I am intrigued by the evolution and complex molecular backgrounds of parasite-host interactions. Already during my studies in biology at the University of Tübingen, I consequentially chose to investigate the plant-biotrophic grass smuts (Ustilaginaceae). These are basidiomycetous fungi that evolved a high diversity on a narrow host range [1, 2]. Their most prominent member, Ustilago maydis, provided deep insights into the biology of plant biotrophic fungi, not the least because its genome sequence became available some years ago . Like all sexual smut fungi, U. maydis displays a characteristic biphasic life cycle switching between saprotrophy and biotrophy. The parasitic phase can only be initiated after dikaryotisation. Mating is thus taking a central role in the life cycle. For successful mating, two compatible mating partners have to recognise each other via a pheromone pheromone-receptor (PR) system resulting in the formation and directed growth of conjugation hyphae . After fusion of the conjugation hyphae, dimerising homeodomain transcription factors (HD) regulate the establishment of a dikaryotic filament that is able to penetrate the host plant . Only if both mating partners are heteroallelic in both mating loci a (PR) and b (HD) a full transition from saprophytic yeast cells to parasitic filaments can proceed. After penetration, U. maydis proliferates within the host tissue culminating in the formation of spectacular galls that are filled with wind-borne teliospores [6, 7]. Contrary to earlier expectations, U. maydis and its host plant Zea mays seem to lack a gene-for-gene (GFG) interaction, which are typical for other plant-parasitic fungi like the powdery mildews and rust fungi. Nevertheless, the genome of U. maydis revealed 12 gene clusters of secreted proteins of unknown function that are co-regulated and induced during pathogenesis . As seen in case of pep1, there are additional unclustered virulence genes within the genome of U. maydis further complicating the multiallelic parasite-host interaction .
Currently, I am pursuing the following projects:
1) Mating biology and evolution of grass smuts
In sexual smuts the necessity for mating in order to conserve the parasitical niche imposes strong selection pressure on mating to take place. Of course, mating also leads to the recombination of different genotypes but depending on the specificity of the mating system, it could even enable hybridization of different species. To learn more about the functional and evolutionary framework of mating biology in the Ustilaginaceae molecular, functional and morphological approaches are integrated. Thus, we investigate the specificity of the PR system, the morphological diversity of mating structures, the genetic organisation of a-loci and their evolutionary transitions. By comparing our findings to those made in other fungal groups we want to broaden the fungal perspective on mating biology and evolution.
2) Intraspecific variability of fungal effectors of Ustilago maydis
Recent U. maydis populations seem to have evolved from a parasite population of the first domesticated maize progenitor teosinte 9 – 12,000 years ago . In consequence, the substitution patterns observed today potentially reflect different selection regimes during domestication and could thus unveil useful candidate genes of multiallelic parasite-host interactions for forward genetic approaches. In order to track these evolutionary footprints we investigate the intraspecific signature and genetic variability of fungal effectors of U. maydis. In particular, we focus on the virulence clusters 2A and 19A with different effects on virulence .
1. Begerow D, Göker M, Lutz M, Stoll M: On the evolution of smut fungi on their hosts. In Frontiers in basidiomycote mycology Edited by 2004:81-98.
2. Stoll M, Begerow D, Oberwinkler F: Molecular phylogeny of Ustilago, Sporisorium, and related taxa based on combined analyses of rDNA sequences. Mycol Res 2005, 109(Pt 3):342-356.
3. Brefort T, Doehlemann G, Mendoza-Mendoza A, Reissmann S, Djamei A, Kahmann R: Ustilago maydis as a Pathogen Annu Rev Phytopathol 2009, 47:423-445.
4. Snetselaar KM, Bolker M, Kahmann R: Ustilago maydis Mating Hyphae Orient Their Growth toward Pheromone Sources Fungal Genet Biol 1996, 20(4):299-312.
5. Doehlemann G, Wahl R, Vranes M, de Vries RP, Kamper J, Kahmann R: Establishment of compatibility in the Ustilago maydis/maize pathosystem. J Plant Physiol 2008, 165(1):29-40.
6. Snetselaar KM, Mims CW: Infection of maize stigmas by Ustilago maydis - light and electron-microscopy Phytopathology 1993, 83(8):843-850.
7. Bauer R, Oberwinkler F, Vánky K: Ultrastructural markers and systematics in smut fungi and allied taxa. Can J Bot 1997, 75:1273-1314.
8. Kamper J et al.: Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 2006, 444(7115):97-101.
9. Doehlemann G, van der Linde K, Assmann D, Schwammbach D, Hof A, Mohanty A, Jackson D, Kahmann R: Pep1, a secreted effector protein of Ustilago maydis, is required for successful invasion of plant cells. PLoS Pathog 2009, 5(2):e1000290.
10. Munkacsi AB, Stoxen S, May G: Ustilago maydis populations tracked maize through domestication and cultivation in the Americas. Proc Biol Sci 2008, 275(1638):1037-1046.