Central to our research is the structural and biochemical investigation of microbial interactions. Here, we aim to understand the complex microbial networking in biotrophic interactions exemplified by the smut fungus Ustilago maydis and its host plant maize.
Developing effective strategies to colonize diverse environmental niches is key to the survival of all microorganisms. Here, most species co-exist within complex microbial communities or even tight symbiotic associations. Within these communities, microbes use a large repertoire of molecules to communicate but also shape the composition for their own benefit. We are specifically interested in gaining detailed insights into how pathogenic fungi, such as Ustilago maydis employ effector proteins to shape the biotrophic interaction, and how the communication between fungus and plant is facilitated in general. In addition, we aim to understand how fungi of the Peltigera genus shape their cyanobacterial partner within a symbiotic lichen community. To achieve this, we employ an integrative approach by combining structural and biochemical techniques (X-ray crystallography & cryo-EM) with cell biology techniques (e.g. CRISPR-Cas based genome editing & fluorescence microscopy).
Plant pathogenic fungi are causative agents of the majority of plant diseases and can lead to severe crop loss in infected populations. To colonize plants, fungi have evolved different strategies to avoid and counteract the plant immune system and manipulate their host plants. Of major importance are proteins secreted by the fungi that fulfill diverse functions to support the infection process hence termed effector proteins. More than 400 of these effector proteins have been reported to be encoded on the genome of U. maydis. However, only a few have been studied in detail to date while detailed mechanistic insights are mostly absent. Many of these proteins are highly specialized, and structural and biochemical information delineating their functions is often absent. We therefore combine structural and biochemical approaches with reverse genetics to gain detailed information on candidate effector proteins and understand their function during plant infection.
Complementary to our investigations on soluble effector proteins, we also seek to understand the role of membrane-associated proteins involved in the infection process which have been much less studied to date. To fill this gap, we employed a computational approach to identify membrane proteins in Ustilago maydis that are linked to virulence as judged by elevated gene expression during infection of maize plants. This investigation revealed several membrane proteins lacking domains of known function that are conserved among related smut fungi. We could already demonstrate two of those membrane proteins named Vmp1 and Vmp2 (for: virulence-associated membrane protein) strongly contribute to virulence by yet unknown mechanisms. Our findings are a first step towards understanding how specialized membrane proteins contribute to virulence in smut fungi and set the stage for an in-depth molecular characterization.
Biocommunication between plant and fungus
Plant colonization by pathogenic fungi is a complex process that requires guidance through certain cues and signals that are recognized and processed by the fungus. To this end different types of membrane-associated receptor proteins are employed. The process of mating and appressorium formation are well-studied in U. maydis but information on additional signals that guide the infection and their recognition and processing is scarce. Based on our computational approach outlined above, we extended the currently known repertoire of receptor proteins known in U. maydis and aim to understand their role during pathogenic development.
Lichens are among the most ancient and fascinating examples of complex microbial networks. They are known as pioneers that can establish themselves in extreme environments such as boreal forests, mountain tops and tundras. In lichens, an algal or cyanobacterial photobiont tightly associates with a fungal mycobiont to form complex morphological structures. These structures are formed by the mycobiont and provide shelter but the fungus also takes up essential nutrients and water. The photobiont in turn performs photosynthesis and supplies the mycobiont with macronutrients such as carbon and potentially also lipid compounds. Despite intensive research on lichen biology, molecular mechanisms that determine the establishment and maintenance of these symbiotic interactions presently remain unknown. Exemplified by fungi from the Peltigera genus that interact with Nostoc cyanobacteria, we aim to identify key features and components critical for the establishment of such a symbiosis. We currently focus on fungal carbohydrate-binding proteins (lectins) that allow the establishment and maintenance of intercellular contacts and secreted effector proteins such as antimicrobial proteins (AMPs) to shape the microbial community. A thorough biochemical and functional characterization will expand our current knowledge of how these proteins shape the lichen microbiota.
Weiland P., Dempwolff F., Steinchen W., Freibert S.A., Tian H., Glatter T., Martin R., Thomma, B.P.H.J., Bange G.#, Altegoer F.# (2023) Structural and functional analysis of the cerato-platanin-like effector protein Cpl1 suggests diverging functions in smut fungi. Mol Plant Pathol.
Altegoer, F.#, Quax T.E.F., Weiland P., Nußbaum P., Giammarinaro P.I., Patro, M., Zhengqun L., Oesterhelt D., Grininger M., Albers, S.V., Bange G. # (2022) Structural insights into the mechanism of archaellar rotational switching. Nat Commun, 13(1):2857
Feyh, R., Waeber, N. B., Prinz, S., Giammarinaro, P. I., Bange, G., Hochberg, G., Hartmann, R. K. #, & Altegoer, F. # (2021). Structure and mechanistic features of the prokaryotic minimal RNase P. Elife, 10.
Weiland, P., & Altegoer, F. (2021). Identification and Characterization of Two Transmembrane Proteins Required for Virulence of Ustilago maydis. Front Plant Sci, 12, 669835.
Altegoer, F. #, Weiland, P., Giammarinaro, P. I., Freibert, S. A., Binnebesel, L., Han, X., Lepak, A., Kahmann, R., Lechner, M., & Bange, G. # (2020). The two paralogous kiwellin proteins KWL1 and KWL1-b from maize are structurally related and have overlapping functions in plant defense. J Biol Chem, 295, 7816-7825.
Han, X., Altegoer, F., Steinchen, W., Binnebesel, L., Schuhmacher, J., Glatter, T., Giammarinaro, P. I., Djamei, A., Rensing, S. A., Reissmann, S., Kahmann, R., & Bange, G. (2019). A kiwellin disarms the metabolic activity of a secreted fungal virulence factor. Nature, 565, 650-653.
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