Targeted interactomics reveals a complex core cell cycle machinery in Arabidopsis thaliana

Abstract Cell proliferation is the main driving force for plant growth. Although genome sequence analysis revealed a high number of cell cycle genes in plants, little is known about the molecular complexes steering cell division. In a targeted proteomics approach, we mapped the core complex machiner...

Full description

Saved in:
Bibliographic Details
Main Authors: Jelle Van Leene, Jens Hollunder, Dominique Eeckhout, Geert Persiau, Eveline Van De Slijke, Hilde Stals, Gert Van Isterdael, Aurine Verkest, Sandy Neirynck, Yelle Buffel, Stefanie De Bodt, Steven Maere, Kris Laukens, Anne Pharazyn, Paulo C G Ferreira, Nubia Eloy, Charlotte Renne, Christian Meyer, Jean‐Denis Faure, Jens Steinbrenner, Jim Beynon, John C Larkin, Yves Van de Peer, Pierre Hilson, Martin Kuiper, Lieven De Veylder, Harry Van Onckelen, Dirk Inzé, Erwin Witters, Geert De Jaeger
Format: Article
Language:English
Published: Springer Nature 2010-08-01
Series:Molecular Systems Biology
Subjects:
Online Access:https://doi.org/10.1038/msb.2010.53
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849225785639960576
author Jelle Van Leene
Jens Hollunder
Dominique Eeckhout
Geert Persiau
Eveline Van De Slijke
Hilde Stals
Gert Van Isterdael
Aurine Verkest
Sandy Neirynck
Yelle Buffel
Stefanie De Bodt
Steven Maere
Kris Laukens
Anne Pharazyn
Paulo C G Ferreira
Nubia Eloy
Charlotte Renne
Christian Meyer
Jean‐Denis Faure
Jens Steinbrenner
Jim Beynon
John C Larkin
Yves Van de Peer
Pierre Hilson
Martin Kuiper
Lieven De Veylder
Harry Van Onckelen
Dirk Inzé
Erwin Witters
Geert De Jaeger
author_facet Jelle Van Leene
Jens Hollunder
Dominique Eeckhout
Geert Persiau
Eveline Van De Slijke
Hilde Stals
Gert Van Isterdael
Aurine Verkest
Sandy Neirynck
Yelle Buffel
Stefanie De Bodt
Steven Maere
Kris Laukens
Anne Pharazyn
Paulo C G Ferreira
Nubia Eloy
Charlotte Renne
Christian Meyer
Jean‐Denis Faure
Jens Steinbrenner
Jim Beynon
John C Larkin
Yves Van de Peer
Pierre Hilson
Martin Kuiper
Lieven De Veylder
Harry Van Onckelen
Dirk Inzé
Erwin Witters
Geert De Jaeger
author_sort Jelle Van Leene
collection DOAJ
description Abstract Cell proliferation is the main driving force for plant growth. Although genome sequence analysis revealed a high number of cell cycle genes in plants, little is known about the molecular complexes steering cell division. In a targeted proteomics approach, we mapped the core complex machinery at the heart of the Arabidopsis thaliana cell cycle control. Besides a central regulatory network of core complexes, we distinguished a peripheral network that links the core machinery to up‐ and downstream pathways. Over 100 new candidate cell cycle proteins were predicted and an in‐depth biological interpretation demonstrated the hypothesis‐generating power of the interaction data. The data set provided a comprehensive view on heterodimeric cyclin‐dependent kinase (CDK)–cyclin complexes in plants. For the first time, inhibitory proteins of plant‐specific B‐type CDKs were discovered and the anaphase‐promoting complex was characterized and extended. Important conclusions were that mitotic A‐ and B‐type cyclins form complexes with the plant‐specific B‐type CDKs and not with CDKA;1, and that D‐type cyclins and S‐phase‐specific A‐type cyclins seem to be associated exclusively with CDKA;1. Furthermore, we could show that plants have evolved a combinatorial toolkit consisting of at least 92 different CDK–cyclin complex variants, which strongly underscores the functional diversification among the large family of cyclins and reflects the pivotal role of cell cycle regulation in the developmental plasticity of plants.
format Article
id doaj-art-ac7a8f0b60cd4d878f9bc09568d11dc5
institution Kabale University
issn 1744-4292
language English
publishDate 2010-08-01
publisher Springer Nature
record_format Article
series Molecular Systems Biology
spelling doaj-art-ac7a8f0b60cd4d878f9bc09568d11dc52025-08-24T12:00:27ZengSpringer NatureMolecular Systems Biology1744-42922010-08-016111210.1038/msb.2010.53Targeted interactomics reveals a complex core cell cycle machinery in Arabidopsis thalianaJelle Van Leene0Jens Hollunder1Dominique Eeckhout2Geert Persiau3Eveline Van De Slijke4Hilde Stals5Gert Van Isterdael6Aurine Verkest7Sandy Neirynck8Yelle Buffel9Stefanie De Bodt10Steven Maere11Kris Laukens12Anne Pharazyn13Paulo C G Ferreira14Nubia Eloy15Charlotte Renne16Christian Meyer17Jean‐Denis Faure18Jens Steinbrenner19Jim Beynon20John C Larkin21Yves Van de Peer22Pierre Hilson23Martin Kuiper24Lieven De Veylder25Harry Van Onckelen26Dirk Inzé27Erwin Witters28Geert De Jaeger29Department of Plant Systems BiologyDepartment of Plant Systems BiologyDepartment of Plant Systems BiologyDepartment of Plant Systems BiologyDepartment of Plant Systems BiologyDepartment of Plant Systems BiologyDepartment of Plant Systems BiologyDepartment of Plant Systems BiologyDepartment of Plant Systems BiologyDepartment of Plant Systems BiologyDepartment of Plant Systems BiologyDepartment of Plant Systems BiologyDepartment of Mathematics and Computer Science, University of AntwerpDepartment of Biology, Center for Proteome Analysis and Mass Spectrometry, University of AntwerpInstituto de Bioquímica Médica, Centro de Ciências da Saúde, Universidade Federal do Rio de JaneiroDepartment of Plant Systems BiologyInstitut Jean‐Pierre Bourgin, INRA‐AgroParisTechInstitut Jean‐Pierre Bourgin, INRA‐AgroParisTechInstitut Jean‐Pierre Bourgin, INRA‐AgroParisTechSchool of Life Sciences, Warwick UniversitySchool of Life Sciences, Warwick UniversityDepartment of Biological Sciences, Louisiana State UniversityDepartment of Plant Systems BiologyDepartment of Plant Systems BiologyDepartment of Plant Systems BiologyDepartment of Plant Systems BiologyDepartment of Biology, Center for Proteome Analysis and Mass Spectrometry, University of AntwerpDepartment of Plant Systems BiologyDepartment of Biology, Center for Proteome Analysis and Mass Spectrometry, University of AntwerpDepartment of Plant Systems BiologyAbstract Cell proliferation is the main driving force for plant growth. Although genome sequence analysis revealed a high number of cell cycle genes in plants, little is known about the molecular complexes steering cell division. In a targeted proteomics approach, we mapped the core complex machinery at the heart of the Arabidopsis thaliana cell cycle control. Besides a central regulatory network of core complexes, we distinguished a peripheral network that links the core machinery to up‐ and downstream pathways. Over 100 new candidate cell cycle proteins were predicted and an in‐depth biological interpretation demonstrated the hypothesis‐generating power of the interaction data. The data set provided a comprehensive view on heterodimeric cyclin‐dependent kinase (CDK)–cyclin complexes in plants. For the first time, inhibitory proteins of plant‐specific B‐type CDKs were discovered and the anaphase‐promoting complex was characterized and extended. Important conclusions were that mitotic A‐ and B‐type cyclins form complexes with the plant‐specific B‐type CDKs and not with CDKA;1, and that D‐type cyclins and S‐phase‐specific A‐type cyclins seem to be associated exclusively with CDKA;1. Furthermore, we could show that plants have evolved a combinatorial toolkit consisting of at least 92 different CDK–cyclin complex variants, which strongly underscores the functional diversification among the large family of cyclins and reflects the pivotal role of cell cycle regulation in the developmental plasticity of plants.https://doi.org/10.1038/msb.2010.53Arabidopsis thalianacell cycleinteractomeprotein complexprotein interactions
spellingShingle Jelle Van Leene
Jens Hollunder
Dominique Eeckhout
Geert Persiau
Eveline Van De Slijke
Hilde Stals
Gert Van Isterdael
Aurine Verkest
Sandy Neirynck
Yelle Buffel
Stefanie De Bodt
Steven Maere
Kris Laukens
Anne Pharazyn
Paulo C G Ferreira
Nubia Eloy
Charlotte Renne
Christian Meyer
Jean‐Denis Faure
Jens Steinbrenner
Jim Beynon
John C Larkin
Yves Van de Peer
Pierre Hilson
Martin Kuiper
Lieven De Veylder
Harry Van Onckelen
Dirk Inzé
Erwin Witters
Geert De Jaeger
Targeted interactomics reveals a complex core cell cycle machinery in Arabidopsis thaliana
Molecular Systems Biology
Arabidopsis thaliana
cell cycle
interactome
protein complex
protein interactions
title Targeted interactomics reveals a complex core cell cycle machinery in Arabidopsis thaliana
title_full Targeted interactomics reveals a complex core cell cycle machinery in Arabidopsis thaliana
title_fullStr Targeted interactomics reveals a complex core cell cycle machinery in Arabidopsis thaliana
title_full_unstemmed Targeted interactomics reveals a complex core cell cycle machinery in Arabidopsis thaliana
title_short Targeted interactomics reveals a complex core cell cycle machinery in Arabidopsis thaliana
title_sort targeted interactomics reveals a complex core cell cycle machinery in arabidopsis thaliana
topic Arabidopsis thaliana
cell cycle
interactome
protein complex
protein interactions
url https://doi.org/10.1038/msb.2010.53
work_keys_str_mv AT jellevanleene targetedinteractomicsrevealsacomplexcorecellcyclemachineryinarabidopsisthaliana
AT jenshollunder targetedinteractomicsrevealsacomplexcorecellcyclemachineryinarabidopsisthaliana
AT dominiqueeeckhout targetedinteractomicsrevealsacomplexcorecellcyclemachineryinarabidopsisthaliana
AT geertpersiau targetedinteractomicsrevealsacomplexcorecellcyclemachineryinarabidopsisthaliana
AT evelinevandeslijke targetedinteractomicsrevealsacomplexcorecellcyclemachineryinarabidopsisthaliana
AT hildestals targetedinteractomicsrevealsacomplexcorecellcyclemachineryinarabidopsisthaliana
AT gertvanisterdael targetedinteractomicsrevealsacomplexcorecellcyclemachineryinarabidopsisthaliana
AT aurineverkest targetedinteractomicsrevealsacomplexcorecellcyclemachineryinarabidopsisthaliana
AT sandyneirynck targetedinteractomicsrevealsacomplexcorecellcyclemachineryinarabidopsisthaliana
AT yellebuffel targetedinteractomicsrevealsacomplexcorecellcyclemachineryinarabidopsisthaliana
AT stefaniedebodt targetedinteractomicsrevealsacomplexcorecellcyclemachineryinarabidopsisthaliana
AT stevenmaere targetedinteractomicsrevealsacomplexcorecellcyclemachineryinarabidopsisthaliana
AT krislaukens targetedinteractomicsrevealsacomplexcorecellcyclemachineryinarabidopsisthaliana
AT annepharazyn targetedinteractomicsrevealsacomplexcorecellcyclemachineryinarabidopsisthaliana
AT paulocgferreira targetedinteractomicsrevealsacomplexcorecellcyclemachineryinarabidopsisthaliana
AT nubiaeloy targetedinteractomicsrevealsacomplexcorecellcyclemachineryinarabidopsisthaliana
AT charlotterenne targetedinteractomicsrevealsacomplexcorecellcyclemachineryinarabidopsisthaliana
AT christianmeyer targetedinteractomicsrevealsacomplexcorecellcyclemachineryinarabidopsisthaliana
AT jeandenisfaure targetedinteractomicsrevealsacomplexcorecellcyclemachineryinarabidopsisthaliana
AT jenssteinbrenner targetedinteractomicsrevealsacomplexcorecellcyclemachineryinarabidopsisthaliana
AT jimbeynon targetedinteractomicsrevealsacomplexcorecellcyclemachineryinarabidopsisthaliana
AT johnclarkin targetedinteractomicsrevealsacomplexcorecellcyclemachineryinarabidopsisthaliana
AT yvesvandepeer targetedinteractomicsrevealsacomplexcorecellcyclemachineryinarabidopsisthaliana
AT pierrehilson targetedinteractomicsrevealsacomplexcorecellcyclemachineryinarabidopsisthaliana
AT martinkuiper targetedinteractomicsrevealsacomplexcorecellcyclemachineryinarabidopsisthaliana
AT lievendeveylder targetedinteractomicsrevealsacomplexcorecellcyclemachineryinarabidopsisthaliana
AT harryvanonckelen targetedinteractomicsrevealsacomplexcorecellcyclemachineryinarabidopsisthaliana
AT dirkinze targetedinteractomicsrevealsacomplexcorecellcyclemachineryinarabidopsisthaliana
AT erwinwitters targetedinteractomicsrevealsacomplexcorecellcyclemachineryinarabidopsisthaliana
AT geertdejaeger targetedinteractomicsrevealsacomplexcorecellcyclemachineryinarabidopsisthaliana