Differential Regulation and Production of Secondary Metabolites among Isolates of the Fungal Wheat Pathogen Zymoseptoria tritici

The genome of the wheat-pathogenic fungus Zymoseptoria tritici represents extensive presence-absence variation in gene content. Here, we addressed variation in biosynthetic gene cluster (BGC) content and biochemical profiles among three isolates. We analyzed secondary metabolite properties based on genome, transcriptome, and metabolome data. The isolates represent highly distinct genome architecture but harbor similar repertoires of BGCs. Expression profiles for most BGCs show comparable patterns of regulation among the isolates, suggesting a conserved biochemical infection program. For all three isolates, we observed a strong upregulation of a putative abscisic acid (ABA) gene cluster during biotrophic host colonization, indicating that Z. tritici interferes with host defenses by the biosynthesis of this phytohormone. Further, during in vitro growth, the isolates show similar metabolomes congruent with the predicted BGC content. We assessed if secondary metabolite production is regulated by histone methylation using a mutant impaired in formation of facultative heterochromatin (H3K27me3). In contrast to other ascomycete fungi, chromatin modifications play a less prominent role in regulation of secondary metabolites. In summary, we show that Z. tritici has a conserved program of secondary metabolite production, contrasting with the immense variation in effector expression, and some of these metabolites might play a key role during host colonization. IMPORTANCE Zymoseptoria tritici is one of the most devastating pathogens of wheat. So far the molecular determinants of virulence and their regulation are poorly understood. Previous studies have focused on proteinaceous virulence factors and their extensive diversity. In this study, we focus on secondary metabolites produced by Z. tritici. Using a comparative framework, we characterize core and noncore metabolites produced by Z. tritici by combining genome, transcriptome, and metabolome data sets. Our findings indicate highly conserved biochemical profiles with contrasting genetic and phenotypic diversity of the field isolates investigated here. This discovery has relevance for future crop protection strategies

Advancing Our Functional Understanding of Host–Microbiota Interactions: A Need for New Types of Studies

Multicellular life evolved in the presence of microorganisms and formed complex associations with their microbiota, the sum of all associated archaea, bacteria, fungi, and viruses. These associations greatly affect the health and life history of the host, which led to a new understanding of “self” and establishment of the “metaorganism” concept.1 The Collaborative Research Centre (CRC) 1182 aims at elucidating the evolution and function of metaorganisms. Its annual conference, the Young Investigator Research Day (YIRD), serves as a platform for scientists of various disciplines to share novel findings on host–microbiota interactions, thereby providing a comprehensive overview of recent developments and new directions in metaorganism research. Even though we have gained tremendous insights into the composition and dynamics of host‐associated microbial communities and their correlations with host health and disease, it also became evident that moving from correlative toward functional studies is needed to examine the underlying mechanisms of interactions within the metaorganism. Non‐classical model organisms in particular possess significant potential to functionally address many open questions in metaorganism research. Here, we suggest and introduce a roadmap moving from correlation toward a functional understanding of host–microbiota interactions and highlight its potential in emerging ecological, agricultural, and translational medical applications

Microbial interactions within the plant holobiont

Abstract Since the colonization of land by ancestral plant lineages 450 million years ago, plants and their associated microbes have been interacting with each other, forming an assemblage of species that is often referred to as a “holobiont.” Selective pressure acting on holobiont components has likely shaped plant-associated microbial communities and selected for host-adapted microorganisms that impact plant fitness. However, the high microbial densities detected on plant tissues, together with the fast generation time of microbes and their more ancient origin compared to their host, suggest that microbe-microbe interactions are also important selective forces sculpting complex microbial assemblages in the phyllosphere, rhizosphere, and plant endosphere compartments. Reductionist approaches conducted under laboratory conditions have been critical to decipher the strategies used by specific microbes to cooperate and compete within or outside plant tissues. Nonetheless, our understanding of these microbial interactions in shaping more complex plant-associated microbial communities, along with their relevance for host health in a more natural context, remains sparse. Using examples obtained from reductionist and community-level approaches, we discuss the fundamental role of microbe-microbe interactions (prokaryotes and micro-eukaryotes) for microbial community structure and plant health. We provide a conceptual framework illustrating that interactions among microbiota members are critical for the establishment and the maintenance of host-microbial homeostasis