Recombination suppression in heterozygotes for a pericentric inversion induces the interchromosomal effect on crossovers in Arabidopsis

Authors: Pasquale Termolino, Matthieu Falque, Riccardo Aiese Cigliano, Gaetana Cremona, Rosa Paparo, Antoine Ederveen, Olivier C. Martin, Federica M. Consiglio, Clara Conicella

Institutions:

Institute of Biosciences and Bioresources (IBBR), National Research Council of Italy (CNR), 80055 Portici, Italy
Génétique Quantitative et Evolution‐Le Moulon, Institut National de la Recherche Agronomique, Université Paris‐Sud, CNRS, AgroParisTech, Université Paris‐Saclay, 91190 Gif‐sur‐Yvette, France
Sequentia Biotech, Barcelona, Spain
Department of Molecular Plant Physiology, Institute for Water and Wetland Research (IWWR), Radboud University Nijmegen, 9102 6500 Nijmegen, the Netherlands

Publication: The Plant Journal

Date: August 2019

Full paper: https://onlinelibrary.wiley.com/doi/full/10.1111/tpj.14505

Abstract:

During meiosis, recombination ensures allelic exchanges through crossovers (COs) between the homologous chromosomes. Advances in our understanding of the rules of COs have come from studies of mutations including structural chromosomal rearrangements that, when heterozygous, are known to impair COs in various organisms. In this work, we investigate the effect of a large heterozygous pericentric inversion on male and female recombination in Arabidopsis. The inversion was discovered in the Atmcc1 mutant background and was characterized through genetic and next‐generation sequencing analysis. Reciprocal backcross populations, each consisting of over 400 individuals, obtained from the mutant and the wild type, both crossed with Landsberg erecta, were analyzed genome‐wide by 143 single‐nucleotide polymorphisms. The negative impact of inversion became evident in terms of CO loss in the rearranged chromosome in both male and female meiosis. No single‐CO event was detected within the inversion, consistent with a post‐meiotic selection operating against unbalanced gametes. Cytological analysis of chiasmata in F₁ plants confirmed that COs were reduced in male meiosis in the chromosome with inversion. Crossover suppression on the rearranged chromosome is associated with a significant increase of COs in the other chromosomes, thereby maintaining unchanged the number of COs per cell. The CO pattern observed in our study is consistent with the interchromosomal (IC) effect as first described in Drosophila. In contrast to male meiosis, in female meiosis no IC effect is visible. This may be related to the greater strength of interference that constrains the CO number in excess of the minimum value imposed by CO assurance in Arabidopsis female meiosis.