A Microbial Avenue to Cell Cycle Control in the Plant Superkingdom[C][W][OPEN]

A genetic screen in the green alga Chlamydomonas reinhardtii has molecularly identified >50 temperature-sensitive mutations in genes required for cell division. Most have homologs in land plants. The cyclin-dependent kinase CDKA and the plant-specific CDKB have differentiated cell cycle functions. Potential plant-kingdom-specific cell cycle regulators, and genes conserved across eukaryotes, were identified. Research in yeast and animals has resulted in a well-supported consensus model for eukaryotic cell cycle control. The fit of this model to early diverging eukaryotes, such as the plant kingdom, remains unclear. Using the green alga Chlamydomonas reinhardtii, we developed an efficient pipeline, incorporating robotics, semiautomated image analysis, and deep sequencing, to molecularly identify >50 genes, mostly conserved in higher plants, specifically required for cell division but not cell growth. Mutated genes include the cyclin-dependent kinases CDKA (resembling yeast and animal Cdk1) and the plant-specific CDKB. The Chlamydomonas cell cycle consists of a long G1 during which cells can grow >10-fold, followed by multiple rapid cycles of DNA replication and segregation. CDKA and CDKB execute nonoverlapping functions: CDKA promotes transition between G1 and entry into the division cycle, while CDKB is essential specifically for spindle formation and nuclear division, but not for DNA replication, once CDKA-dependent initiation has occurred. The anaphase-promoting complex is required for similar steps in the Chlamydomonas cell cycle as in Opisthokonts; however, the spindle assembly checkpoint, which targets the APC in Opisthokonts, appears severely attenuated in Chlamydomonas, based on analysis of mutants affecting microtubule function. This approach allows unbiased integration of the consensus cell cycle control model with innovations specific to the plant lineage.

• Publication year

  2014

• Venue

  The Plant Cell

• Publication date

  2014-10-01

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1105/tpc.114.129312PMID 25336509PMCID PMC4247570
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Revisiting the Evolutionary History and Roles of Protein Phosphatases with Kelch-Like Domains in Plants1[C][W]

  2014cited by this paper
• The Cell Cycle: Principles of Control

  2014cited by this paper
• Site‐specific basal body duplication in Chlamydomonas

  2014cited by this paper
• Whole Genome Sequencing Identifies a Deletion in Protein Phosphatase 2A That Affects Its Stability and Localization in Chlamydomonas reinhardtii

  2013cited by this paper
• Independent Localization of Plasma Membrane and Chloroplast Components during Eyespot Assembly

  2013cited by this paper
• Structural characterization of the cyclin-dependent protein kinase family.

  2013cited by this paper
• Fast gapped-read alignment with Bowtie 2

  2012influential reference
• Rare allele of OsPPKL1 associated with grain length causes extra-large grain and a significant yield increase in rice

  2012cited by this paper
• A General G1/S-Phase Cell-Cycle Control Module in the Flowering Plant Arabidopsis thaliana

  2012cited by this paper
• Genetic framework of cyclin-dependent kinase function in Arabidopsis.

  2012influential reference
• Molecular control and function of endoreplication in development and physiology.

  2011cited by this paper
• GIGAS CELL1, a Novel Negative Regulator of the Anaphase-Promoting Complex/Cyclosome, Is Required for Proper Mitotic Progression and Cell Fate Determination in Arabidopsis[W]

  2011cited by this paper
• Evolution of networks and sequences in eukaryotic cell cycle control

  2011cited by this paper
• Centrioles are freed from cilia by severing prior to mitosis

  2010cited by this paper
• Regulation of the Chlamydomonas Cell Cycle by a Stable, Chromatin-Associated Retinoblastoma Tumor Suppressor Complex[W]

  2010influential reference
• The metazoan Mediator co-activator complex as an integrative hub for transcriptional regulation

  2010cited by this paper
• Brassinosteroid signal transduction from receptor kinases to transcription factors.

  2010cited by this paper
• Control of Cell Proliferation, Organ Growth, and DNA Damage Response Operate Independently of Dephosphorylation of the Arabidopsis Cdk1 Homolog CDKA;1[C][W]

  2009cited by this paper
• The Sequence Alignment/Map format and SAMtools

  2009cited by this paper
• Arabidopsis DUO POLLEN3 Is a Key Regulator of Male Germline Development and Embryogenesis[C][W]

  2009cited by this paper
• Phosducin-Like Protein 3 Is Required for Microtubule-Dependent Steps of Cell Division but Not for Meristem Growth in Arabidopsis[W][OA]

  2008cited by this paper
• The Uni2 phosphoprotein is a cell cycle regulated component of the basal body maturation pathway in Chlamydomonas reinhardtii.

  2008cited by this paper
• The spindle-assembly checkpoint in space and time

  2007influential reference
• The Chlamydomonas Genome Reveals the Evolution of Key Animal and Plant Functions

  2007cited by this paper
• The ins and outs of the plant cell cycle

  2007cited by this paper
• Cell Cycle: Principles of Control

  2007cited by this paper
• The anaphase promoting complex/cyclosome: a machine designed to destroy

  2006cited by this paper
• Microtubule nucleation: gamma-tubulin and beyond.

  2006cited by this paper
• Cell Size Checkpoint Control by the Retinoblastoma Tumor Suppressor Pathway

  2006influential reference
• Microtubule nucleation: γ-tubulin and beyond

  2006cited by this paper
• Preventing re-replication of chromosomal DNA

  2005cited by this paper
• Condensins: organizing and segregating the genome.

  2005cited by this paper
• Polyploidy and genome evolution in plants.

  2005cited by this paper
• Genome-Wide Annotation and Expression Profiling of Cell Cycle Regulatory Genes in Chlamydomonas reinhardtii1[w]

  2005influential reference
• Atypical Regulation of a Green Lineage-Specific B-Type Cyclin-Dependent Kinase1

  2005cited by this paper
• Faculty Opinions recommendation of In vivo analysis of cell division, cell growth, and differentiation at the shoot apical meristem in Arabidopsis.

  2004cited by this paper
• A NIMA-related kinase, Fa2p, localizes to a novel site in the proximal cilia of Chlamydomonas and mouse kidney cells.

  2004cited by this paper
• A dynamic transcriptional network communicates growth potential to ribosome synthesis and critical cell size.

  2004cited by this paper
• In Vivo Analysis of Cell Division, Cell Growth, and Differentiation at the Shoot Apical Meristem in Arabidopsis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.017962.

  2004cited by this paper
• Nuclear protein phosphatases with Kelch-repeat domains modulate the response to brassinosteroids in Arabidopsis.

  2004cited by this paper
• Genome-Wide Analysis of Core Cell Cycle Genes in Arabidopsis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010445.

  2002cited by this paper
• Tubulin folding cofactors: half a dozen for a dimer.

  2002cited by this paper
• Control of cell division by a retinoblastoma protein homolog in Chlamydomonas.

  2001influential reference
• A Plant-specific Cyclin-dependent Kinase Is Involved in the Control of G2/M Progression in Plants*

  2001cited by this paper
• SIAMESE, a gene controlling the endoreduplication cell cycle in Arabidopsis thaliana trichomes.

  2000cited by this paper
• Chlamydomonas Cell Cycle Mutants

  1999cited by this paper
• Pharmacological and genetic evidence for a role of rootlet and phycoplast microtubules in the positioning and assembly of cleavage furrows in Chlamydomonas reinhardtii.

  1998cited by this paper
• The Arabidopsis Cks1At protein binds the cyclin‐dependent kinases Cdc2aAt and Cdc2bAt

  1997cited by this paper
• Saccharomyces cerevisiae G1 cyclins differ in their intrinsic functional specificities

  1996influential reference
• Mating and tetrad analysis in Chlamydomonas reinhardtii.

  1995cited by this paper
• Isolation and partial characterization of conditional cell division cycle mutants inChlamydomonas

  1995cited by this paper
• Ins and outs

  1994cited by this paper
• 莱哈衣藻（Chlamydomonas reinhardtii ...

  1993cited by this paper
• A mutation in the alpha 1-tubulin gene of Chlamydomonas reinhardtii confers resistance to anti-microtubule herbicides.

  1993cited by this paper
• Requirement for ESP1 in the nuclear division of Saccharomyces cerevisiae.

  1992cited by this paper
• Feedback control of mitosis in budding yeast.

  1991cited by this paper
• Universal control mechanism regulating onset of M-phase

  1990cited by this paper
• Dominoes and clocks: the union of two views of the cell cycle.

  1989cited by this paper
• Coordination of division events in theChlamydomonas cell cycle

  1986influential reference
• Cell cycle control by timer and sizer in Chlamydomonas

  1983cited by this paper
• Cell Volume and the Control of the Chlamydomonas Cell Cycle

  1982cited by this paper
• THE NUCLEAR CELL CYCLE IN CHLAMYDOMONAS (CHLOROPHYCEAE) 1

  1982cited by this paper
• Regulation of the Chlamydomonas cell cycle by light and dark

  1980cited by this paper
• Genetic control of the cell division cycle in the fission yeast Schizosaccharomyces pombe

  1976cited by this paper
• Genetic control of the cell division cycle in yeast.

  1974cited by this paper
• Genetic control of the cell-division cycle in yeast. I. Detection of mutants.

  1970cited by this paper
• FINE STRUCTURE OF CELL DIVISION IN CHLAMYDOMONAS REINHARDI

  1968cited by this paper
• Polyploidy and Genome Evolution in Plants This Review Comes from a Themed Issue on Genome Studies and Molecular Genetics Edited

  year unknowncited by this paper

• StOSD1/UVI4 is crucial for accurate mitotic progression and the maintenance of leaf morphology in potato

  2025cites this paper
• Mitotic entry is controlled by the plant-specific phosphatase BSL1 and cyclin-dependent kinase B

  2025cites this paper
• Optimised Ribosome Profiling Reveals New Insights Into Translational Regulation in Synchronised Chlamydomonas reinhardtii Cultures

  2025cites this paper
• Chlamydomonas.

  2024cites this paper
• A cytological and functional framework of the meiotic spindle assembly checkpoint in Arabidopsis thaliana

  2023cites this paper
• Rab GTPases, tethers, and SNAREs work together to regulate Arabidopsis cell plate formation

  2023cites this paper
• A Preliminary Study on the Mechanisms of Growth and Physiological Changes in Response to Different Temperatures in Neopyropia yezoensis (Rhodophyta)

  2022cites this paper
• Hyperosmotic stress-induced microtubule disassembly in Chlamydomonas reinhardtii

  2022cites this paper
• The Chlamydomonas Genome Project, version 6: Reference assemblies for mating-type plus and minus strains reveal extensive structural mutation in the laboratory

  2022cites this paper
• Chlamydomonas CHT7 is involved in repressing DNA replication and mitotic genes during synchronous growth

  2022cites this paper
• Control of division in Chlamydomonas by cyclin B/CDKB1 and the anaphase-promoting complex

  2022influential citation
• Hyperosmotic stress-induced microtubule disassembly in Chlamydomonas reinhardtii

  2022cites this paper
• Systems-wide analysis revealed shared and unique responses to moderate and acute high temperatures in the green alga Chlamydomonas reinhardtii

  2021cites this paper
• Co-expression networks in Chlamydomonas reveal significant rhythmicity in batch cultures and empower gene function discovery

  2021cites this paper
• Assaying Cyclin-Dependent Kinase Activity in Synchronized Algal Cultures.

  2021cites this paper
• Control of division and microtubule dynamics in Chlamydomonas by cyclin B/CDKB1 and the anaphase-promoting complex

  2021cites this paper
• Control of pre-replicative complex during the division cycle in Chlamydomonas reinhardtii

  2021influential citation
• OP-PLCE210041 1058..1082

  2021influential citation
• Chlamydomonas cell cycle mutant crcdc5 over-accumulates starch and oil.

  2020cites this paper
• Cyclin‐Dependent Protein Kinases in the Control of Cell Cycle in Plants

  2020cites this paper
• Co-Expression Networks in the Green Alga Chlamydomonas reinhardtii Empower Gene Discovery and Functional Exploration

  2020influential citation
• Revised annotation and extended characterizations of components of the Chlamydomonas reinhardtii SUMOylation system

  2020cites this paper
• Conservation and divergence of DNA replication control in Chlamydomonas reinhardtii

  2020cites this paper
• Regulation of Multiple Fission and Cell-Cycle-Dependent Gene Expression by CDKA1 and the Rb-E2F Pathway in Chlamydomonas.

  2020influential citation
• SUMO Protease SMT7 Modulates Ribosomal Protein L30 and Regulates Cell-Size Checkpoint Function[OPEN]

  2020cites this paper
• A Series of Fortunate Events: Introducing Chlamydomonas as a Reference Organism[OPEN]

  2019cites this paper
• Chlamydomonas reinhardtii formin FOR1 and profilin PRF1 are optimized for acute rapid actin filament assembly

  2019cites this paper
• Multiomics resolution of molecular events during a day in the life of Chlamydomonas

  2019cites this paper
• Comparative and Functional Algal Genomics.

  2019cites this paper
• A single light-responsive sizer can control multiple-fission cycles in Chlamydomonas

  2019cites this paper
• Response of the Green Alga Chlamydomonas reinhardtii to the DNA Damaging Agent Zeocin

  2019influential citation
• Cell Cycle Arrest by Supraoptimal Temperature in the Alga Chlamydomonas reinhardtii

  2019cites this paper
• Cleavage-furrow formation without F-actin in Chlamydomonas

  2019cites this paper
• Cell Cycle Control by Cyclin-CDKS in Chlamydomonas ReinhardtII

  2018cites this paper
• MAPINS, a Highly Efficient Detection Method That Identifies Insertional Mutations and Complex DNA Rearrangements1[OPEN]

  2018cites this paper
• F-actin homeostasis through transcriptional regulation and proteasome-mediated proteolysis

  2018cites this paper
• Effects of cyclin-dependent kinase activity on the coordination of growth and the cell cycle in green algae at different temperatures

  2018cites this paper
• A Brief History of Eukaryotic Cell Cycle Research

  2018cites this paper
• Comprehensive Discovery of Cell-Cycle-Essential Pathways in Chlamydomonas reinhardtii

  2018cites this paper
• Interregulation of CDKA/CDK1 and the Plant-Specific Cyclin-Dependent Kinase CDKB in Control of the Chlamydomonas Cell Cycle[OPEN]

  2018influential citation
• Sizing up the cell cycle: systems and quantitative approaches in Chlamydomonas.

  2018cites this paper
• Validated Bayesian Differentiation of Causative and Passenger Mutations

  2017cites this paper
• The Spindle Assembly Checkpoint in Arabidopsis Is Rapidly Shut Off during Severe Stress.

  2017cites this paper
• Changes in nitric oxide/hydrogen peroxide content and cell cycle progression: Study with synchronized cultures of green alga Chlamydomonas reinhardtii.

  2017cites this paper
• Models of cell division initiation in Chlamydomonas: A challenge to the consensus view.

  2017cites this paper
• Chapter 10 High-Throughput Genetics Strategies for Identifying New Components of Lipid Metabolism in the Green Alga Chlamydomonas reinhardtii

  2016cites this paper
• High-Throughput Robotically Assisted Isolation of Temperature-sensitive Lethal Mutants in Chlamydomonas reinhardtii

  2016cites this paper
• The plant‐specific CDKB1‐CYCB1 complex mediates homologous recombination repair in Arabidopsis

  2016cites this paper
• An Indexed, Mapped Mutant Library Enables Reverse Genetics Studies of Biological Processes in Chlamydomonas reinhardtii[OPEN]

  2016cites this paper
• The nonopisthokont septins: How many there are, how little we know about them, and how we might learn more.

  2016cites this paper
• High-Throughput Genetics Strategies for Identifying New Components of Lipid Metabolism in the Green Alga Chlamydomonas reinhardtii.

  2016cites this paper
• A Transcriptome-based Perspective of Cell Cycle Regulation in Dinoflagellates.

  2016cites this paper
• A new class of cyclin dependent kinase in Chlamydomonas is required for coupling cell size to cell division

  2016cites this paper
• The Cell Cycle of Microalgae

  2016cites this paper
• Somatic embryogenesis from immature and mature zygotic embryos of the açaí palm (Euterpe oleracea): Induction of embryogenic cultures, morphoanatomy and its morphological characteristics

  2016cites this paper
• Chlamydomonas reinhardtii formin FOR1 and profilin PRF1 are optimized for acute rapid actin filament assembly

  2016cites this paper
• Integrated Microalgae Analysis Photobioreactor for Rapid Strain Selection.

  2016cites this paper
• Molecular techniques to interrogate and edit the Chlamydomonas nuclear genome.

  2015cites this paper
• High-Resolution Profiling of a Synchronized Diurnal Transcriptome from Chlamydomonas reinhardtii Reveals Continuous Cell and Metabolic Differentiation[OPEN]

  2015influential citation
• The mitotic PP2A regulator ENSA/ARPP-19 is remarkably conserved across plants and most eukaryotes.

  2015cites this paper
• Patching Holes in the Chlamydomonas Genome

  2015cites this paper
• Cyclin-Dependent Kinase Regulation of Diurnal Transcription in Chlamydomonas

  2015influential citation
• The Chlamydomonas cell cycle

  2015influential citation
• Evidence That an Unconventional Actin Can Provide Essential F-Actin Function and That a Surveillance System Monitors F-Actin Integrity in Chlamydomonas

  2015influential citation