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

Christina A. Cuomo, Guus Bakkeren, Hala Badr Khalil, Vinay Panwar, David Joly, Rob Linning, Sharadha Sakthikumar, Xiao Song, Xian Adiconis, Lin Fan, Jonathan M. Goldberg, Joshua Z. Levin, Sarah Young, Qiandong Zeng, Yehoshua Anikster, Myron Bruce, Meinan Wang, Chuntao Yin, Brent McCallum, Les J. SzaboScot Hulbert, Xianming Chen, John P. Fellers

Research output: Contribution to journalArticlepeer-review

52 Scopus citations

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.

Original languageEnglish (US)
Pages (from-to)361-376
Number of pages16
JournalG3: Genes, Genomes, Genetics
Volume7
Issue number2
DOIs
StatePublished - 2017

Bibliographical note

Funding Information:
We thank the Broad Genomics Platform for generating DNA and RNA sequences and the Michael Smith Genome Sciences Centre in Vancouver for sequencing the BAC ends. C.A.C thanks G. Cerqueira for sharing the syntenia code. G.B. thanks M. Coelho for helpful discussions and acknowledges funding from the Canadian Genomics Research and Development Initiative. This project was supported by the United States Department of Agriculture (USDA) Cooperative State Research, Education, and Extension Service (awards 2008-35600-04693 and 2009-65109-05916). Mention of a trademark of a proprietary product does not constitute a guarantee of warranty of the product by the USDA, and does not imply its approval to the exclusion of other products that may also be sui. USDA is an equal opportunity provider and employer.

Publisher Copyright:
© 2017 Cuomo et al.

Keywords

  • Effectors
  • Genome comparisons
  • Mating-type genes
  • Puccinia
  • Sexual stage

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