Adaptive evolution of centromere proteins in plants and animals.
BACKGROUND
Centromeres represent the last frontiers of plant and animal genomics. Although they perform a conserved function in chromosome segregation, centromeres are typically composed of repetitive satellite sequences that are rapidly evolving. The nucleosomes of centromeres are characterized by a special H3-like histone (CenH3), which evolves rapidly and adaptively in Drosophila and Arabidopsis. Most plant, animal and fungal centromeres also bind a large protein, centromere protein C (CENP-C), that is characterized by a single 24 amino-acid motif (CENPC motif).


RESULTS
Whereas we find no evidence that mammalian CenH3 (CENP-A) has been evolving adaptively, mammalian CENP-C proteins contain adaptively evolving regions that overlap with regions of DNA-binding activity. In plants we find that CENP-C proteins have complex duplicated regions, with conserved amino and carboxyl termini that are dissimilar in sequence to their counterparts in animals and fungi. Comparisons of Cenpc genes from Arabidopsis species and from grasses revealed multiple regions that are under positive selection, including duplicated exons in some grasses. In contrast to plants and animals, yeast CENP-C (Mif2p) is under negative selection.


CONCLUSIONS
CENP-Cs in all plant and animal lineages examined have regions that are rapidly and adaptively evolving. To explain these remarkable evolutionary features for a single-copy gene that is needed at every mitosis, we propose that CENP-Cs, like some CenH3s, suppress meiotic drive of centromeres during female meiosis. This process can account for the rapid evolution and the complexity of centromeric DNA in plants and animals as compared to fungi.
Talbert
Paul B
PB
Howard Hughes Medical Institute, Fred Hutchinson Cancer Research Center, Seattle, WA 98109-1024, USA.
Bryson
Terri D
TD
Henikoff
Steven
S
D000222:Adaptation, Physiological; D000595:Amino Acid Sequence; D000818:Animals; D001324:Autoantigens / Q000235:genetics; D001483:Base Sequence; D002503:Centromere / Q000737:chemistry / Q000378:metabolism; D000076247:Centromere Protein A; D002868:Chromosomal Proteins, Non-Histone / Q000235:genetics*; D004268:DNA-Binding Proteins / Q000235:genetics; D019143:Evolution, Molecular; D005091:Exons; D008540:Meiosis; D051379:Mice; D008969:Molecular Sequence Data; D010940:Plant Proteins / Q000235:genetics*; D006109:Poaceae / Q000235:genetics; D051381:Rats; D029701:Saccharomyces cerevisiae Proteins / Q000235:genetics; D016415:Sequence Alignment
D001324:Autoantigens; C000619701:Cenpa protein, mouse; D000076247:Centromere Protein A; D002868:Chromosomal Proteins, Non-Histone; D004268:DNA-Binding Proteins; C083768:MIF2 protein, S cerevisiae; D010940:Plant Proteins; D029701:Saccharomyces cerevisiae Proteins; C060905:centromere protein C