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: since 2020
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 444838523

Accessory chromosomes show presence/absence polymorphism between individuals of a population. In plants and animals they are considered to be selfish genetic elements that increase their frequency by a preferential segregation during mitosis or meiosis. In plant pathogenic fungi however, accessory chromosomes often directly affect host specificity and virulence but their mode of transmission during cell-divisions is mostly unknown. This project aims at understanding the transmission and maintenance of fungal accessory chromosomes using the wheat pathogen Zymoseptoria tritici. This economically important fungus contains up to eight distinct accessory chromosomes. For seven of these we could recently show an increase in frequency during meiosis by a chromosome drive. Importantly, this drive appears to be functionally different from all other previously described chromosome drive mechanisms by relying on an additional DNA replication step and not on preferential segregation. In contrast to the dynamics during meiosis, accessory chromosomes in Z tritici are lost at very high frequency during mitosis. These mitotic losses are affected by histone modifications, which are enriched on the accessory chromosome, in particular H3K27me3, which in turn also influences DNA replication. To date, the exact mechanisms underlying both the meiotic drive and the mitotic losses as well as the evolutionary origin of these two distinct forms of transmission during cell divisions are unknown. The objectives of this project are thus to enhance our understanding of these mechanisms and their evolution by addressing four distinct questions. i) Do histone modification also affect the meiotic drive of accessory chromosomes? ii) Is the meiotic drive influenced by the size of the chromosomes? iii) Do accessory chromosomes in closely related species exhibit a similar mitotic transmission? - and in an explorative part of the project - iv) What are the structures involved in sexual reproduction of Z. tritici and how do they relate to the occurrence of the chromosome drive? To address these questions I will manipulate the histone modification pattern and the chromosome size of accessory chromosomes and test whether these changes influence the meiotic drive and the mitotic losses. In addition, I will use confocal microscopy to characterize the sexual development of Z. tritici in the wheat host and relate the characteristics to the chromosome drive. Taken together, this project will yield a new mechanistic understanding of both the novel meiotic drive mechanism as well as the associated mitotic loss of accessory chromosomes. It will also assess the role of histone modifications as well as cis-acting genetic elements on the drive mechanism. This information will further our understanding of the processes involved in maintaining the accessory chromosomes in Z. tritici and may also help to explain their prevalence in other important plant pathogens.

• DFG Programme: Research Grants