Wheat is a major global food crop, accounting for 18% of total dietary calories consumed across the world. We are particularly big fans of wheat in the UK, with 14.4 million tonnes grown in England in 2022 across 13% of the total land area. One of the greatest threats to wheat production in Europe is the devastating disease Septoria tritici blotch, caused by the fungal pathogen Zymoseptoria tritici, which leads to grain yield losses of up to 50% in the worst epidemics. Farmers attempt to control the disease by planting disease resistant wheat varieties and applying fungicides, costing €1 billion annually. But evolution of resistance to these control strategies in Z. tritici mean that yield losses remain high.
Z. tritici has an intriguing infection cycle composed of two distinct phases. After Z. tritici spores land on the wheat leaf, they germinate and grow as long filaments (known as hyphae) across the surface. The hyphae then penetrate the leaf tissue through the stomata and grow between the cells without causing disease symptoms. Overall, this symptomless phase usually lasts ~1-2 weeks, during which the fungus supresses the wheat immune system and evades detection by concealing molecular signatures of its cell wall using proteins called LysM proteins. This infection strategy has been called ‘stealth pathogenesis’. After the symptomless phase, Z. tritici starts to kill the wheat leaf cells, secreting proteins which induce host cell death and degrade the host tissue. This is termed the necrotrophic phase. The molecular mechanisms controlling the transition between these phases are not fully understood, including what initiates fungal suppression of host immunity in the symptomless phase and what induces the switch to necrotrophic growth.
In a recent study, researchers at the University of Exeter and Rothamsted Research investigated the role of two cell signalling pathways in controlling the progression of Z. tritici infection. They isolated strains which could not cause symptoms on wheat and identified mutations in two genes, ZtBCK1 and ZtCYR1, required for the cell wall integrity (CWI) and the cyclic AMP signalling pathways, respectively. They then deleted these two genes and investigated the impact on gene expression during infection, by carrying out RNA sequencing on wheat leaves infected with these strains.
This analysis identified contrasting sets of genes regulated by the two pathways, including those encoding secreted proteins produced by the fungus to manipulate the host, known as effectors. Inhibiting CWI signalling led to widespread suppression of effectors during the early symptomless phase of infection, including LysM proteins which are known to be essential for Z. tritici virulence through host immune suppression. This is consistent with the observation that this mutant couldn’t invade far beyond the stomata and that it causes upregulation of wheat immune defence genes, early in infection. Contrastingly, the cAMP signalling mutant was able to invade the leaf tissue but didn’t cause host cell death. This was associated with changes in expression of a distinct group of effectors and genes involved in nutrient acquisition, which could be required for inducing host cell death and utilising nutrition from dying host cells.
Overall, these results indicate that the CWI pathway is crucial for Z. tritici to adapt to the host environment and establish the symptomless infection phase, while cAMP signalling is required for triggering the switch to aggressive necrotrophic growth. These findings increase our understanding of the molecular processes that control Z. tritici infection, which is vital for developing improved control strategies in the fight against this destructive cereal killer.
Harry T. Child, Michael J. Deeks, Jason J. Rudd and Steven Bates published this study in Molecular Plant Pathology:
Comparison of the impact of two key fungal signalling pathways on Zymoseptoria tritici infection reveals divergent contribution to invasive growth through distinct regulation of infection‐associated genes.
TITLE IMAGE: Disease symptoms on wheat leaves after 21 days post inoculation by Δztcyr1 and Δztbck1 mutant strains compared to the wild-type (IPO323) and uninfected (Mock) controls. All images used with permission of the author.