Dr Kirsten Bomblies, JIC
Adaptation of meiosis and recombination after whole genome duplication
Whole genome duplication (WGD) results in polyploidy, which has important implications for adaptation, speciation, and agriculture. But doubling the number of homologous chromosomes in a genome poses serious challenges to reliable chromosome segregation in meiosis. Newly formed polyploids often have low fertility attributable to meiotic defects such as multivalent associations among the available homologs, or failures in pairing that result in univalents. These challenges are, however, evolutionarily surmountable - many polyploid species have stable diploid-like chromosome segregation – but the mechanism underlying this has remained mysterious. We hypothesize that meiotic stabilization in polyploids involves crossover reduction and terminalization via an increase in crossover interference. We use Arabidopsis arenosa, an outcrossing relative of A. thaliana with extant natural diploid and autotetraploid populations. The autotetraploid is approximately 20,000 generations old, and has cytologically diploidized meiosis, reduced crossover rates, and increased terminalization of crossovers relative to the diploid – a pattern that follows what is seen in a wide range of polyploids in nature. We are currently building on our prior genome resequencing data that highlighted a clear set of candidate genes: among 18 genes under very strong selection in polyploids are six functionally connected meiosis genes. The products of these genes are known from mutant studies in model systems to be structural proteins that function collaboratively to coordinate chromosome pairing, synapsis, and the number and distribution of crossovers. We show for one gene that the tetraploid allele drives more terminal placement of crossovers, and in other work find that increased crossover interference is likely important not only for reducing crossover numbers, but also by favoring crossover placement patterns in multi-chromosome associations that are minimally dangerous. Our work has led us to favor a model in which stabilization of chromosome segregation in autopolyploids is achieved by modifying core structural proteins active in prophase I, which ultimately leads to a reduction in crossover number, as well as crossover terminalization. We hypothesize that the derived protein variants found in tetraploids together represent a co-evolved polygenic solution to WGD-associated chromosome segregation challenges. This work also provides insights into how crossover rates and placement can be modified by evolution more generally, as all these structures are present and relevant in diploids as well.