Wheat rust fungi are switching off the production of certain proteins to evade plant immune detection, and researchers want to know how. These rusts secrete effector proteins into wheat cells to suppress defences, but some wheat varieties carry resistance proteins that recognise specific effectors and trigger immunity. The problem is that pathogens evolve rapidly to avoid recognition, often by deleting or mutating the genes for those effectors. This project focuses on a less understood strategy: epigenetic switching, where a fungus stops making an effector without altering its DNA sequence. The team will study the yellow rust pathogen *Puccinia striiformis* and a recently identified effector whose loss of expression has enabled a new virulent strain to spread across Europe. They will examine three epigenetic mechanisms—DNA methylation, RNA silencing, and histone modifications—and test whether environmental stressors such as climate change accelerate these switches. If successful, this work could transform how researchers discover new effectors in rust fungi, leading to more durable resistance strategies in wheat. This is fundamental science: it addresses a basic gap in understanding how obligate biotrophic pathogens evolve, with no immediate practical application but clear long-term relevance to global food security.
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A central question in plant pathology is how pathogens are recognised by their hosts and how the subsequent activation of immunity may be evaded by pathogens to promote disease. Wheat rusts severely damage cereal production worldwide. During infection, rust fungi secrete effector proteins into wheat plants to reprogramme host plant circuitry, supporting their own growth and development. Yet, certain wheat plants contain resistance (R) proteins that can recognise a subset of these effector proteins (termed Avr factors) as signatures of invasion and activate defence responses to halt pathogen progression. However, host recognition creates a strong evolutionary pressure on Avr effectors, favouring their modification to evade immunity. This leads to frequent emergence of new virulent pathogen races, compromising R-gene mediated resistance and limiting the longevity of deployed R genes. To understand how these devastating pathogens evolve to evade R-gene mediated resistance requires the identity of these Avr proteins to be determined. To date, only three Avr proteins have been identified for the wheat rust fungi and all through comparative genomic studies considering loss of Avr function through sequence modification and/or deletion. However, one potential, understudied strategy to evade recognition is to prevent the synthesis of Avr proteins - through a process regulated by epigenetic switching. The critical contribution of epigenetics in virulence gains for human pathogens is well established. While our understanding of epigenetic regulation in evolution of loss of host recognition for fungal plant pathogens remains in its infancy. The aim of this proposal is to determine the contribution of epigenetic switching of Avr factors in the evolution of new wheat rust strains and how this process could be augmented by climate change. We will focus on the wheat yellow rust pathogen (Puccinia striiformis f. sp. tritici (Pst)) and a recently identified Pst effector (PST_425), where loss of expression in a subset of Pst isolates is linked to a recent virulence gain in Europe. We will consider the contribution of the three prevalent epigenetic mechanisms of regulation in fungi that could be influencing gain of Pst virulence: DNA methylation, RNA silencing and histone modifications. We will also consider how the rates of epigenetic switching and virulence gains could be augmented by environmental stressors such as climate change. This project is particularly timely as it builds on emerging research for genetically tractable fungal plant pathogens such as Magnaporthe oryzae that has demonstrated the considerable importance of epigenetics in the regulation of fungal development and pathogenesis. In addition, as the first comprehensive study considering epigenetic switching of Avr effectors for an obligate biotroph (Pst), the results will be of exceptional value for researchers studying similar complex systems. Furthermore, establishing the role of epigenetic switching in the gain of Pst virulence may act as a catalyst to accelerate future Avr discovery for the wheat rusts by founding the methodology and knowledge to integrate epigenetic switching into the Avr discovery pipeline. Ultimately leading to the development of better-informed resistance strategies, whilst potentially revealing target points that could be used to combat fungal pathogenesis.
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