Evolutionary dynamics of genes controlling meiotic recombination in polyploid crop plants – DUPLIC

The DUPLIC project has brought together experts with a complementary range of skills and facilities. Thanks to this, a complete set of integrated analyses was used to explore many inter-related aspects of meiotic gene evolution following polyploidy: i.e. the fate (retention/loss), expression (transcription/silencing), and overlapping function of duplicated meiotic genes. We first carried out a large-scale bio-informatic study to analyse the dynamics of duplicate gene loss in the sequenced genome of 14 paleo- (i.e. ancient) polyploid plants. We next extended our analysis to Triticum aestivum (bread wheat) and Brassica napus (oilseed rape), two species that have undergone very recent WGDs (< 10,000 YA), to determine whether meiotic recombination duplicates (1) return to a single copy after only a few thousand generations, (2) are still expressed, (3) are able to compensate for each other (using mutants) and (4) are genetically variable.

We have shown that the rate at which duplicates are lost decreases through time, a tendency that is also observed genome-wide and may thus prove to be a general trend post-WGD. The sharpest decline is observed for the subset of genes mediating meiotic recombination; however, we found no evidence that the presence of these duplicates is counter-selected and therefore propose that their loss is passive, highlighting how quickly WGDs are resolved in the absence of selective duplicate retention.

Our results can serve to improve functional prediction of uncharacterized meiotic genes in plants; this prediction being based on i) the functionnal characterization of their homologues using a plant model and ii) their phylogenomic evolution. This is a crucial step for translational research, which on the long run can be used to manipulate recombination in crop breeding programmes.

The data obtained within the project have been presented in several national and international conferences and have been submitted for publication. The project has contributed to education and training of graduates and post-docs, an element that we regard as an essential repercussion of our work. Through all these actions, DUPLIC has already contributed to improve the partners’ international renown

Meiotic recombination is a fundamental process for all sexual eukaryotes, which is required to produce balanced gametes and therefore contribute to the fertility and fitness of species. Meiotic recombination is also crucial for plant breeding because it allows, through the crossovers (COs), to reshuffle genetic material between individuals and between species. Huge international efforts have thus been made to identify the genes that are responsible for meiotic recombination in plants, using Arabidopsis thaliana, and to a lesser extent rice and maize, as model systems. However our understanding still remains incomplete, in particular because the effect of polyploidy, which is a hallmark of plant genome evolution, has not been evaluated. We simply don't know the extent to which increased genome complexity in polyploid species (more chromosomes, divergent partners…) is paralleled by an increased complexity in the genetic architecture underpinning crossover recombination (more genes? new networks? others?). Are genes contributing to meiotic recombination randomly distributed between singleton and duplicated genes or conversely are they preferentially retained or preferentially lost after one episode of polyploidy? Are all the copies retained from the progenitor species expressed? Are they still functionally redundant? Or have they diversified following WGD? All these questions are still open and the very limited information available on these issues can not be integrated in a consistent way: while duplications were massively responsible for the early diversification of genes controlling meiotic recombination, each of these early duplicates apparently became duplication-resistant afterwards, being iteratively returned to a singleton status in the paleopolyploid genomes of Arabidopsis and rice. Given the pervasive role played by polyploidy in angiosperm evolution, this apparent incongruity deserves further and specific consideration.
Our project aims to advance understanding on the evolution of genes involved in meiotic recombination following polyploidy events. We will notably try to decipher if preferential elimination of duplicated copies is a general, thus predictable response in polyploid species or conversely if polyploidy may foster genetic innovation in the control of CO formation. Our specific research objectives are to determine: (1) the patterns of duplicated copy retention/loss for 18 recombination genes in two complementary polyploid crop species, oilseed rape (Brassica napus) and bread wheat (Triticum aestivum); (2) for a subset of the most relevant 7-8 genes, if all the retained copies are functional and expressed; (3) for a nested subset of 3-4 genes, if the retained copies are functionally redundant or if they have diversified post-polyploidy, and (4) for the same subset of 7-8 genes, if duplicated meiotic genes show different levels of polymorphism and different rates of molecular evolution.
Because a complete set of integrated analyses will be carried out on two widely divergent and complementary systems (oilseed rape and wheat), our project will provide information with a greater interpretive and predictive power on the fate of duplicated recombination genes in polyploid species. Joint analyses of the same set of meiotic genes should allow the identification of general principles (if any) of meiotic gene evolution, thereby improving our ability to predict this outcome more broadly across plant lineages or to monitor recombination in plant breeding.