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

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

doi:10.1111/tpj.14505

Abstract

SummaryDuring 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.

Highlights

Meiotic recombination is fundamental in creating genetic diversity through the shuffling of alleles over generations
We investigated the recombination in male and female meiosis by analyzing
Single Nucleotide Polymorphism (SNP) analyzed in the four BC1 populations, were 1871 in Mmut (N=418 plants) and 1259 in Fmut (N=417 plants), while 1834 and 1279 COs were found in Mctr (N=414 plants) and Fctr (N=410 plants), respectively

Summary

Introduction

Meiotic recombination is fundamental in creating genetic diversity through the shuffling of alleles over generations. Recombination is initiated by the formation of DNA double-strand breaks (DSBs) that are repaired, partly, as crossovers (COs), i.e., through reciprocal exchanges between the homologous chromosomes. To ensure proper chromosome segregation at Meiosis I, at least one CO per homologous chromosome pair (obligatory CO) has to occur while the formation of excess COs is almost always limited, possibly by mechanical reasons (such as entanglement) or evolutionary pressures (putative mutagenicity of COs). CO homeostasis has been documented in yeast [3] and mouse [5]. In the latter, the authors suggested that homeostatic control operates at the different steps of meiotic recombination in a progressive manner, i.e., from the formation of early recombination intermediates till CO formation after homologs have fully synapsed during pachytene. CO homeostasis does not seem to be prominent in maize [7]

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