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

Citation

Cuomo, C.A., Bakkeren, G., Khalil, H.B., Panwar, V., Joly, D., Linning, R., Sakthikumar, S., Song, X., Adiconis, X., Fan, L., Goldberg, J.M., Levin, J.Z., Young, S., Zeng, Q., Anikster, Y., Bruce, M., Wang, M., Yin, C., McCallum, B., Szabo, L.J., Hulbert, S., Chen, X., Fellers, J.P. (2017). Comparative analysis highlights variable genome content of wheat rusts and divergence of the mating loci. G3: Genes, Genomes, Genetics, [online] 7(2), 361-376. http://dx.doi.org/10.1534/g3.116.032797

Plain language summary

Three members of the Puccinia genus, P. 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: brown or leaf rust, yellow or stripe rust, and black or stem rust, respectively. While similar in biology and life cycle, each species is uniquely adapted and specialized. The genomes of Pt and Pst were sequenced and compared through computer analyses to that of Pgt to identify common and distinguishing gene content. We showed that the genomes are very variable with many repetitive and transposable elements that could account for their high intrinsic mutation rates that could be the cause of their frequent defeating new wheat resistance genes. We identified in Pt 1,358 predicted effectors (small proteins that the pathogen secretes to overcome host defenses), of which 784 are expressed across diverse life cycle stages including the sexual stage. Understanding how these manipulate the host defense response may lead to novel ways to combat this disease. We also found specific genes that are likely responsible for sexual mating but also seem to play a role in the infection process. These can also be targets for novel approaches to combat wheat rusts.

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.