title: Discovery of an unconventional centromere in budding yeast redefines evolution of point centromeres.
abstract: Centromeres are the chromosomal regions promoting kinetochore assembly for chromosome segregation. In many eukaryotes, the centromere consists of up to mega base pairs of DNA. On such "regional centromeres," kinetochore assembly is mainly defined by epigenetic regulation [1]. By contrast, a clade of budding yeasts (Saccharomycetaceae) has a "point centromere" of 120-200 base pairs of DNA, on which kinetochore assembly is defined by the consensus DNA sequence [2, 3]. During evolution, budding yeasts acquired point centromeres, which replaced ancestral, regional centromeres [4]. All known point centromeres among different yeast species share common consensus DNA elements (CDEs) [5, 6], implying that they evolved only once and stayed essentially unchanged throughout evolution. Here, we identify a yeast centromere that challenges this view: that of the budding yeast Naumovozyma castellii is the first unconventional point centromere with unique CDEs. The N. castellii centromere CDEs are essential for centromere function but have different DNA sequences from CDEs in other point centromeres. Gene order analyses around N. castellii centromeres indicate their unique, and separate, evolutionary origin. Nevertheless, they are still bound by the ortholog of the CBF3 complex, which recognizes CDEs in other point centromeres. The new type of point centromere originated prior to the divergence between N. castellii and its close relative Naumovozyma dairenensis and disseminated to all N. castellii chromosomes through extensive genome rearrangement. Thus, contrary to the conventional view, point centromeres can undergo rapid evolutionary changes. These findings give new insights into the evolution of point centromeres.
authors.affiliation: Centre for Gene Regulation and Expression, College of Life Sciences, University of Dundee, Dundee DD1 5EH, UK.
authors.forename: Norihiko
authors.initials: N
authors.lastname: Kobayashi
authors.affiliation: Department of Computational Biology, School of Frontier Medicine, University of Tokyo, Chiba 277-8562, Japan.
authors.forename: Yutaka
authors.initials: Y
authors.lastname: Suzuki
authors.affiliation: Whitehead Institute for Biomedical Research, Cambridge, MA 02142, USA; Howard Hughes Medical Institute and Department of Biology, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
authors.forename: Lori W
authors.initials: LW
authors.lastname: Schoenfeld
authors.affiliation: Sir William Dunn School of Pathology, University of Oxford, Oxford OX1 3RE, UK.
authors.forename: Carolin A
authors.initials: CA
authors.lastname: Müller
authors.affiliation: Sir William Dunn School of Pathology, University of Oxford, Oxford OX1 3RE, UK.
authors.forename: Conrad
authors.initials: C
authors.lastname: Nieduszynski
authors.affiliation: UCD Conway Institute, School of Medicine and Medical Science, University College Dublin, Dublin 4, Ireland.
authors.forename: Kenneth H
authors.initials: KH
authors.lastname: Wolfe
authors.affiliation: Centre for Gene Regulation and Expression, College of Life Sciences, University of Dundee, Dundee DD1 5EH, UK. Electronic address: t.tanaka@dundee.ac.uk.
authors.forename: Tomoyuki U
authors.initials: TU
authors.lastname: Tanaka
mesh_terms: D002503:Centromere / Q000235:genetics* / Q000378:metabolism; D004271:DNA, Fungal / Q000235:genetics* / Q000378:metabolism; D019143:Evolution, Molecular; D004718:Saccharomycetales / Q000235:genetics* / Q000378:metabolism
chemical_list: D004271:DNA, Fungal