Abstract
Pathogenic fungi must extend filamentous hyphae across solid surfaces to cause diseases of plants. However, the full inventory of genes which support this is incomplete and many may be currently concealed due to their essentiality for the hyphal growth form. During a random T-DNA mutagenesis screen performed on the pleomorphic wheat (Triticum aestivum) pathogen Zymoseptoria tritici, we acquired a mutant unable to extend hyphae specifically when on solid surfaces. In contrast “yeast-like” growth, and all other growth forms, were unaffected. The inability to extend surface hyphae resulted in a complete loss of virulence on plants. The affected gene encoded a predicted type 2 glycosyltransferase (ZtGT2). Analysis of >800 genomes from taxonomically diverse fungi highlighted a generally widespread, but discontinuous, distribution of ZtGT2 orthologues, and a complete absence of any similar proteins in non-filamentous ascomycete yeasts. Deletion mutants of the ZtGT2 orthologue in the taxonomically un-related fungus Fusarium graminearum were also severely impaired in hyphal growth and non-pathogenic on wheat ears. ZtGT2 expression increased during filamentous growth and electron microscopy on deletion mutants (ΔZtGT2) suggested the protein functions to maintain the outermost surface of the fungal cell wall. Despite this, adhesion to leaf surfaces was unaffected in ΔZtGT2 mutants and global RNAseq-based gene expression profiling highlighted that surface-sensing and protein secretion was also largely unaffected. However, ΔZtGT2 mutants constitutively overexpressed several transmembrane and secreted proteins, including an important LysM-domain chitin-binding virulence effector, Zt3LysM. ZtGT2 likely functions in the synthesis of a currently unknown, potentially minor but widespread, extracellular or outer cell wall polysaccharide which plays a key role in facilitating many interactions between plants and fungi by enabling hyphal growth on solid matrices.
Highlights
Micro-organisms have evolved many different mechanisms to enable them to cause diseases of plants
Z. tritici GT2 (ZtGT2) orthologues are present in most ascomycete filamentous fungi, and we show that the orthologous gene from the distantly related wheat ear infecting fungus, Fusarium graminearum, is required for hyphal growth and virulence
The pleomorphic growth characteristics of Zymoseptoria tritci enabled the identification of the specific growth state in which ZtGT2 plays a crucial role, that being hyphal growth when in physical contact with solid matrices
Summary
Micro-organisms have evolved many different mechanisms to enable them to cause diseases of plants. All known fungi infecting the aerial tissues of plants (flowers, leaves, stems) are referred to as “filamentous”, meaning that they arrive on plant surfaces as either air- or waterborne spores, they subsequently transition into filamentous hyphae to grow over or through tissues and cells [4]. This discriminates filamentous fungi from the model ascomycete yeast species Saccharomyces cerevisiae and Schizosaccharomyces pombe and their close relatives, which are free living and do not form true hyphae. Hyphal growth over solid surfaces is a pre-requisite step for potentially all fungal diseases of plants
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