Distinct life histories impact dikaryotic genome evolution in the wheat stripe rust fungus Puccinia striiformis f. sp. tritici

Wheat stripe rust, caused by the obligate biotrophic fungus Puccinia striiformis f. sp. tritici (Pst), is a major threat to wheat production world-wide with an yearly loss of ~ US$ 1 billion. Pst undergoes a complex multi-spore life-cycle and infects wheat during its asexual stage mostly via reinfection by dikaryotic urediniospores. The recent advances in long-read sequencing technologies and tailored-assembly algorithms enable us to disentangle the two haploid genomes of Pst. This provides us with haplotype-specific information at a whole-genome level. Exploiting this novel information, we perform whole genome comparative genomics of two Pst isolates with contrasting life histories. We compare one isolate of the old European linage (PstS0), which has been asexual for over 50 years, and a Warrior isolate (PstS7 linage) from a new incursion into Europe in 2011, which is derived from sexual populations in the Himalayan region. This comparison provides evidence that long-term asexual evolution leads to genome expansion, accumulation of transposable elements, and increased heterozygosity at the single nucleotide, structural and allele levels. At the whole genome level, the candidate effectors are not compartmentalized and the whole candidate effector repertoire is conserved at a similarly as all other genes. This detailed comparative analysis of two haplotype-aware assemblies of Pst are the first steps to understand the evolution of dikaryotic rust fungi at a whole genome level.