Search

In allopolyploids, correct chromosome segregation requires suppression of non-homologous crossovers while levels of homologous crossovers are ensured. To date, no mechanism able to specifically inhibit non-homologous crossovers has been described in allopolyploids other than in bread wheat. Here, we show that reducing the number of functional copies of MSH4, an essential gene for the main crossover pathway, prevents non-homologous crossovers in allotetraploid Brassica napus. We show that non-homologous crossovers originate almost exclusively from the MSH4-dependent recombination pathway and that their numbers decrease when MSH4 returns to single copy in B. napus; by contrast, homologous crossovers remain unaffected by MSH4 duplicate loss. We also demonstrate that MSH4 systematically returns to single copy following numerous independent polyploidy events, a pattern that is probably not by chance. These results suggest that stabilization of allopolyploid meiosis can be enhanced by loss of a key meiotic recombination gene.

Meiosis is the cell division that reshuffles genetic information between generations. Recently, much progress has been made in understanding this process; in particular, the identification and functional analysis of more than 80 plant genes involved in meiosis have dramatically deepened our knowledge of this peculiar cell division. In this review, we provide an overview of advancements in the understanding of all aspects of plant meiosis, including recombination, chromosome synapsis, cell cycle control, chromosome distribution, and the challenge of polyploidy.

Polyploidy can result in both evolutionary dead-ends and successful evolutionary transitions. A pair of recent papers indicates that adapting meiosis is a necessary step on the way to becoming a successful polyploid., (Copyright © 2013 Elsevier Ltd. All rights reserved.)

Precise chromosome segregation is vital for polyploid speciation. Here, we highlight recent findings that revitalize the old question of the genetic control of diploid-like meiosis behaviour in polyploid species. We first review new information on the genetic control of autopolyploid and allopolyploid cytological diploidization, notably in wheat and Brassica. These major advances provide new opportunities for speculating about the adaptation of meiosis during polyploid evolution. Some of these advances are discussed, and it is suggested that research on polyploidy and on meiosis should no longer be unlinked.

Although the genetic regulation of recombination in allopolyploid species plays a pivotal role in evolution and plant breeding, it has received little recent attention, except in wheat (Triticum aestivum). PrBn is the main locus that determines the number of nonhomologous associations during meiosis of microspore cultured Brassica napus haploids (AC; 19 chromosomes). In this study, we examined the role played by PrBn in recombination. We generated two haploid x euploid populations using two B. napus haploids with differing PrBn (and interacting genes) activity. We analyzed molecular marker transmission in these two populations to compare genetic changes, which have arisen during meiosis. We found that cross-over number in these two genotypes was significantly different but that cross-overs between nonhomologous chromosomes showed roughly the same distribution pattern. We then examined genetic recombination along a pair of A chromosomes during meiosis of B. rapa x B. napus AAC and AACC hybrids that were produced with the same two B. napus genotypes. We observed significant genotypic variation in cross-over rates between the two AAC hybrids but no difference between the two AACC hybrids. Overall, our results show that PrBn changes the rate of recombination between nonhomologous chromosomes during meiosis of B. napus haploids and also affects homologous recombination with an effect that depends on plant karyotype.

Chromosomal rearrangements can be triggered by recombination between distinct but related regions. Brassica napus (AACC; 2n = 38) is a recent allopolyploid species whose progenitor genomes are widely replicated. In this article, we analyze the extent to which chromosomal rearrangements originate from homeologous recombination during meiosis of haploid B. napus (n = 19) by genotyping progenies of haploid x euploid B. napus with molecular markers. Our study focuses on three pairs of homeologous regions selected for their differing levels of divergence (N1/N11, N3/N13, and N9/N18). We show that a high number of chromosomal rearrangements occur during meiosis of B. napus haploid and are transmitted by first division restitution (FDR)-like unreduced gametes to their progeny; half of the progeny of Darmor-bzh haploids display duplications and/or losses in the chromosomal regions being studied. We demonstrate that half of these rearrangements are due to recombination between regions of primary homeology, which represents a 10- to 100-fold increase compared to the frequency of homeologous recombination measured in euploid lines. Some of the other rearrangements certainly result from recombination between paralogous regions because we observed an average of one to two autosyndetic A-A and/or C-C bivalents at metaphase I of the B. napus haploid. These results are discussed in the context of genome evolution of B. napus.

Understanding meiotic crossover (CO) variation in crops like bread wheat (Triticum aestivum L.) is necessary as COs are essential to create new, original and powerful combinations of genes for traits of agronomical interest. We cytogenetically characterized a set of wheat aneuploid lines missing part or all of chromosome 3B to identify the most influential regions for chiasma formation located on this chromosome. We showed that deletion of the short arm did not change the total number of chiasmata genome-wide, whereas this latter was reduced by ~35% while deleting the long arm. Contrary to what was hypothesized in a previous study, deletion of the long arm does not disturb the initiation of the synaptonemal complex (SC) in early meiotic stages. However, progression of the SC is abnormal, and we never observed its completion when the long arm is deleted. By studying six different deletion lines (missing different parts of the long arm), we revealed that at least two genes located in both the proximal (C-3BL2-0.22) and distal (3BL7-0.63-1.00) deletion bins are involved in the control of chiasmata, each deletion reducing the number of chiasmata by ~15%. We combined sequence analyses of deletion bins with RNA-Seq data derived from meiotic tissues and identified a set of genes for which at least the homoeologous copy on chromosome 3B is expressed and which are involved in DNA processing. Among these genes, eight (CAP-E1/E2, DUO1, MLH1, MPK4, MUS81, RTEL1, SYN4, ZIP4) are known to be involved in the recombination pathway. [ABSTRACT FROM AUTHOR]

Then, as meiosis progresses, AtASY1 is removed from the meiotic chromosome axes, preventing the maturation of additional recombination intermediates into crossovers. Cuacos et al. (2021) notably confirmed that residual crossovers were proportionally enriched in terminal regions, as if 'ASY1 was antagonizing telomere-led recombination and promoted spaced crossover formation along the chromosomes via interference' (Lambing et al., 2020a). This partial loading of ASY1 could possibly explain why the meiotic phenotype of pch2 mutants is less pronounced than that of asy1 mutants, in which there is no ASY1 protein left to activate DMC1 and enforce interhomologue bias. [Extracted from the article]

Allopolyploid species contain more than two sets of related chromosomes (homoeologs) that must be sorted during meiosis to ensure fertility. As polyploid species usually have multiple origins, one intriguing, yet largely underexplored, question is whether different mechanisms suppressing crossovers between homoeologs may coexist within the same polyphyletic species. We addressed this question using Brassica napus , a young polyphyletic allopolyploid species. We first analyzed the meiotic behavior of 363 allohaploids produced from 29 accessions, which represent a large part of B. napus genetic diversity. Two main clear-cut meiotic phenotypes were observed, encompassing a twofold difference in the number of univalents at metaphase I. We then sequenced two chloroplast intergenic regions to gain insight into the maternal origins of the same 29 accessions; only two plastid haplotypes were found, and these correlated with the dichotomy of meiotic phenotypes. Finally, we analyzed genetic diversity at the PrBn locus, which was shown to determine meiotic behavior in a segregating population of B. napus allohaploids. We observed that segregation of two alleles at PrBn could adequately explain a large part of the variation in meiotic behavior found among B. napus allohaploids. Overall, our results suggest that repeated polyploidy resulted in different levels of crossover suppression between homoeologs in B. napus allohaploids. [ABSTRACT FROM AUTHOR]