Comparative analysis highlights variable genome content of wheat rusts and divergence of the mating loci

Abstract

Three members of the Puccinia genus, Puccinia triticina (Pt), P. striiformis f.sp. tritici (Pst), and P. graminis f.sp. tritici (Pgt), cause the most common and often most significant foliar diseases of wheat. While similar in biology and life cycle, each species is uniquely adapted and specialized. The genomes of Pt and Pst were sequenced and compared to that of Pgt to identify common and distinguishing gene content, to determine gene variation among wheat rust pathogens, other rust fungi, and basidiomycetes, and to identify genes of significance for infection. Pt had the largest genome of the three, estimated at 135 Mb with expansion due to mobile elements and repeats encompassing 50.9% of contig bases; in comparison, repeats occupy 31.5% for Pst and 36.5% for Pgt. We find all three genomes are highly heterozygous, with Pst [5.97 single nucleotide polymorphisms (SNPs)/kb] nearly twice the level detected in Pt (2.57 SNPs/kb) and that previously reported for Pgt. Of 1358 predicted effectors in Pt, 784 were found expressed across diverse life cycle stages including the sexual stage. Comparison to related fungi highlighted the expansion of gene families involved in transcriptional regulation and nucleotide binding, protein modification, and carbohydrate degradation enzymes. Two allelic homeodomain pairs, HD1 and HD2, were identified in each dikaryotic Puccinia species along with three pheromone receptor (STE3) mating-type genes, two of which are likely representing allelic specificities. The HD proteins were active in a heterologous Ustilago maydis mating assay and host-induced gene silencing (HIGS) of the HD and STE3 alleles reduced wheat host infection.

A novel fungal effector from Puccinia graminis suppressing RNA silencing and plant defense responses

“…No conserved functional domains were found in the PgtSR1 proteins, and no homologues were identified in closely related Puccinia species. This is consistent with the diversity of most characterized RSSs (Csorba et al ., ) and is common for the rapidly evolving effectors in rust fungi (Cuomo et al ., ). PgtSR1 alleles also promoted susceptibility to multiple pathogens, including P. syringae DC3000, INSV and Pgt when expressed in A. thaliana , N. benthamiana and wheat, respectively.…”

Transcriptional profiling reveals no response of fungal pathogens to the durable, quantitative Lr34 disease resistance gene of wheat

“… The transcriptome coverage was calculated based on the estimation of the Blumeria graminis f. sp. hordei transcriptome size of 18 Mb (Cuomo et al ., ). …”

The transcription factor PstSTE12 is required for virulence of Puccinia striiformis f. sp. tritici

“…Subsequently, three pheromone receptor ( STE3 ) mating‐type genes, together with two allelic homeodomain (HD) pairs ( HD1 and HD2 ), were identified in each dikaryotic Puccinia species. The HD proteins were active during mating through heterologous expression in Ustilago maydis , and host‐induced gene silencing (HIGS) of the HD and STE3 genes reduced infection in wheat (Cuomo et al ., ). In this study, we report our findings on the characterized mating‐related gene from Pst , PstSTE12 , which was identified by transcriptome sequencing.…”