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Dec 18
Research Highlight: Evolution of the ToxB gene in Pyrenophora tritici-repentis and related species
​Reem Aboukhaddour, Cereal Pathology Lab, Agriculture and Agri-Food Canada, Lethbridge, AB, Canada​

Overall Background

Across the expansive Canadian prairies, wheat can stretch as far as the eye can see, and during the growing season, its green leaves are a food source to several foliar-infecting pathogens. Among these pathogens is the fungus Pyrenophora tritici-repentis, which causes tan spot of wheat, a destructive foliar disease that emerged as a specialized necrotroph about 50 years ago. Since its emergence as a wheat pathogen, it has caused significant losses in North America, Australia, and other parts of the world. Today, tan spot is still one of the most destructive foliar diseases of wheat, and it is mainly managed by fungicides applications.

Why This Work and How It Came to Be

The question of how this fungus became a pathogen has been a pivotal inquiry among the research community, including my team, and aligns well with the ongoing exploration of the emergence of necrotrophic diseases. Since 2016, my lab has concentrated on wheat diseases, resulting in this paper as part of our overall studies. I have actively engaged with inquiries from students and scientists globally, providing guidance on accurately identifying the tan spot fungus and troubleshooting various aspects of working with the system. Some interactions were driven by my interest in tracing the pathogen's identification as a wheat pathogen in Japan in 1928, seeking old isolates, well characterized at the University of Manitoba and collected by my late Ph.D. supervisor, Dr. Lamari, who dedicated his research to establishing the tan spot-wheat interaction as a model system. These isolates, collected along the silk road, hold significant value for comparative genomic studies to trace the pathogen's evolution. Chance encounters with collaborators at conferences and meetings have further contributed to the establishment of a collaborative network spanning North and South America, North Africa, Europe, Japan, and Australia.

What began as a simple quest to single-spore the pathogen and conduct its proper characterization, though laborious and time-consuming, resulted in a substantial collection of isolates from diverse global locations and hosts and covering an interesting time scale. The increasing affordability of full genome sequencing, coupled with COVID-19 restrictions, prompted a shift in focus. Collaborating with experts, including Dr. Megan McDonald from the University of Birmingham in the United Kingdom, we released the pathogen's pangenome, chromosomal structural organization, and the reorganization of its effector-encoding genes and surrounding regions (Gourlie et al., 2022). Simultaneously, we explored the allelic diversity of effector-encoding genes in a broader collection of wheat leaf-spotting pathogens, with a specific emphasis on the ToxA gene, a key virulence determinant in North America and Australia (Aboukhaddour et al., 2023). Our research extended beyond the tan spot pathogen to encompass related species.

Simultaneously, our investigation of P. tritici-repentis virulence in North Africa (Kamel et al., 2019) revealed a prevalent ToxB effector in the pathogen populations. The ToxB gene, relatively understudied due to limited access in North American and Australian labs, presented an intriguing aspect for exploring virulence evolution in the fungal genome given its multicopy nature. Tan spot, increasingly concerning in North Africa and neighboring regions where ToxB is widespread, contrasts with North America, where ToxB is nearly absent; instead, a nonfunctional homolog prevails in certain pathogen races infecting durum wheat or recovered from grasses. A few years ago, we accidentally discovered that ToxB-producing isolates induce mild chlorosis in specific barley genotypes. Identifying a dominant single locus responsible for conferring sensitivity to ToxB-producing isolates in barley, a secondary host for the pathogen, added an interest to explore further the ToxB evolution (Aboukhaddour and Strelkov, 2016; Wei et al, 2020).

Considering these findings, the research highlighted here by Hafez et al. delves into the diversity and evolution of ToxB in tan spot pathogens and related species. This work complements our broader investigation into the evolutionary puzzle of tan spot virulence, shedding light on the sudden emergence of this wheat pathogen. The paper provides the research community with a more comprehensive understanding of the diversity of the ToxB gene and its homologs and access to valuable information from a large global collection that would otherwise be challenging to obtain. Ongoing research, in collaboration with Dr. McDonald, aims to decipher the mechanism of virulence gene duplications in the fungal genome. Armed with a wealth of well-studied isolates and continually expanding resources, this endeavor feels like a generational effort booming into an international collaboration to decode the emergence of this wheat pathogen.

Learn more about Mohamed Hafez in his InterConnections article​​.

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