Host jump enabling factors in a fungal/grass pathosystem

• Applicant: Dr. Ulrich Güldener
• Subject Area: Evolution and Systematics of Plants and Fungi ; Bioinformatics and Theoretical Biology
• Term: from 2016 to 2021
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 321339447

• Final Report Year: 2021

Final Report Abstract

The goal of the project was to elucidate the factors necessary to enable host switching of the barley- infecting smut fungus Ustilago hordei to the non-host plant Brachypodium distachyon. The research strategy is based on the finding that U. hordei and the Brachypodium distachyon infecting smut fungus Ustilago bromivora can mate and form hybrids, which can cause symptoms on the model grass B. distachyon. An important starting point for identifying the factors necessary for the observed host switching are hybrid backcrosses, in which the hybrid strain U. bromivora/ U. hordei mat1 is mated with U. hordei mat2 in each generation until symptoms disappear. By screening numerous infected plants for phenotypes over 4 backcross generations using a newly developed phenotyping system (PhenoBox) and then sequencing the fungal hybrids, we identified 75 genes in regions associated with virulence. Different approaches were used to identify SNPs to differentiate the ancestry of these genomic regions and genes that are infection/symptom essential. The genes are located in three regions of the U. bromivora genome that are likely important for pathogenicity of U. bromivora on Brachypodium spp. The regions are present on U. bromivora chromosomes 8, 13, and 22 with strongest association with hybrid virulence from chromosome 8. We showed that this region has more putative effector proteins but is not essential for virulence, suggesting that infection can occur with different effector complements. It seems likely that host specificity evolved rather slowly, gradually, and may not have arisen from a specific event. Perhaps the ancestors of U. bromivora and U. hordei encountered Brachypodium spp. due to migration on the plant or fungal side, or climate change enabled infection as is currently observed for Magnaporthe grisea pathogenicity on wheat. Given the widespread potential for hybridization among members of the family Ustilaginaceae, one could envision hybrid infections as a useful tool for studying host-specific pathogenicity in smut fungi in general and perhaps more broadly.

Publications

• 2018. The “PhenoBox”, a flexible, automated, open-source plant phenotyping solution. New Phytol.
  Czedik-Eysenberg, A., Seitner, S., Güldener, U., Koemeda, S., Jez, J., Colombini, M., Djamei, A.
  
• 2019. Two Is Better Than One: Studying Ustilago bromivora–Brachypodium Compatibility by Using a Hybrid Pathogen. MPMI 32, 1623–1634
  Bosch, J., Czedik-Eysenberg, A., Hastreiter, M., Khan, M., Güldener, U., Djamei, A.