Research Area: Molecular phytopathology
Smut fungi comprise a large group of biotrophic pathogens which parasitize mostly on grasses including a number of cereal hosts like maize, barley and wheat. They are characterized by a narrow host range, infect plants systemically and usually cause symptoms in male and female inflorescences only. The fungus Ustilago maydis, causing smut disease in maize, is an exception in that symptoms, in this case large tumors, can develop on all above ground parts of the plant. This leads to stunted growth and significant reduction in crop yield. The particular feature of U. maydis to infect all above ground parts of a maize plant, allows to conduct virulence assays in less than two weeks in maize seedlings. Combined with its highly efficient homologous recombination system that can be used to generate deletion mutants and the many molecular tools developed, the U. maydis-maize system has become one of the most attractive models for biotrophic plant pathogenic fungi and for elucidating how such pathogens cause disease.
In all smut fungi pathogenic development is initiated by the filamentous dikaryon that forms infection structures (appressoria) on the leaf surface (Fig.1), which allow direct penetration of the cuticle, presumably aided by lytic enzymes. During penetration the plasma membrane of the host invaginates and surrounds the infection hyphae, shielding the fungus from direct contact with the host cytoplasm. The dikaryon-stage can be bypassed in so-called solopathogenic lines. These are haploid strains that have been engineered to express an active bE/bW homeodomain protein complex and display autocrine pheromone stimulation. Although biotrophic U. maydis hyphae traverse plant cells, there are only limited host defense responses and the infected plant tissue remains alive until late in the infection process, when fungal proliferation occurs mostly in the apoplast. Initial plant defense responses, presumably triggered by fungal PAMPs, are actively suppressed by the pathogen during colonization. This is accomplished by a battery of about 300 secreted effector molecules that either have a function in the tight interaction zone between fungal hyphae and host plasma membrane or are translocated to host cells and modulate endogenous plant processes (Fig. 1).
Fig.1 | Development of U. maydis on the leaf surface and during colonization of the epidermis. The scheme depicts the stage where a filamentous hyphae on the leaf surface has developed an appressorium and the penetrating hyphae has entered the epidermal layer. Fungal cytoplasm is shown in pink. To get to this stage, plant surface signals are perceived and trigger the development of appressoria, the synthesis of plant cell wall degrading enzymes and effectors needed for penetration and establishment of the biotrophic phase. Secreted effectors can remain in the interface between fungal hyphae and plant plasma membrane (apoplastic effectors) or are taken up by plant cells (cytoplasmic effectors). In the latter case, such effectors may be spreading form one cell to the neighboring cells, presumably through plasmodesmata, to prepare the host for invasion by U. maydis.
Most of the secreted effector molecules are novel and lack characteristic motifs that could give hints to their function. Additionally, their expression is tightly coupled to the biotrophic phase. In U. maydis, many of the respective effector genes reside in clusters in the genome and this feature is conserved in most of the related smut fungi. Our work during the period of the report has focused on fungal differentiation after contact with the leaf surface, on genome comparisons between U. maydis and related smut fungi and on how secreted effectors shape the biotrophic interaction.