Evolutionary maintenance of selfish accessory chromosomes in a fungal plant pathogen

• Applicant: Dr. Michael Habig
• Subject Area: Organismic Interactions, Chemical Ecology and Microbiomes of Plant Systems ; Evolution, Anthropology
• Term: from 2020 to 2024
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 444838523

• Final Report Year: 2024

Final Report Abstract

Accessory chromosomes show presence/absence polymorphism, meaning they are present in some but not all individuals of a population. These chromosomes are widespread across plant, animal, and fungal species and, while considered non-essential for growth, can significantly impact fitness. They can also exhibit notable differences from essential core chromosomes during mitotic and meiotic transmission. This project aimed to explore the transmission of fungal accessory chromosomes during meiosis and mitosis, focusing on plant-pathogenic fungi from the Zymoseptoria genus and insect-pathogenic fungi from the Metarhizium genus. In a first study, we assessed the impact of posttranslational histone modifications on the transmission and mutation rates of accessory chromosomes in Z. tritici. Histone marks associated with heterochromatin, such as H3K9me3 and H3K27me3, were found to influence both mutation rates and chromosome stability. The removal of H3K9me3 increased base substitution mutation rates, while the removal of H3K27me3 decreased them. These histone modifications also had significant effects on the rate of structural variants, the mobilization of transposable elements, and the stability and replication of core and accessory chromosomes. In another study focusing on meiotic transmission in Z. tritici, we analyzed 23 complete tetrads and found that accessory chromosomes had higher recombination rates than core chromosomes. Additionally, we identified repeat-induced point mutations (RIP), a fungal defense mechanism against transposons, as the primary cause of meiotic mutations in Z. tritici. This study was the first to experimentally demonstrate that RIP is active in this species. In a separate study, we showed that an accessory chromosome, chrA, in the insect pathogen M. robertsii, was horizontally transferred multiple times, while no other genetic material was transferred. ChrA seemed to provide a competitive advantage under specific host conditions and was transferred across species boundaries within the Metarhizium genus. Lastly, in an unpublished part of the project, we examined the impact of histone modifications on accessory chromosome transmission in Z. ardabiliae, a sister species of Z. tritici, revealing contrasting patterns between the two species. Overall, these findings provide insights into the roles of histone modifications, mitotic processes, horizontal transfer, and meiotic mechanisms in the transmission and evolution of fungal accessory chromosomes.

Publications

• Epigenetic modifications affect the rate of spontaneous mutations in a pathogenic fungus. Nature Communications, 12(1).
  Habig, Michael; Lorrain, Cecile; Feurtey, Alice; Komluski, Jovan & Stukenbrock, Eva H.
  
• Non-Mendelian transmission of accessory chromosomes in fungi. Chromosome Research, 30(2-3), 241-253.
  Komluski, Jovan; Stukenbrock, Eva H. & Habig, Michael
  
• Repeat-Induced Point Mutation and Gene Conversion Coinciding with Heterochromatin Shape the Genome of a Plant-Pathogenic Fungus. mBio, 14(3).
  Komluski, Jovan; Habig, Michael & Stukenbrock, Eva H.
  
• Frequent horizontal chromosome transfer between asexual fungal insect pathogens. Proceedings of the National Academy of Sciences, 121(11).
  Habig, Michael; Grasse, Anna V.; Müller, Judith; Stukenbrock, Eva H.; Leitner, Hanna & Cremer, Sylvia