title: Chloroplast dysfunction causes multiple defects in cell cycle progression in the Arabidopsis crumpled leaf mutant.
abstract: The majority of research on cell cycle regulation is focused on the nuclear events that govern the replication and segregation of the genome between the two daughter cells. However, eukaryotic cells contain several compartmentalized organelles with specialized functions, and coordination among these organelles is required for proper cell cycle progression, as evidenced by the isolation of several mutants in which both organelle function and overall plant development were affected. To investigate how chloroplast dysfunction affects the cell cycle, we analyzed the crumpled leaf (crl) mutant of Arabidopsis (Arabidopsis thaliana), which is deficient for a chloroplastic protein and displays particularly severe developmental defects. In the crl mutant, we reveal that cell cycle regulation is altered drastically and that meristematic cells prematurely enter differentiation, leading to reduced plant stature and early endoreduplication in the leaves. This response is due to the repression of several key cell cycle regulators as well as constitutive activation of stress-response genes, among them the cell cycle inhibitor SIAMESE-RELATED5. One unique feature of the crl mutant is that it produces aplastidic cells in several organs, including the root tip. By investigating the consequence of the absence of plastids on cell cycle progression, we showed that nuclear DNA replication occurs in aplastidic cells in the root tip, which opens future research prospects regarding the dialogue between plastids and the nucleus during cell cycle regulation in higher plants.
authors.affiliation: Institut de Biologie des Plantes, Unité Mixte de Recherche 8618 Centre National de la Recherche Scientifique Université-Paris Sud, Laboratoire d'Excellence Saclay Plant Science, bât 630 91405 Orsay, France (E.H., S.D., C.M., C.B., M.Be., C.R.);Division of Biological Science, Graduate School of Science, Nagoya University, Chikusa-ku, Nagoya 464-8602, Japan (Y.Y.);Fédération de Recherche de Gif FRC3115, Pôle de Biologie Cellulaire, 91198 Gif-sur-Yvette, France (M.Bo.);Unité de Recherche en Génomique Végétale, CP5708 Evry, France (L.S.-T.);Department of Plant Systems Biology, Vlaams Instituut voor Biotechnologie, B-9052 Ghent, Belgium (D.Y., L.D.V.);Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (D.Y., L.D.V.);Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7141, Laboratoire de Physiologie Membranaire et Moléculaire du Chloroplaste, Institut de Biologie Physico-Chimique, 75005 Paris, France (S.B.);Department of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences, University of Tokyo, Bunkyo-ku, Tokyo 113-8657, Japan (H.H.); andDivision of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal 23955-6900, Kingdom of Saudi Arabia (M.Be.).
authors.forename: Elodie
authors.initials: E
authors.lastname: Hudik
authors.affiliation: Institut de Biologie des Plantes, Unité Mixte de Recherche 8618 Centre National de la Recherche Scientifique Université-Paris Sud, Laboratoire d'Excellence Saclay Plant Science, bât 630 91405 Orsay, France (E.H., S.D., C.M., C.B., M.Be., C.R.);Division of Biological Science, Graduate School of Science, Nagoya University, Chikusa-ku, Nagoya 464-8602, Japan (Y.Y.);Fédération de Recherche de Gif FRC3115, Pôle de Biologie Cellulaire, 91198 Gif-sur-Yvette, France (M.Bo.);Unité de Recherche en Génomique Végétale, CP5708 Evry, France (L.S.-T.);Department of Plant Systems Biology, Vlaams Instituut voor Biotechnologie, B-9052 Ghent, Belgium (D.Y., L.D.V.);Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (D.Y., L.D.V.);Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7141, Laboratoire de Physiologie Membranaire et Moléculaire du Chloroplaste, Institut de Biologie Physico-Chimique, 75005 Paris, France (S.B.);Department of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences, University of Tokyo, Bunkyo-ku, Tokyo 113-8657, Japan (H.H.); andDivision of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal 23955-6900, Kingdom of Saudi Arabia (M.Be.).
authors.forename: Yasushi
authors.initials: Y
authors.lastname: Yoshioka
authors.affiliation: Institut de Biologie des Plantes, Unité Mixte de Recherche 8618 Centre National de la Recherche Scientifique Université-Paris Sud, Laboratoire d'Excellence Saclay Plant Science, bât 630 91405 Orsay, France (E.H., S.D., C.M., C.B., M.Be., C.R.);Division of Biological Science, Graduate School of Science, Nagoya University, Chikusa-ku, Nagoya 464-8602, Japan (Y.Y.);Fédération de Recherche de Gif FRC3115, Pôle de Biologie Cellulaire, 91198 Gif-sur-Yvette, France (M.Bo.);Unité de Recherche en Génomique Végétale, CP5708 Evry, France (L.S.-T.);Department of Plant Systems Biology, Vlaams Instituut voor Biotechnologie, B-9052 Ghent, Belgium (D.Y., L.D.V.);Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (D.Y., L.D.V.);Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7141, Laboratoire de Physiologie Membranaire et Moléculaire du Chloroplaste, Institut de Biologie Physico-Chimique, 75005 Paris, France (S.B.);Department of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences, University of Tokyo, Bunkyo-ku, Tokyo 113-8657, Japan (H.H.); andDivision of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal 23955-6900, Kingdom of Saudi Arabia (M.Be.).
authors.forename: Séverine
authors.initials: S
authors.lastname: Domenichini
authors.affiliation: Institut de Biologie des Plantes, Unité Mixte de Recherche 8618 Centre National de la Recherche Scientifique Université-Paris Sud, Laboratoire d'Excellence Saclay Plant Science, bât 630 91405 Orsay, France (E.H., S.D., C.M., C.B., M.Be., C.R.);Division of Biological Science, Graduate School of Science, Nagoya University, Chikusa-ku, Nagoya 464-8602, Japan (Y.Y.);Fédération de Recherche de Gif FRC3115, Pôle de Biologie Cellulaire, 91198 Gif-sur-Yvette, France (M.Bo.);Unité de Recherche en Génomique Végétale, CP5708 Evry, France (L.S.-T.);Department of Plant Systems Biology, Vlaams Instituut voor Biotechnologie, B-9052 Ghent, Belgium (D.Y., L.D.V.);Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (D.Y., L.D.V.);Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7141, Laboratoire de Physiologie Membranaire et Moléculaire du Chloroplaste, Institut de Biologie Physico-Chimique, 75005 Paris, France (S.B.);Department of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences, University of Tokyo, Bunkyo-ku, Tokyo 113-8657, Japan (H.H.); andDivision of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal 23955-6900, Kingdom of Saudi Arabia (M.Be.).
authors.forename: Mickaël
authors.initials: M
authors.lastname: Bourge
authors.affiliation: Institut de Biologie des Plantes, Unité Mixte de Recherche 8618 Centre National de la Recherche Scientifique Université-Paris Sud, Laboratoire d'Excellence Saclay Plant Science, bât 630 91405 Orsay, France (E.H., S.D., C.M., C.B., M.Be., C.R.);Division of Biological Science, Graduate School of Science, Nagoya University, Chikusa-ku, Nagoya 464-8602, Japan (Y.Y.);Fédération de Recherche de Gif FRC3115, Pôle de Biologie Cellulaire, 91198 Gif-sur-Yvette, France (M.Bo.);Unité de Recherche en Génomique Végétale, CP5708 Evry, France (L.S.-T.);Department of Plant Systems Biology, Vlaams Instituut voor Biotechnologie, B-9052 Ghent, Belgium (D.Y., L.D.V.);Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (D.Y., L.D.V.);Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7141, Laboratoire de Physiologie Membranaire et Moléculaire du Chloroplaste, Institut de Biologie Physico-Chimique, 75005 Paris, France (S.B.);Department of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences, University of Tokyo, Bunkyo-ku, Tokyo 113-8657, Japan (H.H.); andDivision of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal 23955-6900, Kingdom of Saudi Arabia (M.Be.).
authors.forename: Ludivine
authors.initials: L
authors.lastname: Soubigout-Taconnat
authors.affiliation: Institut de Biologie des Plantes, Unité Mixte de Recherche 8618 Centre National de la Recherche Scientifique Université-Paris Sud, Laboratoire d'Excellence Saclay Plant Science, bât 630 91405 Orsay, France (E.H., S.D., C.M., C.B., M.Be., C.R.);Division of Biological Science, Graduate School of Science, Nagoya University, Chikusa-ku, Nagoya 464-8602, Japan (Y.Y.);Fédération de Recherche de Gif FRC3115, Pôle de Biologie Cellulaire, 91198 Gif-sur-Yvette, France (M.Bo.);Unité de Recherche en Génomique Végétale, CP5708 Evry, France (L.S.-T.);Department of Plant Systems Biology, Vlaams Instituut voor Biotechnologie, B-9052 Ghent, Belgium (D.Y., L.D.V.);Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (D.Y., L.D.V.);Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7141, Laboratoire de Physiologie Membranaire et Moléculaire du Chloroplaste, Institut de Biologie Physico-Chimique, 75005 Paris, France (S.B.);Department of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences, University of Tokyo, Bunkyo-ku, Tokyo 113-8657, Japan (H.H.); andDivision of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal 23955-6900, Kingdom of Saudi Arabia (M.Be.).
authors.forename: Christelle
authors.initials: C
authors.lastname: Mazubert
authors.affiliation: Institut de Biologie des Plantes, Unité Mixte de Recherche 8618 Centre National de la Recherche Scientifique Université-Paris Sud, Laboratoire d'Excellence Saclay Plant Science, bât 630 91405 Orsay, France (E.H., S.D., C.M., C.B., M.Be., C.R.);Division of Biological Science, Graduate School of Science, Nagoya University, Chikusa-ku, Nagoya 464-8602, Japan (Y.Y.);Fédération de Recherche de Gif FRC3115, Pôle de Biologie Cellulaire, 91198 Gif-sur-Yvette, France (M.Bo.);Unité de Recherche en Génomique Végétale, CP5708 Evry, France (L.S.-T.);Department of Plant Systems Biology, Vlaams Instituut voor Biotechnologie, B-9052 Ghent, Belgium (D.Y., L.D.V.);Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (D.Y., L.D.V.);Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7141, Laboratoire de Physiologie Membranaire et Moléculaire du Chloroplaste, Institut de Biologie Physico-Chimique, 75005 Paris, France (S.B.);Department of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences, University of Tokyo, Bunkyo-ku, Tokyo 113-8657, Japan (H.H.); andDivision of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal 23955-6900, Kingdom of Saudi Arabia (M.Be.).
authors.forename: Dalong
authors.initials: D
authors.lastname: Yi
authors.affiliation: Institut de Biologie des Plantes, Unité Mixte de Recherche 8618 Centre National de la Recherche Scientifique Université-Paris Sud, Laboratoire d'Excellence Saclay Plant Science, bât 630 91405 Orsay, France (E.H., S.D., C.M., C.B., M.Be., C.R.);Division of Biological Science, Graduate School of Science, Nagoya University, Chikusa-ku, Nagoya 464-8602, Japan (Y.Y.);Fédération de Recherche de Gif FRC3115, Pôle de Biologie Cellulaire, 91198 Gif-sur-Yvette, France (M.Bo.);Unité de Recherche en Génomique Végétale, CP5708 Evry, France (L.S.-T.);Department of Plant Systems Biology, Vlaams Instituut voor Biotechnologie, B-9052 Ghent, Belgium (D.Y., L.D.V.);Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (D.Y., L.D.V.);Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7141, Laboratoire de Physiologie Membranaire et Moléculaire du Chloroplaste, Institut de Biologie Physico-Chimique, 75005 Paris, France (S.B.);Department of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences, University of Tokyo, Bunkyo-ku, Tokyo 113-8657, Japan (H.H.); andDivision of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal 23955-6900, Kingdom of Saudi Arabia (M.Be.).
authors.forename: Sandrine
authors.initials: S
authors.lastname: Bujaldon
authors.affiliation: Institut de Biologie des Plantes, Unité Mixte de Recherche 8618 Centre National de la Recherche Scientifique Université-Paris Sud, Laboratoire d'Excellence Saclay Plant Science, bât 630 91405 Orsay, France (E.H., S.D., C.M., C.B., M.Be., C.R.);Division of Biological Science, Graduate School of Science, Nagoya University, Chikusa-ku, Nagoya 464-8602, Japan (Y.Y.);Fédération de Recherche de Gif FRC3115, Pôle de Biologie Cellulaire, 91198 Gif-sur-Yvette, France (M.Bo.);Unité de Recherche en Génomique Végétale, CP5708 Evry, France (L.S.-T.);Department of Plant Systems Biology, Vlaams Instituut voor Biotechnologie, B-9052 Ghent, Belgium (D.Y., L.D.V.);Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (D.Y., L.D.V.);Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7141, Laboratoire de Physiologie Membranaire et Moléculaire du Chloroplaste, Institut de Biologie Physico-Chimique, 75005 Paris, France (S.B.);Department of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences, University of Tokyo, Bunkyo-ku, Tokyo 113-8657, Japan (H.H.); andDivision of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal 23955-6900, Kingdom of Saudi Arabia (M.Be.).
authors.forename: Hiroyuki
authors.initials: H
authors.lastname: Hayashi
authors.affiliation: Institut de Biologie des Plantes, Unité Mixte de Recherche 8618 Centre National de la Recherche Scientifique Université-Paris Sud, Laboratoire d'Excellence Saclay Plant Science, bât 630 91405 Orsay, France (E.H., S.D., C.M., C.B., M.Be., C.R.);Division of Biological Science, Graduate School of Science, Nagoya University, Chikusa-ku, Nagoya 464-8602, Japan (Y.Y.);Fédération de Recherche de Gif FRC3115, Pôle de Biologie Cellulaire, 91198 Gif-sur-Yvette, France (M.Bo.);Unité de Recherche en Génomique Végétale, CP5708 Evry, France (L.S.-T.);Department of Plant Systems Biology, Vlaams Instituut voor Biotechnologie, B-9052 Ghent, Belgium (D.Y., L.D.V.);Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (D.Y., L.D.V.);Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7141, Laboratoire de Physiologie Membranaire et Moléculaire du Chloroplaste, Institut de Biologie Physico-Chimique, 75005 Paris, France (S.B.);Department of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences, University of Tokyo, Bunkyo-ku, Tokyo 113-8657, Japan (H.H.); andDivision of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal 23955-6900, Kingdom of Saudi Arabia (M.Be.).
authors.forename: Lieven
authors.initials: L
authors.lastname: De Veylder
authors.affiliation: Institut de Biologie des Plantes, Unité Mixte de Recherche 8618 Centre National de la Recherche Scientifique Université-Paris Sud, Laboratoire d'Excellence Saclay Plant Science, bât 630 91405 Orsay, France (E.H., S.D., C.M., C.B., M.Be., C.R.);Division of Biological Science, Graduate School of Science, Nagoya University, Chikusa-ku, Nagoya 464-8602, Japan (Y.Y.);Fédération de Recherche de Gif FRC3115, Pôle de Biologie Cellulaire, 91198 Gif-sur-Yvette, France (M.Bo.);Unité de Recherche en Génomique Végétale, CP5708 Evry, France (L.S.-T.);Department of Plant Systems Biology, Vlaams Instituut voor Biotechnologie, B-9052 Ghent, Belgium (D.Y., L.D.V.);Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (D.Y., L.D.V.);Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7141, Laboratoire de Physiologie Membranaire et Moléculaire du Chloroplaste, Institut de Biologie Physico-Chimique, 75005 Paris, France (S.B.);Department of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences, University of Tokyo, Bunkyo-ku, Tokyo 113-8657, Japan (H.H.); andDivision of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal 23955-6900, Kingdom of Saudi Arabia (M.Be.).
authors.forename: Catherine
authors.initials: C
authors.lastname: Bergounioux
authors.affiliation: Institut de Biologie des Plantes, Unité Mixte de Recherche 8618 Centre National de la Recherche Scientifique Université-Paris Sud, Laboratoire d'Excellence Saclay Plant Science, bât 630 91405 Orsay, France (E.H., S.D., C.M., C.B., M.Be., C.R.);Division of Biological Science, Graduate School of Science, Nagoya University, Chikusa-ku, Nagoya 464-8602, Japan (Y.Y.);Fédération de Recherche de Gif FRC3115, Pôle de Biologie Cellulaire, 91198 Gif-sur-Yvette, France (M.Bo.);Unité de Recherche en Génomique Végétale, CP5708 Evry, France (L.S.-T.);Department of Plant Systems Biology, Vlaams Instituut voor Biotechnologie, B-9052 Ghent, Belgium (D.Y., L.D.V.);Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (D.Y., L.D.V.);Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7141, Laboratoire de Physiologie Membranaire et Moléculaire du Chloroplaste, Institut de Biologie Physico-Chimique, 75005 Paris, France (S.B.);Department of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences, University of Tokyo, Bunkyo-ku, Tokyo 113-8657, Japan (H.H.); andDivision of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal 23955-6900, Kingdom of Saudi Arabia (M.Be.).
authors.forename: Moussa
authors.initials: M
authors.lastname: Benhamed
authors.affiliation: Institut de Biologie des Plantes, Unité Mixte de Recherche 8618 Centre National de la Recherche Scientifique Université-Paris Sud, Laboratoire d'Excellence Saclay Plant Science, bât 630 91405 Orsay, France (E.H., S.D., C.M., C.B., M.Be., C.R.);Division of Biological Science, Graduate School of Science, Nagoya University, Chikusa-ku, Nagoya 464-8602, Japan (Y.Y.);Fédération de Recherche de Gif FRC3115, Pôle de Biologie Cellulaire, 91198 Gif-sur-Yvette, France (M.Bo.);Unité de Recherche en Génomique Végétale, CP5708 Evry, France (L.S.-T.);Department of Plant Systems Biology, Vlaams Instituut voor Biotechnologie, B-9052 Ghent, Belgium (D.Y., L.D.V.);Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (D.Y., L.D.V.);Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7141, Laboratoire de Physiologie Membranaire et Moléculaire du Chloroplaste, Institut de Biologie Physico-Chimique, 75005 Paris, France (S.B.);Department of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences, University of Tokyo, Bunkyo-ku, Tokyo 113-8657, Japan (H.H.); andDivision of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal 23955-6900, Kingdom of Saudi Arabia (M.Be.) cecile.raynaud@u-psud.fr.
authors.forename: Cécile
authors.initials: C
authors.lastname: Raynaud
mesh_terms: D017360:Arabidopsis / Q000502:physiology*; D029681:Arabidopsis Proteins / Q000378:metabolism / Q000502:physiology*; D002453:Cell Cycle; D018797:Cell Cycle Proteins / Q000378:metabolism; D002454:Cell Differentiation; D049109:Cell Proliferation; D002736:Chloroplasts / Q000502:physiology*; D016213:Cyclins / Q000378:metabolism; D018506:Gene Expression Regulation, Plant
chemical_list: D029681:Arabidopsis Proteins; C486919:CRUMPLED LEAF protein, Arabidopsis; D018797:Cell Cycle Proteins; C496944:CycD3 protein, Arabidopsis; D016213:Cyclins; C000592968:SMR5 protein, Arabidopsis