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

Abstract

During meiosis, recombination ensures the allele exchange through crossovers (COs) between the homologous chromosomes and, additionally, their proper segregation. CO events are under a strict control but molecular mechanisms underlying CO regulation are still elusive. Some advances in this field were made by structural chromosomal rearrangements that are known at heterozygous state to impair COs in various organisms. In this paper, we have investigated the effect that a large pericentric inversion involving chromosome 3 of Arabidopsis thaliana has on male and female recombination. The inversion associated to a T-DNA dependent mutation likely resulted from a side effect of the T-DNA integration. Reciprocal backcross populations, each consisting of over 400 individuals, obtained from the T-DNA mutant and the wild type, both crossed with Landsberg, have been analyzed at genome-wide level by 143 SNPs. We found a strong suppression of COs in the rearranged region in both male and female meiosis. As expected, we did not detect single COs in the inverted region consistently with the post-meiotic selection operating against unbalanced gametes. Cytological analysis of chiasmata in F1 plants confirmed that COs are effectively dropping in chromosome 3 pair. Indeed, CO failure within the inversion is not altogether counterbalanced by CO increase in the regions outside the inversion on chromosome 3. Strikingly, this CO suppression induces a significant increase of COs in chromosome pairs 1, 2 and 5 in male meiosis. We conclude that these chromosomes acquire additional COs thereby compensating the recombination suppression occurring in chromosome 3, similarly to what has been described as interchromosomal (IC) effect in other organisms. In female meiosis, IC effect is not evident. This may be related to the fact that CO number in female is close to the minimum value imposed by the obligatory CO rule.\n\nAuthor SummaryIt is well known that chromosome structure changes in heterozygous condition influence the pattern of meiotic recombination at broad scale. In natural populations, inversions are recognized as the most effective force to reduce COs. In this way, adaptive allele combinations which otherwise would be broken by recombination are maintained. In the present work, we studied the effect on recombination of a large pericentric inversion involving Arabidopsis chromosome 3. The analysis on heterozygous populations provided evidence of strong recombination suppression in chromosome 3. However, the most striking aspect of this study is the finding that the failure of chromosome 3 to recombine is coupled to increased CO frequencies on the other chromosome pairs in male meiosis. These CO compensatory increases are strictly an interchromosomal (IC) effect as was first described in Drosophila. As far as we know, it is the first time IC effect has been reported in plants. Unfortunately, the molecular mechanisms underlying IC effect in the other organisms are still elusive. To understand how a CO change on just one chromosome triggers the global response of the meiocyte to obtain the adequate CO number/cell remains a fascinating question in sexually reproducing species.