R-evolution · Why two and not one? Evolutionary consequences of maintaining individual genome copies in two separate nuclei

The effect of ploidy and genome organization on evolution and adaptation is a central question in biology. Most organisms contain a single nucleus per cell, irrespective of their genome size and ploidy level. The kingdom Fungi represents a notable, yet significantly understudied, exception. Most fungal species partition individual haplotype genome copies into discrete nuclei. What evolutionary advantages arise from partitioning different haplotypes into multiple nuclei is a fundamental and unsolved puzzle in eukaryote genomics. This project addresses several questions that will improve our fundamental understanding of multinuclear genome biology by identifying genetic and epigenetic inter-nuclear differences in the stripe rust fungus (Puccinia striiformis f. sp. tritici, Pst). In contrast to diploids, it partitions its two haplotypes into two distinct nuclei (dikaryon). It is one of the most harmful wheat pathogens with significant impacts on global wheat production and food security. Pst epidemics in wheat growing regions including Europe and Australia have been dominated by lineages that reproduced exclusively asexually for decades. The haplotypes of the asexually evolving lineages diverge over time through independent accumulation of genetic variation. In this proposal I will dissect how the presence of multiple nuclei in the same cytoplasm in rust fungi contributes to rapid adaptation to variable and changing agricultural environments. Understanding the underlying mechanisms that drive rapid evolution of new genotypes in absence of sexual recombination is important to make predictions about durability of host resistance and management strategies.