RNAi is a critical determinant of centromere evolution in closely related fungi
Citation
Yadav, V., Sun, S., Billmyre, R.B., Thimmappa, B.C., Shea, T., Lintner, R., Bakkeren, G., Cuomo, C.A., Heitman, J., Sanyal, K. (2018). RNAi is a critical determinant of centromere evolution in closely related fungi. Proceedings of the National Academy of Sciences of the United States of America, [online] 115(12), 3108-3113. http://dx.doi.org/10.1073/pnas.1713725115
Plain language summary
Centromeres are regions of chromosomes important for proper distribution of each part of a duplicated pair of chromosomes during cell division. Even though centromeres have conserved functions among eukaryotes, their DNA sequences vary. This has been known as a paradox. Here, the centromeres of chromosomes from three closely related human fungal pathogens belonging to the Cryptococcus species complex were compared. Centromeres are known to consist of DNA repeats that are often transposable elements, known mobile elements that can cause chromosome instability. Almost all organisms have therefore a mechanism that keeps the activities of such elements in check, using a so-called RNA silencing mechanism. The species that did not have a functional RNA silencing machinery showed occasional shortened centromeres with smaller, seemingly defective transposable elements, and lost more characteristic signaling marks on one of their DNA bases. Computer analysis among two related plant pathogenic smut fungi, one with and one without a functional RNA silencing mechanism, pointed to the same phenomenon: smaller centromeres in the deficient species.
Abstract
The centromere DNA locus on a eukaryotic chromosome facilitates faithful chromosome segregation. Despite performing such a conserved function, centromere DNA sequence as well as the organization of sequence elements is rapidly evolving in all forms of eukaryotes. The driving force that facilitates centromere evolution remains an enigma. Here, we studied the evolution of centromeres in closely related species in the fungal phylum of Basidiomycota. Using ChIP-seq analysis of conserved inner kinetochore proteins, we identified centromeres in three closely related Cryptococcus species: two of which are RNAi-proficient, while the other lost functional RNAi. We find that the centromeres in the RNAi-deficient species are significantly shorter than those of the two RNAi-proficient species. While centromeres are LTR retrotransposon-rich in all cases, the RNAi-deficient species lost all full-length retroelements from its centromeres. In addition, centromeres in RNAi-proficient species are associated with a significantly higher level of cytosine DNA modifications compared with those of RNAi-deficient species. Furthermore, when an RNAi-proficient Cryptococcus species and its RNAi-deficient mutants were passaged under similar conditions, the centromere length was found to be occasionally shortened in RNAi mutants. In silico analysis of predicted centromeres in a group of closely related Ustilago species, also belonging to the Basidiomycota, were found to have undergone a similar transition in the centromere length in an RNAi-dependent fashion. Based on the correlation found in two independent basidiomycetous species complexes, we present evidence suggesting that the loss of RNAi and cytosine DNA methylation triggered transposon attrition, which resulted in shortening of centromere length during evolution.