Population-wide single-pollen nuclei genotyping in rye sheds light on the genetic basis and environmental plasticity of meiotic recombination

Abstract

The core molecular machinery of meiosis is conserved deep across eukaryotic lineages. Nevertheless, recombination landscapes vary at multiple scales, from chromosomes to populations, caused by an interaction between genetic and environmental factors. To improve our understanding of the causes and consequences of this variation, we need to identify the underlying genetic architecture. In this work, we explored the genetic basis and environmental plasticity of meiotic recombination in a large rye population grown under control and nutrient-deficient conditions. We used single-pollen nuclei (SPN) genotyping to directly measure male meiotic crossovers in 3136 pollen nuclei from 584 individuals. We detected a significant reduction of crossovers in response to nutrient deficiency. Using genome-wide association scans, we uncovered the genetic basis of crossover count, crossover interference, and intrachromosomal shuffling. The presence of multiple additive loci with small to intermediate explained phenotypic variance suggested a polygenic architecture of crossover traits. Loci associated with crossover traits were unique to control or nutrient-deficient conditions, suggesting that alleles regulating crossover traits are dependent on genotype-by-environment interactions, which strongly emphasizes the environmental plasticity of meiotic recombination. Finally, we revealed differences in recombination landscapes measured in gametophytes and sporophytes, which may be explained by a postmeiotic survivorship bias.