Literature DB >> 27616209

Absence of positive selection on CenH3 in Luzula suggests that holokinetic chromosomes may suppress centromere drive.

František Zedek1, Petr Bureš2.   

Abstract

BACKGROUND AND AIMS: The centromere drive theory explains diversity of eukaryotic centromeres as a consequence of the recurrent conflict between centromeric repeats and centromeric histone H3 (CenH3), in which selfish centromeres exploit meiotic asymmetry and CenH3 evolves adaptively to counterbalance deleterious consequences of driving centromeres. Accordingly, adaptively evolving CenH3 has so far been observed only in eukaryotes with asymmetric meiosis. However, if such evolution is a consequence of centromere drive, it should depend not only on meiotic asymmetry but also on monocentric or holokinetic chromosomal structure. Selective pressures acting on CenH3 have never been investigated in organisms with holokinetic meiosis despite the fact that holokinetic chromosomes have been hypothesized to suppress centromere drive. Therefore, the present study evaluates selective pressures acting on the CenH3 gene in holokinetic organisms for the first time, specifically in the representatives of the plant genus Luzula (Juncaceae), in which the kinetochore formation is not co-localized with any type of centromeric repeat.
METHODS: PCR, cloning and sequencing, and database searches were used to obtain coding CenH3 sequences from Luzula species. Codon substitution models were employed to infer selective regimes acting on CenH3 in Luzula KEY
RESULTS: In addition to the two previously published CenH3 sequences from L. nivea, 16 new CenH3 sequences have been isolated from 12 Luzula species. Two CenH3 isoforms in Luzula that originated by a duplication event prior to the divergence of analysed species were found. No signs of positive selection acting on CenH3 in Luzula were detected. Instead, evidence was found that selection on CenH3 of Luzula might have been relaxed.
CONCLUSIONS: The results indicate that holokinetism itself may suppress centromere drive and, therefore, holokinetic chromosomes might have evolved as a defence against centromere drive.
© The Author 2016. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: journals.permissions@oup.com.

Entities:  

Keywords:  CenH3; Luzula; centromere drive; holokinetic chromosomes; positive selection

Mesh:

Substances:

Year:  2016        PMID: 27616209      PMCID: PMC5155603          DOI: 10.1093/aob/mcw186

Source DB:  PubMed          Journal:  Ann Bot        ISSN: 0305-7364            Impact factor:   4.357


  37 in total

1.  Molecular phylogeny of the genus Luzula DC. (Juncaceae, Monocotyledones) based on plastome and nuclear ribosomal regions: a case of incongruence, incomplete lineage sorting and hybridisation.

Authors:  Lenka Záveská Drábková; Cestmír Vlček
Journal:  Mol Phylogenet Evol       Date:  2010-08-07       Impact factor: 4.286

2.  Studies on the Phenomenon of Preferential Segregation in Maize.

Authors:  G Y Kikudome
Journal:  Genetics       Date:  1959-09       Impact factor: 4.562

3.  Organisation of the plant genome in chromosomes.

Authors:  J S Pat Heslop-Harrison; Trude Schwarzacher
Journal:  Plant J       Date:  2011-04       Impact factor: 6.417

4.  Holocentromeres in Rhynchospora are associated with genome-wide centromere-specific repeat arrays interspersed among euchromatin.

Authors:  André Marques; Tiago Ribeiro; Pavel Neumann; Jiří Macas; Petr Novák; Veit Schubert; Marco Pellino; Jörg Fuchs; Wei Ma; Markus Kuhlmann; Ronny Brandt; André L L Vanzela; Tomáš Beseda; Hana Šimková; Andrea Pedrosa-Harand; Andreas Houben
Journal:  Proc Natl Acad Sci U S A       Date:  2015-10-21       Impact factor: 11.205

5.  Holokinetic drive: centromere drive in chromosomes without centromeres.

Authors:  Petr Bureš; František Zedek
Journal:  Evolution       Date:  2014-05-22       Impact factor: 3.694

6.  Differential role of CENP-A in the segregation of holocentric C. elegans chromosomes during meiosis and mitosis.

Authors:  Joost Monen; Paul S Maddox; Francie Hyndman; Karen Oegema; Arshad Desai
Journal:  Nat Cell Biol       Date:  2005-11-06       Impact factor: 28.824

7.  Visualization of diffuse centromeres with centromere-specific histone H3 in the holocentric plant Luzula nivea.

Authors:  Kiyotaka Nagaki; Kazunari Kashihara; Minoru Murata
Journal:  Plant Cell       Date:  2005-06-03       Impact factor: 11.277

8.  Recognition of A. thaliana centromeres by heterologous CENH3 requires high similarity to the endogenous protein.

Authors:  Izabel C R Moraes; Inna Lermontova; Ingo Schubert
Journal:  Plant Mol Biol       Date:  2010-12-29       Impact factor: 4.076

9.  The CentO satellite confers translational and rotational phasing on cenH3 nucleosomes in rice centromeres.

Authors:  Tao Zhang; Paul B Talbert; Wenli Zhang; Yufeng Wu; Zujun Yang; Jorja G Henikoff; Steven Henikoff; Jiming Jiang
Journal:  Proc Natl Acad Sci U S A       Date:  2013-11-04       Impact factor: 11.205

10.  Stretching the rules: monocentric chromosomes with multiple centromere domains.

Authors:  Pavel Neumann; Alice Navrátilová; Elizabeth Schroeder-Reiter; Andrea Koblížková; Veronika Steinbauerová; Eva Chocholová; Petr Novák; Gerhard Wanner; Jiří Macas
Journal:  PLoS Genet       Date:  2012-06-21       Impact factor: 5.917

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  13 in total

1.  Evolution of genome size and genomic GC content in carnivorous holokinetics (Droseraceae).

Authors:  Adam Veleba; Petr Šmarda; František Zedek; Lucie Horová; Jakub Šmerda; Petr Bureš
Journal:  Ann Bot       Date:  2016-12-26       Impact factor: 4.357

2.  Endopolyploidy is a common response to UV-B stress in natural plant populations, but its magnitude may be affected by chromosome type.

Authors:  František Zedek; Klára Plačková; Pavel Veselý; Jakub Šmerda; Petr Šmarda; Lucie Horová; Petr Bureš
Journal:  Ann Bot       Date:  2020-10-06       Impact factor: 4.357

Review 3.  Centromeres Drive a Hard Bargain.

Authors:  Leah F Rosin; Barbara G Mellone
Journal:  Trends Genet       Date:  2017-01-07       Impact factor: 11.639

4.  Holocentric chromosomes: from tolerance to fragmentation to colonization of the land.

Authors:  František Zedek; Petr Bureš
Journal:  Ann Bot       Date:  2018-01-25       Impact factor: 4.357

5.  Recurrent but Short-Lived Duplications of Centromeric Proteins in Holocentric Caenorhabditis Species.

Authors:  Lews Caro; Pravrutha Raman; Florian A Steiner; Michael Ailion; Harmit S Malik
Journal:  Mol Biol Evol       Date:  2022-10-07       Impact factor: 8.800

Review 6.  Satellite DNA: An Evolving Topic.

Authors:  Manuel A Garrido-Ramos
Journal:  Genes (Basel)       Date:  2017-09-18       Impact factor: 4.096

7.  Chromosome numbers of Carex (Cyperaceae) and their taxonomic implications.

Authors:  Helena Więcław; Anna Kalinka; Jacob Koopman
Journal:  PLoS One       Date:  2020-02-10       Impact factor: 3.240

Review 8.  The cellular mechanisms and consequences of centromere drive.

Authors:  Lisa E Kursel; Harmit S Malik
Journal:  Curr Opin Cell Biol       Date:  2018-02-16       Impact factor: 8.382

9.  CenH3 evolution reflects meiotic symmetry as predicted by the centromere drive model.

Authors:  František Zedek; Petr Bureš
Journal:  Sci Rep       Date:  2016-09-15       Impact factor: 4.379

10.  Holocentric chromosomes.

Authors:  Mauro Mandrioli; Gian Carlo Manicardi
Journal:  PLoS Genet       Date:  2020-07-30       Impact factor: 5.917

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