Abstract
Stripe rust of wheat, caused by the obligate biotrophic fungus Puccinia striiformis f.sp. tritici, is a major threat to wheat production worldwide with an estimated yearly loss of US $1 billion. The recent advances in long-read sequencing technologies and tailored-assembly algorithms enabled 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 P. striiformis f.sp. tritici isolates with contrasting life histories. We compare one isolate of the old European lineage (PstS0), which has been asexual for over 50 years, and a Warrior isolate (PstS7 lineage) from a novel incursion into Europe in 2011 from a sexual population 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, candidate effectors are not compartmentalized and do not exhibit reduced levels of synteny. Yet we were able to identify two subsets of candidate effector populations. About 70% of candidate effectors are invariant between the two isolates, whereas 30% are hypervariable. The latter might be involved in host adaptation on wheat and explain the different phenotypes of the two isolates. Overall, this detailed comparative analysis of two haplotype-aware assemblies of P. striiformis f.sp. tritici is the first step in understanding the evolution of dikaryotic rust fungi at a whole-genome level.
Highlights
Fungi have complex life cycles involving clonal as well as sexual reproduction
We investigated levels of homo- and heterozygosity directly from short-read sequencing data for several additional P. striiformis f.sp. tritici isolates linked to recent incursions from the Himalayan region plus appropriate controls (Hubbard et al 2015; Bueno-Sancho et al 2017; Schwessinger et al 2018; Xia et al 2018; Li, Xia, et al 2019)
FIG. 6.—Candidate effectors are mostly syntenic between the two Puccinia striiformis f.sp. tritici isolates. (A) Shows the percentage of genes that are syntenic at increasing number of allowed gaps within the synteny block. (B) Shows the mean synteny block length at increasing number of allowed gaps within the synteny block
Summary
Fungi have complex life cycles involving clonal as well as sexual reproduction. Sexual reproduction creates genotypic diversity and enables adaptation to new environments by combining beneficial alleles and eliminating harmful genetic traits (Heitman 2015; Seudre et al 2018). Studies of the genomic architecture of fungal pathogens with different reproduction strategies can help us to understand the genetic and genomic processes behind pathogen adaptation. This knowledge is important for predicting the response of pathogens to challenges such as climate change, drugs, fungicides, host resistance, or immunity, and will strengthen the development of methods for combating fungal pathogens (Gladieux et al 2014)
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