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Identification of effectors with avirulence functions in the pathogenic barley smut fungus, using marker-based approaches and comparison among genomes of related species Ali, Shawkat


In plant pathology, the molecular genetic analysis of the interaction between pathogen and host yields knowledge applicable to combat crop disease. During infection, pathogens secrete effector proteins to reprogram the host for its benefit. In special cases, recognition of certain effectors by resistance genes, essential components of the host surveillance system, induces resistance to infection. No effectors with such avirulence function have been described for basidiomycete fungi infecting cereals. Ustilago hordei is a biotrophic basidiomycete fungus that infects barley. One of its effectors functions as an avirulence protein, UhAVR1, rendering it avirulent on barley cultivar Hannchen, having corresponding resistance gene Ruh1. I have located UhAvr1 within the genome using a deletion approach and confirmed its resistance-triggering function. I provide evidence that transposable element (TE) activity in the UhAvr1 promoter region and translocation of the coding region are likely responsible for enabling virulence on Hannchen. This region of the genome harbours a cluster of predicted secreted proteins and is syntenic to a cluster in closely-related corn pathogens, U. maydis and Sporisorium reilianum. In U. maydis, deletion of this region results in dramatic reduction in virulence on corn. This region is under selection pressure in both U. maydis and U. hordei likely to avoid recognition by the host. Evolution of the region in U. maydis seems to involve gene duplication and diversification, while in U. hordei this region is saturated with TEs and repeats which can play a role in genome rearrangements. Computational analysis of the U. hordei genome sequence identified 372 candidate secreted effector proteins (CSEPs), many of which are expected to contribute to virulence and some to trigger resistance in analogy to UhAVR1. Most CSEPs are Ustilago-specific proteins of unknown function and without similarities to sequences in public databases. Evidence for accelerated evolution was observed when comparing CSEPs among smut species. More than half of these CSEPs have four or more cysteine residues in characteristic patterns, possibly involved in disulphide bridge formation and protein folding. The study of effectors with avirulence function can reveal resistance genes which can be used for crop breeding programs to obtain disease-resistant cultivars.

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