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Proc Natl Acad Sci U S A DOI:10.1073/pnas.1713725115

RNAi is a critical determinant of centromere evolution in closely related fungi.

Publication TypeJournal Article
Year of Publication2018
AuthorsYadav, V, Sun, S, R Billmyre, B, Thimmappa, BC, Shea, T, Lintner, R, Bakkeren, G, Cuomo, CA, Heitman, J, Sanyal, K
JournalProc Natl Acad Sci U S A
Date Published2018 03 20
KeywordsBase Sequence, Centromere, Chromosomes, Fungal, Cryptococcus, DNA, Fungal, Evolution, Molecular, RNA Interference

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 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 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 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.


Alternate JournalProc. Natl. Acad. Sci. U.S.A.
PubMed ID29507212
PubMed Central IDPMC5866544
Grant ListR01 AI039115 / AI / NIAID NIH HHS / United States
R01 AI050113 / AI / NIAID NIH HHS / United States
R37 AI039115 / AI / NIAID NIH HHS / United States
U19 AI110818 / AI / NIAID NIH HHS / United States