A fungal pathogen induces systemic susceptibility and systemic shifts in wheat metabolome and microbiome composition

Heike Seybold,Andre Franke,Eva H Stukenbrock,Janine Haueisen,M Amine Hassani,Luisa Lübbers,Ekaterina Reim,Karin Schwarz,Malte Rühlemann,Tobias J Demetrowitsch,Silke Szymczak

doi:10.1038/s41467-020-15633-x

Abstract

Yield losses caused by fungal pathogens represent a major threat to global food production. One of the most devastating fungal wheat pathogens is Zymoseptoria tritici. Despite the importance of this fungus, the underlying mechanisms of plant–pathogen interactions are poorly understood. Here we present a conceptual framework based on coinfection assays, comparative metabolomics, and microbiome profiling to study the interaction of Z. tritici in susceptible and resistant wheat. We demonstrate that Z. tritici suppresses the production of immune-related metabolites in a susceptible cultivar. Remarkably, this fungus-induced immune suppression spreads within the leaf and even to other leaves, a phenomenon that we term “systemic induced susceptibility”. Using a comparative metabolomics approach, we identify defense-related biosynthetic pathways that are suppressed and induced in susceptible and resistant cultivars, respectively. We show that these fungus-induced changes correlate with changes in the wheat leaf microbiome. Our findings suggest that immune suppression by this hemibiotrophic pathogen impacts specialized plant metabolism, alters its associated microbial communities, and renders wheat vulnerable to further infections.

Highlights

Yield losses caused by fungal pathogens represent a major threat to global food production
In order to understand the underlying traits that define compatible versus incompatible interactions between different cultivars of wheat and the fungal pathogen Z. tritici, we conducted infection experiments with the susceptible wheat cultivar Obelisk and the resistant cultivar Chinese Spring[20]
We have shown increased growth of nonadapted P. syringae bacteria in the wheat cultivar Obelisk during infection with the fungal pathogen Z. tritici (Fig. 2a–d)

Summary

Introduction

Yield losses caused by fungal pathogens represent a major threat to global food production. We demonstrate that Z. tritici suppresses the production of immune-related metabolites in a susceptible cultivar. Using a comparative metabolomics approach, we identify defense-related biosynthetic pathways that are suppressed and induced in susceptible and resistant cultivars, respectively. We show that these fungus-induced changes correlate with changes in the wheat leaf microbiome. Zymoseptoria tritici is a global hemibiotrophic plant pathogen that infects wheat, causing up to 50% yield loss[10]. We first addressed whether biotrophic fungal colonization of wheat involves active suppression of immune responses or if the pathogen only avoids host recognition. If the fungus actively suppresses immune responses in susceptible wheat cultivars, this could influence the ability of other nonadapted microorganisms to colonize the plant. We analyzed the bacterial microbiome to generalize the observations made during the coinfections

Methods

Results

Conclusion