Virulent strains of Zymoseptoria tritici suppress the host immune response and facilitate the success of avirulent strains in mixed infections

Abstract

Plants interact with a plethora of pathogenic microorganisms in nature. Pathogen-plant interaction experiments focus mainly on single-strain infections, typically ignoring the complexity of multi-strain infections even though mixed infections are common and critical for the infection outcome. The wheat pathogen Zymoseptoria tritici forms highly diverse fungal populations in which several pathogen strains often colonize the same leaf. Despite the importance of mixed infections, the mechanisms governing interactions between a mixture of pathogen strains within a plant host remain largely unexplored. Here we demonstrate that avirulent pathogen strains benefit from being in mixed infections with virulent strains. We show that virulent strains suppress the wheat immune response, allowing avirulent strains to colonize the apoplast and to reproduce. Our experiments indicate that virulent strains in mixed infections can suppress the plant immune system, probably facilitating the persistence of avirulent pathogen strains in fields planted with resistant host plants.

Estimating the frequency of virulence against anStbgene inZymoseptoria triticipopulations by bulk phenotyping on checkerboard microcanopies of wheat NILs

“…The possibility of infection by ‘stowaway strains’ through facilitation mechanisms, as in the systemic induced susceptibility reaction, has been suggested for Z. tritici (Seybold et al, 2020), consistent with the positive effect of population diversity on symptom intensity sometimes observed (Zelikovitch and Eyal, 1991). Recent reports by Barrett et al (2021) and Bernasconi et al (2023) have confirmed that strains virulent against Stb6 can manipulate the plant immune response in mixed infections, facilitating apoplast colonization by avirulent strains. This mechanism could lead to lesions being caused by avirulent strains on the leaves of the wheat lines carrying the resistance gene, resulting in a ρL ratio slightly higher than the proportion of virulent strains (p) in the inoculum suspension.…”

“…The lower limit for the quantification of virulence proportions depends on the accuracy of spore concentration adjustment; the lowest proportion of virulence strains used here (0.05) appears to be above this limit, but its quantification might have become less reliable below this concentration. Non-proportionality may also result from interactions between strains during infection, as highlighted in studies focusing on mixed infections (Susi et al, 2015; Tollenaere et al, 2016; Bernasconi et al, 2022; 2023). The possibility of infection by ‘stowaway strains’ through facilitation mechanisms, as in the systemic induced susceptibility reaction, has been suggested for Z. tritici (Seybold et al, 2020), consistent with the positive effect of population diversity on symptom intensity sometimes observed (Zelikovitch and Eyal, 1991).…”

A novel genome-wide association approach reveals wheat pathogen genes involved in host specialization

“…Despite the importance of Z. tritici in agroecosystems, the majority of the avirulence genes associated with the 21 major isolate-speci c STB resistance genes remain unknown, though three avirulence genes have been identi ed 5,11,[17][18][19][20][21] . During the asymptomatic phase of its hemibiotrophic lifestyle, Z. tritici suppresses activation of the host immune system 22,23 . A handful of the genetic factors underlying host immune suppression and infection promotion have been described in Z. tritici 21,24,25 .…”