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

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 postmeiotic selection operating against unbalanced gametes. Cytological analysis of chiasmata in F 1 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.

Coarsening dynamics can explain meiotic crossover patterning in both the presence and absence of the synaptonemal complex

“…The complex interplay between HEI10 mediated cis and trans-interference can also provide a potential mechanistic explanation for other crossover phenomena, such as the interchromosomal effect (Miller, 2020; Termolino et al, 2019). The interchromosomal effect describes the observation that when one pair of homologs experiences a reduction in crossover frequency (due to a structural variation, such as an inversion) this is accompanied by a corresponding increase in crossover frequency on the other, structurally normal, homolog pairs (Miller, 2020; Termolino et al, 2019). In this scenario, RIs may be inhibited from occurring normally at the sites of structural variations, leading to a lower level of HEI10 in those regions.…”

Is partial desynapsis in cauliflower (Brassica oleracea L. var. botrytis) pollen mother cells linked to aneuploidy in the crop?

“…The apparent action of this checkpoint between early and late pachytene suggests that this transition is a target for cell cycle regulatory machinery. Termolino et al (2019) described a comparable phenomenon for a paracentric inversion heterozygote in Arabidopsis where crossover suppression in the rearranged chromosome segment is associated with a significant increase of crossovers in the other chromosomes, thereby maintaining the total number of crossovers per cell unaffected. Such a trans regulation mechanism was found restricted to only male meiosis.…”

The Formation of Bivalents and the Control of Plant Meiotic Recombination

“…It is known that the genomic recombination rate is influenced by epigenetic marks, the genetic background ( Sidhu et al, 2015 ; Ziolkowski et al, 2017 ; Dreissig et al, 2019 ; Lawrence et al, 2019 ), and the level of heterozygosity ( Ziolkowski et al, 2015 ). It also greatly depends on chromatin structural variation where large inversion and translocations can suppress recombination ( Rowan et al, 2019 ; Termolino et al, 2019 ). The molecular basis of this suppression is still unclear but probably involves the abnormal SC installation on unpaired chromatin loop domains.…”