Stretching the Rules: Monocentric Chromosomes with Multiple Centromere Domains

The centromere is a functional chromosome domain that is essential for faithful chromosome segregation during cell division and that can be reliably identified by the presence of the centromere-specific histone H3 variant CenH3. In monocentric chromosomes, the centromere is characterized by a single...

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Main Authors: Neumann, Pavel, Navrátilová, Alice, Schroeder-Reiter, Elizabeth, Koblížková, Andrea, Steinbauerová, Veronika, Chocholová, Eva, Novák, Petr, Wanner, Gerhard, Macas, Jiří
Format: Online
Language:English
Published: Public Library of Science 2012
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3380829/
id pubmed-3380829
recordtype oai_dc
spelling pubmed-33808292012-06-26 Stretching the Rules: Monocentric Chromosomes with Multiple Centromere Domains Neumann, Pavel Navrátilová, Alice Schroeder-Reiter, Elizabeth Koblížková, Andrea Steinbauerová, Veronika Chocholová, Eva Novák, Petr Wanner, Gerhard Macas, Jiří Research Article The centromere is a functional chromosome domain that is essential for faithful chromosome segregation during cell division and that can be reliably identified by the presence of the centromere-specific histone H3 variant CenH3. In monocentric chromosomes, the centromere is characterized by a single CenH3-containing region within a morphologically distinct primary constriction. This region usually spans up to a few Mbp composed mainly of centromere-specific satellite DNA common to all chromosomes of a given species. In holocentric chromosomes, there is no primary constriction; the centromere is composed of many CenH3 loci distributed along the entire length of a chromosome. Using correlative fluorescence light microscopy and high-resolution electron microscopy, we show that pea (Pisum sativum) chromosomes exhibit remarkably long primary constrictions that contain 3–5 explicit CenH3-containing regions, a novelty in centromere organization. In addition, we estimate that the size of the chromosome segment delimited by two outermost domains varies between 69 Mbp and 107 Mbp, several factors larger than any known centromere length. These domains are almost entirely composed of repetitive DNA sequences belonging to 13 distinct families of satellite DNA and one family of centromeric retrotransposons, all of which are unevenly distributed among pea chromosomes. We present the centromeres of Pisum as novel “meta-polycentric” functional domains. Our results demonstrate that the organization and DNA composition of functional centromere domains can be far more complex than previously thought, do not require single repetitive elements, and do not require single centromere domains in order to segregate properly. Based on these findings, we propose Pisum as a useful model for investigation of centromere architecture and the still poorly understood role of repetitive DNA in centromere evolution, determination, and function. Public Library of Science 2012-06-21 /pmc/articles/PMC3380829/ /pubmed/22737088 http://dx.doi.org/10.1371/journal.pgen.1002777 Text en Neumann et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
repository_type Open Access Journal
institution_category Foreign Institution
institution US National Center for Biotechnology Information
building NCBI PubMed
collection Online Access
language English
format Online
author Neumann, Pavel
Navrátilová, Alice
Schroeder-Reiter, Elizabeth
Koblížková, Andrea
Steinbauerová, Veronika
Chocholová, Eva
Novák, Petr
Wanner, Gerhard
Macas, Jiří
spellingShingle Neumann, Pavel
Navrátilová, Alice
Schroeder-Reiter, Elizabeth
Koblížková, Andrea
Steinbauerová, Veronika
Chocholová, Eva
Novák, Petr
Wanner, Gerhard
Macas, Jiří
Stretching the Rules: Monocentric Chromosomes with Multiple Centromere Domains
author_facet Neumann, Pavel
Navrátilová, Alice
Schroeder-Reiter, Elizabeth
Koblížková, Andrea
Steinbauerová, Veronika
Chocholová, Eva
Novák, Petr
Wanner, Gerhard
Macas, Jiří
author_sort Neumann, Pavel
title Stretching the Rules: Monocentric Chromosomes with Multiple Centromere Domains
title_short Stretching the Rules: Monocentric Chromosomes with Multiple Centromere Domains
title_full Stretching the Rules: Monocentric Chromosomes with Multiple Centromere Domains
title_fullStr Stretching the Rules: Monocentric Chromosomes with Multiple Centromere Domains
title_full_unstemmed Stretching the Rules: Monocentric Chromosomes with Multiple Centromere Domains
title_sort stretching the rules: monocentric chromosomes with multiple centromere domains
description The centromere is a functional chromosome domain that is essential for faithful chromosome segregation during cell division and that can be reliably identified by the presence of the centromere-specific histone H3 variant CenH3. In monocentric chromosomes, the centromere is characterized by a single CenH3-containing region within a morphologically distinct primary constriction. This region usually spans up to a few Mbp composed mainly of centromere-specific satellite DNA common to all chromosomes of a given species. In holocentric chromosomes, there is no primary constriction; the centromere is composed of many CenH3 loci distributed along the entire length of a chromosome. Using correlative fluorescence light microscopy and high-resolution electron microscopy, we show that pea (Pisum sativum) chromosomes exhibit remarkably long primary constrictions that contain 3–5 explicit CenH3-containing regions, a novelty in centromere organization. In addition, we estimate that the size of the chromosome segment delimited by two outermost domains varies between 69 Mbp and 107 Mbp, several factors larger than any known centromere length. These domains are almost entirely composed of repetitive DNA sequences belonging to 13 distinct families of satellite DNA and one family of centromeric retrotransposons, all of which are unevenly distributed among pea chromosomes. We present the centromeres of Pisum as novel “meta-polycentric” functional domains. Our results demonstrate that the organization and DNA composition of functional centromere domains can be far more complex than previously thought, do not require single repetitive elements, and do not require single centromere domains in order to segregate properly. Based on these findings, we propose Pisum as a useful model for investigation of centromere architecture and the still poorly understood role of repetitive DNA in centromere evolution, determination, and function.
publisher Public Library of Science
publishDate 2012
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3380829/
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