopsis lyrata Thumbnail


Authors

Paul J. Seear

Martin G. France

Catherine L. Gregory

Darren Heavens

Roswitha Schmickl

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LEVI YANT LEVI.YANT@NOTTINGHAM.AC.UK
Professor of Evolutionary Genomics

James D. Higgins



Contributors

Mathilde Grelon
Editor

Abstract

In this study we performed a genotype-phenotype association analysis of meiotic stability in 10 autotetraploid Arabidopsis lyrata and A. lyrata/A. arenosa hybrid populations collected from the Wachau region and East Austrian Forealps. The aim was to determine the effect of eight meiosis genes under extreme selection upon adaptation to whole genome duplication. Individual plants were genotyped by high-throughput sequencing of the eight meiosis genes (ASY1, ASY3, PDS5b, PRD3, REC8, SMC3, ZYP1a/b) implicated in synaptonemal complex formation and phenotyped by assessing meiotic metaphase I chromosome configurations. Our results reveal that meiotic stability varied greatly (20-100%) between individual tetraploid plants and associated with segregation of a novel ASYNAPSIS3 (ASY3) allele derived from A. lyrata. The ASY3 allele that associates with meiotic stability possesses a putative in-frame tandem duplication (TD) of a serine-rich region upstream of the coiled-coil domain that appears to have arisen at sites of DNA microhomology. The frequency of multivalents observed in plants homozygous for the ASY3 TD haplotype was significantly lower than in plants heterozygous for ASY3 TD/ND (non-duplicated) haplotypes. The chiasma distribution was significantly altered in the stable plants compared to the unstable plants with a shift from proximal and interstitial to predominantly distal locations. The number of HEI10 foci at pachytene that mark class I crossovers was significantly reduced in a plant homozygous for ASY3 TD compared to a plant heterozygous for ASY3 ND/TD. Fifty-eight alleles of the 8 meiosis genes were identified from the 10 populations analysed, demonstrating dynamic population variability at these loci. Widespread chimerism between alleles originating from A. lyrata/A. arenosa and diploid/tetraploids indicates that this group of rapidly evolving genes may provide precise adaptive control over meiotic recombination in the tetraploids, the very process that gave rise to them.

Citation

Seear, P. J., France, M. G., Gregory, C. L., Heavens, D., Schmickl, R., Yant, L., & Higgins, J. D. (2020). A novel allele of ASY3 is associated with greater meiotic stability in autotetraploid Arabidopsis lyrata. PLoS Genetics, 16(7), Article e1008900. https://doi.org/10.1371/journal.pgen.1008900

Journal Article Type Article
Acceptance Date Jun 1, 2020
Online Publication Date Jul 15, 2020
Publication Date Jul 1, 2020
Deposit Date Jul 18, 2020
Publicly Available Date Mar 28, 2024
Journal PLoS genetics
Print ISSN 1553-7390
Electronic ISSN 1553-7404
Publisher Public Library of Science
Peer Reviewed Peer Reviewed
Volume 16
Issue 7
Article Number e1008900
DOI https://doi.org/10.1371/journal.pgen.1008900
Keywords Genetics(clinical); Genetics; Cancer Research; Ecology, Evolution, Behavior and Systematics; Molecular Biology
Public URL https://nottingham-repository.worktribe.com/output/4773229
Publisher URL https://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1008900

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