Genome biology and evolution of mating type loci in four cereal rust fungi

Abstract

Sex defining loci or chromosomes often contain large non-recombining regions. In Basidiomycota, two distinct gene loci confer mate compatibility. These loci encode for homeodomain (HD) transcription factors and pheromone receptor (PR)-ligand pairs. In some fungi these two loci are physically linked and give rise to large evolutionary strata with extensive recombination suppression. To date genome level mating type (MAT) loci analysis is lacking for obligate biotrophic basidiomycetes that depend on their host plants for survival, this includes the orderPucciniales. These economically important plant pathogens have long-term dikaryotic life-stages in which matched haploid nuclei must carry compatibleMATloci.Here we focus on fourPucciniacereal rust species, includingPuccinia graminisf.sptritici,P. striiformisf.sptritici,P. triticinaandP. coronataf.spavenae, which infect major cereals including wheat and oat. We identifiedMATlocations on two separate chromosomes that supports previous hypotheses of a tetrapolar mating system in thePucciniales.HDloci displayed largely conserved macrosynteny among species and were not suppressed for recombination. Consistently,HDtranscription factor genes showed no trans-specific polymorphisms between species. Regions, surrounding thePRloci however, displayed extensive genomic degeneration, signs of recombination suppression and were found to be linked to centromeres in some species. Expression analysis suggests that bothMATloci are involved in nuclear pairing during spore formation in the asexual cycle. Together, our study provides insights into the evolution ofMATloci since speciation of key pathogenicPucciniaspecies. This detailed understanding is important to predict the possible combinations of nuclear pairs that can arise via sexual reproduction, somatic recombination, or di-om mating to enable the evolution of newly virulent isolates of these agriculturally important plant pathogens.

A high-resolution haplotype pangenome uncovers somatic hybridization, recombination and intercontinental migration in oat crown rust

“…Pca HD locus alleles published by Luo et al (2024). There is one discrepancy between the bW5 allele between the studies in which the first 12 N-terminal amino acids of bW5 defined by Luo et al (2024) are not encoded in the haplotypes used to define bW5 in this study.…”

“…There is one discrepancy between the bW5 allele between the studies in which the first 12 N-terminal amino acids of bW5 defined by Luo et al (2024) are not encoded in the haplotypes used to define bW5 in this study. In addition, the ‘ bW8bE8 ’ allele pair reported by Luo et al (2024) was only found in a single isolate (90MN5B) that was not included in our pangenome.…”

Mating-compatibility genes employed as diagnostic markers to identify novel incursions of the myrtle rust pathogenAustropuccinia psidii

“…In rust fungi, these are two unlinked loci, one contains pheromone precursors and receptors ( P/R ) and the other contains homeodomain ( HD ) transcription factors that closely linked via a short DNA sequence. The HD locus encodes bW-HD1 and bE-HD2 genes which are highly multiallelic in rust fungi (Luo et al 2024) and many Basidiomycota (Coelho et al 2017). These transcription factors form heterodimeric complexes between alleles and regulate cellular development during mating and the fungal life cycle (Coelho et al 2017; Cuomo et al 2017; Holden et al 2023; Wilson et al 2015).…”

Uncovering the history of recombination and population structure in western Canadian stripe rust populations through mating-type alleles

“…In other cases, the alleles no longer discriminate against self-fertilization or are not required for mating, leading to a bipolar or even unipolar mating-type [10]. So far, all characterized rust fungi are tetrapolar [18], although very little is known about the majority of rusts' mating-type loci.…”

“…Analysis of the published genome assemblies of P. striiformis f. sp. tritici identifies two alleles of each Pst-bW-HD1 and Pst-bE-HD2 in each genome on chromosome 4, although these are not always present in the published assembly, and five distinct alleles of each Pst-bW-HD1 and Pst-bE-HD2 in total, with the P/R locus being on chromosome 9 [18]. It has been hypothesized that maintenance of a plurality of mating-types is evolutionarily unfavourable without selection pressure to maintain outcrossing in sexual reproduction [10,24,25].…”