Loss of centromere function drives karyotype evolution in closely related <i>Malassezia</i> species.

Abstract

Genomic rearrangements associated with speciation often result in variation in chromosome number among closely related species. <i>Malassezia</i> species show variable karyotypes ranging between six and nine chromosomes. Here, we experimentally identified all eight centromeres in <i>M. sympodialis</i> as 3-5-kb long kinetochore-bound regions that span an AT-rich core and are depleted of the canonical histone H3. Centromeres of similar sequence features were identified as CENP-A-rich regions in <i>Malassezia furfur</i>, which has seven chromosomes, and histone H3 depleted regions in <i>Malassezia slooffiae</i> and <i>Malassezia globosa</i> with nine chromosomes each. Analysis of synteny conservation across centromeres with newly generated chromosome-level genome assemblies suggests two distinct mechanisms of chromosome number reduction from an inferred nine-chromosome ancestral state: (a) chromosome breakage followed by loss of centromere DNA and (b) centromere inactivation accompanied by changes in DNA sequence following chromosome-chromosome fusion. We propose that AT-rich centromeres drive karyotype diversity in the <i>Malassezia</i> species complex through breakage and inactivation.