The Ustilago maydis forkhead transcription factor Fox1 is involved in the regulation of genes required for the attenuation of plant defenses during pathogenic development
The basidiomycete Ustilago maydis is a phytopathogenic fungus that causes common smut disease on maize. U. maydis is a dimorphic fungus that can exist as a non-pathogenic yeast-like haploid cell, or as a filamentous growing pathogenic dikaryon. As a biotrophic fungus, completion of the life cycle...
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|The basidiomycete Ustilago maydis is a phytopathogenic fungus that causes
common smut disease on maize. U. maydis is a dimorphic fungus that can exist as a non-pathogenic yeast-like haploid cell, or as a filamentous growing pathogenic
dikaryon. As a biotrophic fungus, completion of the life cycle depends on living host tissue. The biotrophic interaction is initiated upon breaching of the host epidermal layer, and involves invagination of the host plasma membrane around hyphae to form an interaction zone. This is thought to facilitate nutrient acquisition by the fungus, as well as the translocation of fungal effector proteins into the plant cell. The establishment and maintenance of the biotrophic phase requires an adaptation to a multitude of nutritional/environmental conditions, and the response to host specific
signals and defense reactions. Dynamic processes during the host interaction entail a complex regulatory network including a variety of different transcription factors, which work in concert to coordinate successful pathogenic development. While transcriptional regulators involved in the establishment of an infectious dikaryon and penetration into the host have been characterized, transcriptional regulators exclusively required for the post-penetration stages remained to be identified.
The potential forkhead transcription factor Fox1 has been identified by global
gene expression profiling. Fox1 is specifically expressed in planta and required for biotrophic development. In particular, U. maydis delta-fox1 mutant strains are unable to incite tumor formation, and infected leaf tissue displays increased anthocyanin levels.
Expression analysis of the host response revealed the deregulation of genes required for plant cell growth and enlargement, and the induction of genes associated with the
production of anthocyanins.
Microscopic analyses identified that unlike wild-type-hyphae, which are found
frequently within the plant vasculature and mesophyll, hyphae of delta-fox1 mutants predominantly aggregate within the plant vasculature and are rarely detected in the
mesophyll. The reason behind this focused growth remains to be elucidated, however the delta-fox1-dependent repression of genes involved in sugar transport and processing could have a decisive effect on the ability of the fungus to grow in sugar-sparse plant tissue.
Global gene expression profiling identified Fox1 as a b-independent, plant
specific regulator. fox1-dependent genes comprise those encoding secreted proteins, including potential effectors belonging to gene clusters required for virulence. As a consequence, !fox1-hyphae trigger host defense reactions, including the overproduction and accumulation of H2O2 in and around infected cells, and a novel maize defense response phenotypically represented by the encasement of proliferating hyphae in a plant-produced matrix consisting of cellulose and callose.