Identification of Arabidopsis meiotic cyclins reveals functional diversification among plant cyclin genes.

Meiosis is a modified cell division in which a single S-phase is followed by two rounds of chromosome segregation resulting in the production of haploid gametes. The meiotic mode of chromosome segregation requires extensive remodeling of the basic cell cycle machinery and employment of unique regula...

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Main Authors: Petra Bulankova, Svetlana Akimcheva, Nicole Fellner, Karel Riha
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2013-05-01
Series:PLoS Genetics
Online Access:https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1003508&type=printable
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author Petra Bulankova
Svetlana Akimcheva
Nicole Fellner
Karel Riha
author_facet Petra Bulankova
Svetlana Akimcheva
Nicole Fellner
Karel Riha
author_sort Petra Bulankova
collection DOAJ
description Meiosis is a modified cell division in which a single S-phase is followed by two rounds of chromosome segregation resulting in the production of haploid gametes. The meiotic mode of chromosome segregation requires extensive remodeling of the basic cell cycle machinery and employment of unique regulatory mechanisms. Cyclin-dependent kinases (CDKs) and cyclins represent an ancient molecular module that drives and regulates cell cycle progression. The cyclin gene family has undergone a massive expansion in angiosperm plants, but only a few cyclins were thoroughly characterized. In this study we performed a systematic immunolocalization screen to identify Arabidopsis thaliana A- and B-type cyclins expressed in meiosis. Many of these cyclins exhibit cell-type-specific expression in vegetative tissues and distinct subcellular localization. We found six A-type cyclins and a single B-type cyclin (CYCB3;1) to be expressed in male meiosis. Mutant analysis revealed that these cyclins contribute to distinct meiosis-related processes. While A2 cyclins are important for chromosome segregation, CYCB3;1 prevents ectopic cell wall formation. We further show that cyclin SDS does not contain a D-box and is constitutively expressed throughout meiosis. Analysis of plants carrying cyclin SDS with an introduced D-box motif determined that, in addition to its function in recombination, SDS acts together with CYCB3;1 in suppressing unscheduled cell wall synthesis. Our phenotypic and expression data provide extensive evidence that multiplication of cyclins is in plants accompanied by functional diversification.
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publishDate 2013-05-01
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spelling doaj-art-85c3fcc86a574244acdf13e590b668b22025-08-20T03:10:39ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042013-05-0195e100350810.1371/journal.pgen.1003508Identification of Arabidopsis meiotic cyclins reveals functional diversification among plant cyclin genes.Petra BulankovaSvetlana AkimchevaNicole FellnerKarel RihaMeiosis is a modified cell division in which a single S-phase is followed by two rounds of chromosome segregation resulting in the production of haploid gametes. The meiotic mode of chromosome segregation requires extensive remodeling of the basic cell cycle machinery and employment of unique regulatory mechanisms. Cyclin-dependent kinases (CDKs) and cyclins represent an ancient molecular module that drives and regulates cell cycle progression. The cyclin gene family has undergone a massive expansion in angiosperm plants, but only a few cyclins were thoroughly characterized. In this study we performed a systematic immunolocalization screen to identify Arabidopsis thaliana A- and B-type cyclins expressed in meiosis. Many of these cyclins exhibit cell-type-specific expression in vegetative tissues and distinct subcellular localization. We found six A-type cyclins and a single B-type cyclin (CYCB3;1) to be expressed in male meiosis. Mutant analysis revealed that these cyclins contribute to distinct meiosis-related processes. While A2 cyclins are important for chromosome segregation, CYCB3;1 prevents ectopic cell wall formation. We further show that cyclin SDS does not contain a D-box and is constitutively expressed throughout meiosis. Analysis of plants carrying cyclin SDS with an introduced D-box motif determined that, in addition to its function in recombination, SDS acts together with CYCB3;1 in suppressing unscheduled cell wall synthesis. Our phenotypic and expression data provide extensive evidence that multiplication of cyclins is in plants accompanied by functional diversification.https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1003508&type=printable
spellingShingle Petra Bulankova
Svetlana Akimcheva
Nicole Fellner
Karel Riha
Identification of Arabidopsis meiotic cyclins reveals functional diversification among plant cyclin genes.
PLoS Genetics
title Identification of Arabidopsis meiotic cyclins reveals functional diversification among plant cyclin genes.
title_full Identification of Arabidopsis meiotic cyclins reveals functional diversification among plant cyclin genes.
title_fullStr Identification of Arabidopsis meiotic cyclins reveals functional diversification among plant cyclin genes.
title_full_unstemmed Identification of Arabidopsis meiotic cyclins reveals functional diversification among plant cyclin genes.
title_short Identification of Arabidopsis meiotic cyclins reveals functional diversification among plant cyclin genes.
title_sort identification of arabidopsis meiotic cyclins reveals functional diversification among plant cyclin genes
url https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1003508&type=printable
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AT svetlanaakimcheva identificationofarabidopsismeioticcyclinsrevealsfunctionaldiversificationamongplantcyclingenes
AT nicolefellner identificationofarabidopsismeioticcyclinsrevealsfunctionaldiversificationamongplantcyclingenes
AT karelriha identificationofarabidopsismeioticcyclinsrevealsfunctionaldiversificationamongplantcyclingenes