Holocentromeres in Rhynchospora are associated with genome-wide centromere-specific repeat arrays interspersed among euchromatin.
Holocentric chromosomes lack a primary constriction, in contrast to monocentrics. They form kinetochores distributed along almost the entire poleward surface of the chromatids, to which spindle fibers attach. No centromere-specific DNA sequence has been found for any holocentric organism studied so far. It was proposed that centromeric repeats, typical for many monocentric species, could not occur in holocentrics, most likely because of differences in the centromere organization. Here we show that the holokinetic centromeres of the Cyperaceae Rhynchospora pubera are highly enriched by a centromeric histone H3 variant-interacting centromere-specific satellite family designated "Tyba" and by centromeric retrotransposons (i.e., CRRh) occurring as genome-wide interspersed arrays. Centromeric arrays vary in length from 3 to 16 kb and are intermingled with gene-coding sequences and transposable elements. We show that holocentromeres of metaphase chromosomes are composed of multiple centromeric units rather than possessing a diffuse organization, thus favoring the polycentric model. A cell-cycle-dependent shuffling of multiple centromeric units results in the formation of functional (poly)centromeres during mitosis. The genome-wide distribution of centromeric repeat arrays interspersing the euchromatin provides a previously unidentified type of centromeric chromatin organization among eukaryotes. Thus, different types of holocentromeres exist in different species, namely with and without centromeric repetitive sequences.
Laboratory of Plant Cytogenetics and Evolution, Department of Botany, Federal University of Pernambuco, 50670-420 Recife, Pernambuco, Brazil; Leibniz Institute of Plant Genetics and Crop Plant Research Gatersleben, 06466 Stadt Seeland, Germany;
André
A
Marques
Laboratory of Plant Cytogenetics and Evolution, Department of Botany, Federal University of Pernambuco, 50670-420 Recife, Pernambuco, Brazil; Leibniz Institute of Plant Genetics and Crop Plant Research Gatersleben, 06466 Stadt Seeland, Germany;
Tiago
T
Ribeiro
Laboratory of Molecular Cytogenetics, Institute of Plant Molecular Biology, Biology Centre of the Academy of Sciences of the Czech Republic, 370 05 Ceske Budejovice, Czech Republic;
Pavel
P
Neumann
Laboratory of Molecular Cytogenetics, Institute of Plant Molecular Biology, Biology Centre of the Academy of Sciences of the Czech Republic, 370 05 Ceske Budejovice, Czech Republic;
Jiří
J
Macas
Laboratory of Molecular Cytogenetics, Institute of Plant Molecular Biology, Biology Centre of the Academy of Sciences of the Czech Republic, 370 05 Ceske Budejovice, Czech Republic;
Petr
P
Novák
Leibniz Institute of Plant Genetics and Crop Plant Research Gatersleben, 06466 Stadt Seeland, Germany;
Veit
V
Schubert
Leibniz Institute of Plant Genetics and Crop Plant Research Gatersleben, 06466 Stadt Seeland, Germany;
Marco
M
Pellino
Leibniz Institute of Plant Genetics and Crop Plant Research Gatersleben, 06466 Stadt Seeland, Germany;
Jörg
J
Fuchs
Leibniz Institute of Plant Genetics and Crop Plant Research Gatersleben, 06466 Stadt Seeland, Germany;
Wei
W
Ma
Leibniz Institute of Plant Genetics and Crop Plant Research Gatersleben, 06466 Stadt Seeland, Germany;
Markus
M
Kuhlmann
Leibniz Institute of Plant Genetics and Crop Plant Research Gatersleben, 06466 Stadt Seeland, Germany;
Ronny
R
Brandt
Laboratory of Cytogenetics and Plant Diversity, Department of General Biology, State University of Londrina, 86057-970, Londrina, Paraná, Brazil;
André L L
AL
Vanzela
Center of the Region Haná for Biotechnological and Agricultural Research, Institute of Experimental Botany, CZ-78371 Olomouc, Czech Republic.
Tomáš
T
Beseda
Center of the Region Haná for Biotechnological and Agricultural Research, Institute of Experimental Botany, CZ-78371 Olomouc, Czech Republic.
Hana
H
Šimková
Laboratory of Plant Cytogenetics and Evolution, Department of Botany, Federal University of Pernambuco, 50670-420 Recife, Pernambuco, Brazil; andrea.pedrosaharand@pesquisador.cnpq.br houben@ipk-gatersleben.de.
Andrea
A
Pedrosa-Harand
Leibniz Institute of Plant Genetics and Crop Plant Research Gatersleben, 06466 Stadt Seeland, Germany; andrea.pedrosaharand@pesquisador.cnpq.br houben@ipk-gatersleben.de.
Andreas
A
Houben
D002503:Centromere; D029785:Cyperaceae / Q000235:genetics*; D004276:DNA, Satellite / Q000235:genetics; D022041:Euchromatin / Q000235:genetics*; D018745:Genome, Plant; D008969:Molecular Sequence Data; D020080:Tandem Repeat Sequences
D004276:DNA, Satellite; D022041:Euchromatin
centromere; chromosome; evolution; holokinetic; satellite DNA