title: Recurrent loss of CenH3 is associated with independent transitions to holocentricity in insects.
abstract: Faithful chromosome segregation in all eukaryotes relies on centromeres, the chromosomal sites that recruit kinetochore proteins and mediate spindle attachment during cell division. The centromeric histone H3 variant, CenH3, is the defining chromatin component of centromeres in most eukaryotes, including animals, fungi, plants, and protists. In this study, using detailed genomic and transcriptome analyses, we show that CenH3 was lost independently in at least four lineages of insects. Each of these lineages represents an independent transition from monocentricity (centromeric determinants localized to a single chromosomal region) to holocentricity (centromeric determinants extended over the entire chromosomal length) as ancient as 300 million years ago. Holocentric insects therefore contain a CenH3-independent centromere, different from almost all the other eukaryotes. We propose that ancient transitions to holocentricity in insects obviated the need to maintain CenH3, which is otherwise essential in most eukaryotes, including other holocentrics.
authors.affiliation: Division of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, United States.
authors.forename: Ines A
authors.initials: IA
authors.lastname: Drinnenberg
authors.affiliation: Department of Biology, University of Washington, Seattle, United States.
authors.forename: Dakota
authors.initials: D
authors.lastname: deYoung
authors.affiliation: Division of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, United States.
authors.forename: Steven
authors.initials: S
authors.lastname: Henikoff
authors.affiliation: Division of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, United States.
authors.forename: Harmit Singh
authors.identifier: http://orcid.org/0000-0001-6005-0016
authors.initials: HS
authors.lastname: Malik
mesh_terms: D000818:Animals; D001324:Autoantigens / Q000235:genetics* / Q000378:metabolism*; D000076247:Centromere Protein A; D002868:Chromosomal Proteins, Non-Histone / Q000235:genetics* / Q000378:metabolism*; D002875:Chromosomes / Q000648:ultrastructure; D003058:Cockroaches; D005786:Gene Expression Regulation; D006135:Gryllidae; D007313:Insecta; D018386:Kinetochores / Q000378:metabolism; D007915:Lepidoptera; D063191:Odonata; D010802:Phylogeny; D017423:Sequence Analysis, RNA; D013045:Species Specificity
chemical_list: D001324:Autoantigens; D000076247:Centromere Protein A; D002868:Chromosomal Proteins, Non-Histone
keywords: CenH3; Hemiptera; Lepidoptera; Odonata; chromosomes; evolutionary biology; genes; genomics; holocentromere; insects