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Zamora-Zaragoza J, Klap K, Sánchez-Pérez J, Vielle-Calzada JP, Willemsen V, Scheres B. Developmental cues are encoded by the combinatorial phosphorylation of Arabidopsis RETINOBLASTOMA-RELATED protein RBR1. EMBO J 2024; 43:6656-6678. [PMID: 39468281 PMCID: PMC11649800 DOI: 10.1038/s44318-024-00282-3] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/22/2021] [Revised: 08/29/2024] [Accepted: 09/27/2024] [Indexed: 10/30/2024] Open
Abstract
RETINOBLASTOMA-RELATED (RBR) proteins orchestrate cell division, differentiation, and survival in response to environmental and developmental cues through protein-protein interactions that are governed by multisite phosphorylation. Here we explore, using a large collection of transgenic RBR phosphovariants to complement protein function in Arabidopsis thaliana, whether differences in the number and position of RBR phosphorylation events cause a diversification of the protein's function. While the number of point mutations influence phenotypic strength, phosphosites contribute differentially to distinct phenotypes. RBR pocket domain mutations associate primarily with cell proliferation, while mutations in the C-region are linked to stem cell maintenance. Both phospho-mimetic and a phospho-defective variants promote cell death, suggesting that distinct mechanisms can lead to similar cell fates. We observed combinatorial effects between phosphorylated T406 and phosphosites in different protein domains, suggesting that specific, additive, and combinatorial phosphorylation events fine-tune RBR function. Suppression of dominant phospho-defective RBR phenotypes with a mutation that inhibits RBR interacting with LXCXE motifs, and an exhaustive protein-protein interaction assay, not only revealed the importance of DREAM complex members in phosphorylation-regulated RBR function but also pointed to phosphorylation-independent RBR roles in environmental responses. Thus, combinatorial phosphorylation defined and separated developmental, but not environmental, functions of RBR.
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Affiliation(s)
- Jorge Zamora-Zaragoza
- Laboratory of Cell and Developmental Biology, Department of Plant Sciences, Wageningen University and Research, 6708 PB, Wageningen, The Netherlands
- Rijk Zwaan Breeding B.V., Department of Biotechnology, Eerste Kruisweg 9, 4793 RS, Fijnaart, The Netherlands
| | - Katinka Klap
- Laboratory of Cell and Developmental Biology, Department of Plant Sciences, Wageningen University and Research, 6708 PB, Wageningen, The Netherlands
| | - Jaheli Sánchez-Pérez
- Laboratorio Nacional de Genómica para la Biodiversidad, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, 36824, Irapuato, Guanajuato, Mexico
| | - Jean-Philippe Vielle-Calzada
- Laboratorio Nacional de Genómica para la Biodiversidad, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, 36824, Irapuato, Guanajuato, Mexico
| | - Viola Willemsen
- Laboratory of Cell and Developmental Biology, Department of Plant Sciences, Wageningen University and Research, 6708 PB, Wageningen, The Netherlands
| | - Ben Scheres
- Laboratory of Cell and Developmental Biology, Department of Plant Sciences, Wageningen University and Research, 6708 PB, Wageningen, The Netherlands.
- Rijk Zwaan Breeding B.V., Department of Biotechnology, Eerste Kruisweg 9, 4793 RS, Fijnaart, The Netherlands.
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Rusnak B, Clark FK, Vadde BVL, Roeder AHK. What Is a Plant Cell Type in the Age of Single-Cell Biology? It's Complicated. Annu Rev Cell Dev Biol 2024; 40:301-328. [PMID: 38724025 DOI: 10.1146/annurev-cellbio-111323-102412] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 10/04/2024]
Abstract
One of the fundamental questions in developmental biology is how a cell is specified to differentiate as a specialized cell type. Traditionally, plant cell types were defined based on their function, location, morphology, and lineage. Currently, in the age of single-cell biology, researchers typically attempt to assign plant cells to cell types by clustering them based on their transcriptomes. However, because cells are dynamic entities that progress through the cell cycle and respond to signals, the transcriptome also reflects the state of the cell at a particular moment in time, raising questions about how to define a cell type. We suggest that these complexities and dynamics of cell states are of interest and further consider the roles signaling, stochasticity, cell cycle, and mechanical forces play in plant cell fate specification. Once established, cell identity must also be maintained. With the wealth of single-cell data coming out, the field is poised to elucidate both the complexity and dynamics of cell states.
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Affiliation(s)
- Byron Rusnak
- Weill Institute for Cell and Molecular Biology and School of Integrative Plant Science, Section of Plant Biology, Cornell University, Ithaca, New York, USA; , ,
| | - Frances K Clark
- Department of Molecular Biology and Genetics, Cornell University, Ithaca, New York, USA
- Weill Institute for Cell and Molecular Biology and School of Integrative Plant Science, Section of Plant Biology, Cornell University, Ithaca, New York, USA; , ,
| | - Batthula Vijaya Lakshmi Vadde
- Plant Molecular and Cellular Biology Laboratory, Salk Institute for Biological Studies, La Jolla, California, USA;
- Weill Institute for Cell and Molecular Biology and School of Integrative Plant Science, Section of Plant Biology, Cornell University, Ithaca, New York, USA; , ,
| | - Adrienne H K Roeder
- Weill Institute for Cell and Molecular Biology and School of Integrative Plant Science, Section of Plant Biology, Cornell University, Ithaca, New York, USA; , ,
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3
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Yang Y, Liu C, Yu Y, Ran G, Zhai N, Pi L. WUSCHEL RELATED HOMEOBOX5 and 7 maintain callus development by promoting cell division in Arabidopsis. PLANT SCIENCE : AN INTERNATIONAL JOURNAL OF EXPERIMENTAL PLANT BIOLOGY 2024; 346:112133. [PMID: 38795752 DOI: 10.1016/j.plantsci.2024.112133] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 12/29/2023] [Revised: 04/18/2024] [Accepted: 05/20/2024] [Indexed: 05/28/2024]
Abstract
In tissue culture, a high concentration of auxin in the callus induction medium (CIM) stimulates cell division and subsequent callus formation, which acquires root primordium-like characteristics necessary for cell pluripotency. In Arabidopsis, WUSCHEL-RELATED HOMEOBOX5 (WOX5) and its closest homolog WOX7, which are abundant in the middle cell layer of mature callus, play a crucial role in maintaining pluripotency by promoting auxin accumulation and enhancing cytokinin sensitivity. However, the mechanism by which WOX5/7 regulate callus formation remains unclear. In this study, we found that mutations in WOX5/7 resulted in a significant down-regulation of genes involved in the G2M and S phases during callus induction. Loss-of-function mutants of WOX5/7 exhibited reduced callus formation, which was correlated with decreased expression of CYCB1;1 compared to the wild-type. Furthermore, we provided evidence that WOX5 physically interacts with PHYTOCHROME A SIGNAL TRANSDUCTION1 (PAT1), which spatio-temporally co-expresses with WOX5 in early-induced callus, and up-regulates a subset of cycle-regulating genes targeted by PAT1. Collectively, our findings suggest a critical role for the WOX5-PAT1 protein complex in regulating cell cycle progression, thereby promoting the continuous growth capacity of pluripotent callus.
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Affiliation(s)
- Yi Yang
- State Key Laboratory of Hybrid Rice, Institute for Advanced Studies (IAS), Wuhan University, Wuhan, Hubei 430072, China
| | - Caifeng Liu
- State Key Laboratory of Hybrid Rice, Institute for Advanced Studies (IAS), Wuhan University, Wuhan, Hubei 430072, China
| | - Yue Yu
- State Key Laboratory of Hybrid Rice, Institute for Advanced Studies (IAS), Wuhan University, Wuhan, Hubei 430072, China
| | - Guiping Ran
- State Key Laboratory of Hybrid Rice, Institute for Advanced Studies (IAS), Wuhan University, Wuhan, Hubei 430072, China
| | - Ning Zhai
- National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, 300 Fenglin Road, Shanghai 200032, China.
| | - Limin Pi
- State Key Laboratory of Hybrid Rice, Institute for Advanced Studies (IAS), Wuhan University, Wuhan, Hubei 430072, China.
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4
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Miao Y, You H, Liu H, Zhao Y, Zhao J, Li Y, Shen Y, Tang D, Liu B, Zhang K, Cheng Z. RETINOBLASTOMA RELATED 1 switches mitosis to meiosis in rice. PLANT COMMUNICATIONS 2024; 5:100857. [PMID: 38433446 PMCID: PMC11211523 DOI: 10.1016/j.xplc.2024.100857] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 09/22/2023] [Revised: 02/07/2024] [Accepted: 02/27/2024] [Indexed: 03/05/2024]
Abstract
The transition from mitosis to meiosis is a critical event in the reproductive development of all sexually reproducing species. However, the mechanisms that regulate this process in plants remain largely unknown. Here, we find that the rice (Oryza sativa L.) protein RETINOBLASTOMA RELATED 1 (RBR1) is essential to the transition from mitosis to meiosis. Loss of RBR1 function results in hyper-proliferative sporogenous-cell-like cells (SCLs) in the anther locules during early stages of reproductive development. These hyper-proliferative SCLs are unable to initiate meiosis, eventually stagnating and degrading at late developmental stages to form pollen-free anthers. These results suggest that RBR1 acts as a gatekeeper of entry into meiosis. Furthermore, cytokinin content is significantly increased in rbr1 mutants, whereas the expression of type-B response factors, particularly LEPTO1, is significantly reduced. Given the known close association of cytokinins with cell proliferation, these findings imply that hyper-proliferative germ cells in the anther locules may be attributed to elevated cytokinin concentrations and disruptions in the cytokinin pathway. Using a genetic strategy, the association between germ cell hyper-proliferation and disturbed cytokinin signaling in rbr1 has been confirmed. In summary, we reveal a unique role of RBR1 in the initiation of meiosis; our results clearly demonstrate that the RBR1 regulatory module is connected to the cytokinin signaling pathway and switches mitosis to meiosis in rice.
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Affiliation(s)
- Yongjie Miao
- Guangdong Provincial Key Laboratory of Plant Adaptation and Molecular Design, Innovative Center of Molecular Genetics and Evolution, School of Life Sciences, Guangzhou University, Guangzhou 510006, China; Jiangsu Key Laboratory of Crop Genomics and Molecular Breeding/Zhongshan Biological Breeding Laboratory/Key Laboratory of Plant Functional Genomics of the Ministry of Education, Agricultural College of Yangzhou University, Yangzhou 225009, China
| | - Hanli You
- Jiangsu Key Laboratory of Crop Genomics and Molecular Breeding/Zhongshan Biological Breeding Laboratory/Key Laboratory of Plant Functional Genomics of the Ministry of Education, Agricultural College of Yangzhou University, Yangzhou 225009, China
| | - Huixin Liu
- State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, Innovation Academy for Seed Design, Chinese Academy of Sciences, Beijing 100101, China
| | - Yangzi Zhao
- State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, Innovation Academy for Seed Design, Chinese Academy of Sciences, Beijing 100101, China
| | - Jiangzhe Zhao
- Zhejiang Provincial Key Laboratory of Biotechnology on Specialty Economic Plants, Department of Biology, College of Life Sciences, Zhejiang Normal University, Jinhua 321004, China
| | - Yafei Li
- State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, Innovation Academy for Seed Design, Chinese Academy of Sciences, Beijing 100101, China
| | - Yi Shen
- State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, Innovation Academy for Seed Design, Chinese Academy of Sciences, Beijing 100101, China
| | - Ding Tang
- State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, Innovation Academy for Seed Design, Chinese Academy of Sciences, Beijing 100101, China
| | - Baohui Liu
- Guangdong Provincial Key Laboratory of Plant Adaptation and Molecular Design, Innovative Center of Molecular Genetics and Evolution, School of Life Sciences, Guangzhou University, Guangzhou 510006, China.
| | - Kewei Zhang
- Zhejiang Provincial Key Laboratory of Biotechnology on Specialty Economic Plants, Department of Biology, College of Life Sciences, Zhejiang Normal University, Jinhua 321004, China.
| | - Zhukuan Cheng
- Jiangsu Key Laboratory of Crop Genomics and Molecular Breeding/Zhongshan Biological Breeding Laboratory/Key Laboratory of Plant Functional Genomics of the Ministry of Education, Agricultural College of Yangzhou University, Yangzhou 225009, China; Jiangsu Co-Innovation Center for Modern Production Technology of Grain Crops/Jiangsu Key Laboratory of Crop Genetics and Physiology, Yangzhou University, Yangzhou 225009, China.
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Zaragoza JZ, Klap K, Heidstra R, Zhou W, Scheres B. The dual role of the RETINOBLASTOMA-RELATED protein in the DNA damage response is coordinated by the interaction with LXCXE-containing proteins. THE PLANT JOURNAL : FOR CELL AND MOLECULAR BIOLOGY 2024; 118:1194-1206. [PMID: 38321589 DOI: 10.1111/tpj.16665] [Citation(s) in RCA: 2] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Received: 02/08/2022] [Revised: 01/10/2024] [Accepted: 01/18/2024] [Indexed: 02/08/2024]
Abstract
Living organisms possess mechanisms to safeguard genome integrity. To avoid spreading mutations, DNA lesions are detected and cell division is temporarily arrested to allow repair mechanisms. Afterward, cells either resume division or respond to unsuccessful repair by undergoing programmed cell death (PCD). How the success rate of DNA repair connects to later cell fate decisions remains incompletely known, particularly in plants. The Arabidopsis thaliana RETINOBLASTOMA-RELATED1 (RBR) protein and its partner E2FA, play both structural and transcriptional functions in the DNA damage response (DDR). Here we provide evidence that distinct RBR protein interactions with LXCXE motif-containing proteins guide these processes. Using the N849F substitution in the RBR B-pocket domain, which specifically disrupts binding to the LXCXE motif, we show that these interactions are dispensable in unchallenging conditions. However, N849F substitution abolishes RBR nuclear foci and promotes PCD and growth arrest upon genotoxic stress. NAC044, which promotes growth arrest and PCD, accumulates after the initial recruitment of RBR to foci and can bind non-focalized RBR through the LXCXE motif in a phosphorylation-independent manner, allowing interaction at different cell cycle phases. Disrupting NAC044-RBR interaction impairs PCD, but their genetic interaction points to opposite independent roles in the regulation of PCD. The LXCXE-binding dependency of the roles of RBR in the DDR suggests a coordinating mechanism to translate DNA repair success to cell survival. We propose that RBR and NAC044 act in two distinct DDR pathways, but interact to integrate input from both DDR pathways to decide upon an irreversible cell fate decision.
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Affiliation(s)
- Jorge Zamora Zaragoza
- Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University and Research, 6708 PB, Wageningen, The Netherlands
- Department of Biotechnology, Rijk Zwaan Breeding B.V., Eerste Kruisweg 9, 4793 RS, Fijnaart, The Netherlands
| | - Katinka Klap
- Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University and Research, 6708 PB, Wageningen, The Netherlands
| | - Renze Heidstra
- Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University and Research, 6708 PB, Wageningen, The Netherlands
| | - Wenkun Zhou
- Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University and Research, 6708 PB, Wageningen, The Netherlands
- State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing, 100193, China
| | - Ben Scheres
- Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University and Research, 6708 PB, Wageningen, The Netherlands
- Department of Biotechnology, Rijk Zwaan Breeding B.V., Eerste Kruisweg 9, 4793 RS, Fijnaart, The Netherlands
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6
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Rawat SS, Laxmi A. Sugar signals pedal the cell cycle! FRONTIERS IN PLANT SCIENCE 2024; 15:1354561. [PMID: 38562561 PMCID: PMC10982403 DOI: 10.3389/fpls.2024.1354561] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Subscribe] [Scholar Register] [Received: 12/12/2023] [Accepted: 02/19/2024] [Indexed: 04/04/2024]
Abstract
Cell cycle involves the sequential and reiterative progression of important events leading to cell division. Progression through a specific phase of the cell cycle is under the control of various factors. Since the cell cycle in multicellular eukaryotes responds to multiple extracellular mitogenic cues, its study in higher forms of life becomes all the more important. One such factor regulating cell cycle progression in plants is sugar signalling. Because the growth of organs depends on both cell growth and proliferation, sugars sensing and signalling are key control points linking sugar perception to regulation of downstream factors which facilitate these key developmental transitions. However, the basis of cell cycle control via sugars is intricate and demands exploration. This review deals with the information on sugar and TOR-SnRK1 signalling and how they manoeuvre various events of the cell cycle to ensure proper growth and development.
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Affiliation(s)
| | - Ashverya Laxmi
- National Institute of Plant Genome Research, Aruna Asaf Ali Marg, New Delhi, India
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7
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León-Ruiz JA, Cruz Ramírez A. Predicted landscape of RETINOBLASTOMA-RELATED LxCxE-mediated interactions across the Chloroplastida. THE PLANT JOURNAL : FOR CELL AND MOLECULAR BIOLOGY 2022; 112:1507-1524. [PMID: 36305297 DOI: 10.1111/tpj.16012] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 06/08/2022] [Revised: 09/20/2022] [Accepted: 10/14/2022] [Indexed: 05/16/2023]
Abstract
The colonization of land by a single streptophyte algae lineage some 450 million years ago has been linked to multiple key innovations such as three-dimensional growth, alternation of generations, the presence of stomata, as well as innovations inherent to the birth of major plant lineages, such as the origins of vascular tissues, roots, seeds and flowers. Multicellularity, which evolved multiple times in the Chloroplastida coupled with precise spatiotemporal control of proliferation and differentiation were instrumental for the evolution of these traits. RETINOBLASTOMA-RELATED (RBR), the plant homolog of the metazoan Retinoblastoma protein (pRB), is a highly conserved and multifunctional core cell cycle regulator that has been implicated in the evolution of multicellularity in the green lineage as well as in plant multicellularity-related processes such as proliferation, differentiation, stem cell regulation and asymmetric cell division. RBR fulfills these roles through context-specific protein-protein interactions with proteins containing the Leu-x-Cys-x-Glu (LxCxE) short-linear motif (SLiM); however, how RBR-LxCxE interactions have changed throughout major innovations in the Viridiplantae kingdom is a question that remains unexplored. Here, we employ an in silico evo-devo approach to predict and analyze potential RBR-LxCxE interactions in different representative species of key Chloroplastida lineages, providing a valuable resource for deciphering RBR-LxCxE multiple functions. Furthermore, our analyses suggest that RBR-LxCxE interactions are an important component of RBR functions and that interactions with chromatin modifiers/remodelers, DNA replication and repair machinery are highly conserved throughout the Viridiplantae, while LxCxE interactions with transcriptional regulators likely diversified throughout the water-to-land transition.
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Affiliation(s)
- Jesús A León-Ruiz
- Molecular and Developmental Complexity Group, Unidad de Genómica Avanzada, Laboratorio Nacional de Genómica para la Biodiversidad, Cinvestav Sede Irapuato, Km. 9.6 Libramiento Norte Carretera, Irapuato-León, Irapuato, 36821, Guanajuato, Mexico
| | - Alfredo Cruz Ramírez
- Molecular and Developmental Complexity Group, Unidad de Genómica Avanzada, Laboratorio Nacional de Genómica para la Biodiversidad, Cinvestav Sede Irapuato, Km. 9.6 Libramiento Norte Carretera, Irapuato-León, Irapuato, 36821, Guanajuato, Mexico
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8
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Aragón-Raygoza A, Herrera-Estrella L, Cruz-Ramírez A. Transcriptional analysis of Ceratopteris richardii young sporophyte reveals conservation of stem cell factors in the root apical meristem. FRONTIERS IN PLANT SCIENCE 2022; 13:924660. [PMID: 36035690 PMCID: PMC9413220 DOI: 10.3389/fpls.2022.924660] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Subscribe] [Scholar Register] [Received: 04/20/2022] [Accepted: 07/14/2022] [Indexed: 06/15/2023]
Abstract
Gene expression in roots has been assessed in different plant species in studies ranging from complete organs to specific cell layers, and more recently at the single cell level. While certain genes or functional categories are expressed in the root of all or most plant species, lineage-specific genes have also been discovered. An increasing amount of transcriptomic data is available for angiosperms, while a limited amount of data is available for ferns, and few studies have focused on fern roots. Here, we present a de novo transcriptome assembly from three different parts of the Ceratopteris richardii young sporophyte. Differential gene expression analysis of the root tip transcriptional program showed an enrichment of functional categories related to histogenesis and cell division, indicating an active apical meristem. Analysis of a diverse set of orthologous genes revealed conserved expression in the root meristem, suggesting a preserved role for different developmental roles in this tissue, including stem cell maintenance. The reconstruction of evolutionary trajectories for ground tissue specification genes suggests a high degree of conservation in vascular plants, but not for genes involved in root cap development, showing that certain genes are absent in Ceratopteris or have intricate evolutionary paths difficult to track. Overall, our results suggest different processes of conservation and divergence of genes involved in root development.
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Affiliation(s)
- Alejandro Aragón-Raygoza
- Molecular and Developmental Complexity Group, Unidad De Genómica Avanzada, Laboratorio Nacional De Genómica Para la Biodiversidad, Cinvestav Unidad Irapuato, Irapuato, Guanajuato, Mexico
- Metabolic Engineering Group, Unidad De Genómica Avanzada, Laboratorio Nacional De Genómica Para la Biodiversidad, Cinvestav Unidad Irapuato, Irapuato, Guanajuato, Mexico
| | - Luis Herrera-Estrella
- Metabolic Engineering Group, Unidad De Genómica Avanzada, Laboratorio Nacional De Genómica Para la Biodiversidad, Cinvestav Unidad Irapuato, Irapuato, Guanajuato, Mexico
- Department of Plant and Soil Science, Institute of Genomics for Crop Abiotic Stress Tolerance, Texas Tech University, Lubbock, TX, United States
| | - Alfredo Cruz-Ramírez
- Molecular and Developmental Complexity Group, Unidad De Genómica Avanzada, Laboratorio Nacional De Genómica Para la Biodiversidad, Cinvestav Unidad Irapuato, Irapuato, Guanajuato, Mexico
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Gutierrez C. A Journey to the Core of the Plant Cell Cycle. Int J Mol Sci 2022; 23:8154. [PMID: 35897730 PMCID: PMC9330084 DOI: 10.3390/ijms23158154] [Citation(s) in RCA: 3] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/01/2022] [Revised: 07/16/2022] [Accepted: 07/21/2022] [Indexed: 02/04/2023] Open
Abstract
Production of new cells as a result of progression through the cell division cycle is a fundamental biological process for the perpetuation of both unicellular and multicellular organisms. In the case of plants, their developmental strategies and their largely sessile nature has imposed a series of evolutionary trends. Studies of the plant cell division cycle began with cytological and physiological approaches in the 1950s and 1960s. The decade of 1990 marked a turn point with the increasing development of novel cellular and molecular protocols combined with advances in genetics and, later, genomics, leading to an exponential growth of the field. In this article, I review the current status of plant cell cycle studies but also discuss early studies and the relevance of a multidisciplinary background as a source of innovative questions and answers. In addition to advances in a deeper understanding of the plant cell cycle machinery, current studies focus on the intimate interaction of cell cycle components with almost every aspect of plant biology.
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Affiliation(s)
- Crisanto Gutierrez
- Centro de Biologia Molecular Severo Ochoa, CSIC-UAM, Nicolas Cabrera 1, Cantoblanco, 28049 Madrid, Spain
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10
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A guiding role of the Arabidopsis circadian clock in cell differentiation revealed by time-series single-cell RNA sequencing. Cell Rep 2022; 40:111059. [PMID: 35830805 DOI: 10.1016/j.celrep.2022.111059] [Citation(s) in RCA: 7] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/09/2021] [Revised: 04/01/2022] [Accepted: 06/14/2022] [Indexed: 11/21/2022] Open
Abstract
Circadian rhythms and progression of cell differentiation are closely coupled in multicellular organisms. However, whether establishment of circadian rhythms regulates cell differentiation or vice versa has not been elucidated due to technical limitations. Here, we exploit high cell fate plasticity of plant cells to perform single-cell RNA sequencing during the entire process of cell differentiation. By analyzing reconstructed actual time series of the differentiation processes at single-cell resolution using a method we developed (PeakMatch), we find that the expression profile of clock genes is changed prior to cell differentiation, including induction of the clock gene LUX ARRYTHMO (LUX). ChIP sequencing analysis reveals that LUX induction in early differentiating cells directly targets genes involved in cell-cycle progression to regulate cell differentiation. Taken together, these results not only reveal a guiding role of the plant circadian clock in cell differentiation but also provide an approach for time-series analysis at single-cell resolution.
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Morales-de la Cruz X, Mandujano-Chávez A, Browne DR, Devarenne TP, Sánchez-Segura L, López MG, Lozoya-Gloria E. In Silico and Cellular Differences Related to the Cell Division Process between the A and B Races of the Colonial Microalga Botryococcus braunii. Biomolecules 2021; 11:biom11101463. [PMID: 34680096 PMCID: PMC8533097 DOI: 10.3390/biom11101463] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/08/2021] [Revised: 09/23/2021] [Accepted: 09/25/2021] [Indexed: 11/23/2022] Open
Abstract
Botryococcus braunii produce liquid hydrocarbons able to be processed into combustion engine fuels. Depending on the growing conditions, the cell doubling time can be up to 6 days or more, which is a slow growth rate in comparison with other microalgae. Few studies have analyzed the cell cycle of B. braunii. We did a bioinformatic comparison between the protein sequences for retinoblastoma and cyclin-dependent kinases from the A (Yamanaka) and B (Showa) races, with those sequences from other algae and Arabidopsis thaliana. Differences in the number of cyclin-dependent kinases and potential retinoblastoma phosphorylation sites between the A and B races were found. Some cyclin-dependent kinases from both races seemed to be phylogenetically more similar to A. thaliana than to other microalgae. Microscopic observations were done using several staining procedures. Race A colonies, but not race B, showed some multinucleated cells without chlorophyll. An active mitochondrial net was detected in those multinucleated cells, as well as being defined in polyphosphate bodies. These observations suggest differences in the cell division processes between the A and B races of B. braunii.
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Affiliation(s)
- Xochitl Morales-de la Cruz
- Genetic Engineering Department, CINVESTAV-IPN Irapuato Unit, Irapuato 36824, Mexico; (X.M.-d.l.C.); (L.S.-S.)
| | | | - Daniel R. Browne
- Department of Biochemistry and Biophysics, Texas A&M University, College Station, TX 77843, USA; (D.R.B.); (T.P.D.)
- Pacific Biosciences, Chicago, IL 60606, USA
| | - Timothy P. Devarenne
- Department of Biochemistry and Biophysics, Texas A&M University, College Station, TX 77843, USA; (D.R.B.); (T.P.D.)
| | - Lino Sánchez-Segura
- Genetic Engineering Department, CINVESTAV-IPN Irapuato Unit, Irapuato 36824, Mexico; (X.M.-d.l.C.); (L.S.-S.)
| | - Mercedes G. López
- Biochemistry and Biotechnology Department, CINVESTAV-IPN Irapuato Unit, Irapuato 36824, Mexico;
| | - Edmundo Lozoya-Gloria
- Genetic Engineering Department, CINVESTAV-IPN Irapuato Unit, Irapuato 36824, Mexico; (X.M.-d.l.C.); (L.S.-S.)
- Correspondence: ; Tel.: +52-462-6239659
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Coke MC, Mantelin S, Thorpe P, Lilley CJ, Wright KM, Shaw DS, Chande A, Jones JT, Urwin PE. The GpIA7 effector from the potato cyst nematode Globodera pallida targets potato EBP1 and interferes with the plant cell cycle programme. JOURNAL OF EXPERIMENTAL BOTANY 2021; 72:erab353. [PMID: 34310681 PMCID: PMC8547150 DOI: 10.1093/jxb/erab353] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Received: 02/09/2021] [Accepted: 07/26/2021] [Indexed: 06/13/2023]
Abstract
The potato cyst nematode Globodera pallida acquires all of its nutrients from an elaborate feeding site that it establishes in a host plant root. Normal development of the root cells is re-programmed in a process coordinated by secreted nematode effector proteins. The biological function of the G. pallida GpIA7 effector was investigated in this study. GpIA7 is specifically expressed in the subventral pharyngeal glands of pre-parasitic stage nematodes. Ectopic expression of GpIA7 in potato plants affected plant growth and development, suggesting a potential role for this effector in feeding site establishment. Potato plants overexpressing GpIA7 were shorter, with reduced tuber weight and delayed flowering. We provide evidence that GpIA7 associates with the plant growth regulator StEBP1 (ErbB-3 epidermal growth factor receptor-binding protein 1). GpIA7 modulates the regulatory function of StEBP1, altering the expression level of downstream target genes, including ribonucleotide reductase 2, cyclin D3;1 and retinoblastoma related 1, which are downregulated in plants overexpressing GpIA7. We provide an insight into the molecular mechanism used by the nematode to manipulate the host cell cycle and provide evidence that this may rely, at least in part, on hindering the function of host EBP1.
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Affiliation(s)
- Mirela C Coke
- Centre for Plant Sciences, University of Leeds, Leeds LS2 9JT, UK
| | - Sophie Mantelin
- The James Hutton Institute, Dundee Effector Consortium, Invergowrie, Dundee DD2 5DA, UK
| | - Peter Thorpe
- Centre for Plant Sciences, University of Leeds, Leeds LS2 9JT, UK
- The James Hutton Institute, Dundee Effector Consortium, Invergowrie, Dundee DD2 5DA, UK
| | | | - Kathryn M Wright
- The James Hutton Institute, Dundee Effector Consortium, Invergowrie, Dundee DD2 5DA, UK
| | - Daniel S Shaw
- Centre for Plant Sciences, University of Leeds, Leeds LS2 9JT, UK
| | - Adams Chande
- Centre for Plant Sciences, University of Leeds, Leeds LS2 9JT, UK
| | - John T Jones
- The James Hutton Institute, Dundee Effector Consortium, Invergowrie, Dundee DD2 5DA, UK
- School of Biology, University of St Andrews, North Haugh, St Andrews KY16 9TZ, UK
| | - Peter E Urwin
- Centre for Plant Sciences, University of Leeds, Leeds LS2 9JT, UK
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13
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Hydroxyurea and Caffeine Impact pRb-like Protein-Dependent Chromatin Architecture Profiles in Interphase Cells of Vicia faba. Int J Mol Sci 2021; 22:ijms22094572. [PMID: 33925461 PMCID: PMC8123844 DOI: 10.3390/ijms22094572] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/15/2021] [Revised: 04/06/2021] [Accepted: 04/23/2021] [Indexed: 01/04/2023] Open
Abstract
The survival of cells depends on their ability to replicate correctly genetic material. Cells exposed to replication stress can experience a number of problems that may lead to deregulated proliferation, the development of cancer, and/or programmed cell death. In this article, we have induced prolonged replication arrest via hydroxyurea (HU) treatment and also premature chromosome condensation (PCC) by co-treatment with HU and caffeine (CF) in the root meristem cells of Vicia faba. We have analyzed the changes in the activities of retinoblastoma-like protein (RbS807/811ph). Results obtained from the immunocytochemical detection of RbS807/811ph allowed us to distinguish five unique activity profiles of pRb. We have also performed detailed 3D modeling using Blender 2.9.1., based on the original data and some final conclusions. 3D models helped us to visualize better the events occurring within the nuclei and acted as a high-resolution aid for presenting the results. We have found that, despite the decrease in pRb activity, its activity profiles were mostly intact and clearly recognizable, with some local alterations that may correspond to the increased demand in transcriptional activity. Our findings suggest that Vicia faba’s ability to withstand harsh environments may come from its well-developed and highly effective response to replication stress.
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14
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Ötvös K, Miskolczi P, Marhavý P, Cruz-Ramírez A, Benková E, Robert S, Bakó L. Pickle Recruits Retinoblastoma Related 1 to Control Lateral Root Formation in Arabidopsis. Int J Mol Sci 2021; 22:ijms22083862. [PMID: 33917959 PMCID: PMC8068362 DOI: 10.3390/ijms22083862] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/24/2021] [Revised: 04/04/2021] [Accepted: 04/06/2021] [Indexed: 12/31/2022] Open
Abstract
Lateral root (LR) formation is an example of a plant post-embryonic organogenesis event. LRs are issued from non-dividing cells entering consecutive steps of formative divisions, proliferation and elongation. The chromatin remodeling protein PICKLE (PKL) negatively regulates auxin-mediated LR formation through a mechanism that is not yet known. Here we show that PKL interacts with RETINOBLASTOMA-RELATED 1 (RBR1) to repress the LATERAL ORGAN BOUNDARIES-DOMAIN 16 (LBD16) promoter activity. Since LBD16 function is required for the formative division of LR founder cells, repression mediated by the PKL–RBR1 complex negatively regulates formative division and LR formation. Inhibition of LR formation by PKL–RBR1 is counteracted by auxin, indicating that, in addition to auxin-mediated transcriptional responses, the fine-tuned process of LR formation is also controlled at the chromatin level in an auxin-signaling dependent manner.
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Affiliation(s)
- Krisztina Ötvös
- Department of Plant Physiology, Umeå Plant Science Center, Umeå University, S-901 87 Umeå, Sweden
- Institute of Science and Technology Austria, Am Campus 1, 3400 Klosterneuburg, Austria; (P.M.); (E.B.)
- Bioresources Unit, AIT Austrian Institute of Technology, 3430 Tulln, Austria
- Correspondence: (K.Ö.); (L.B.); Tel.: +46-907867970 (K.Ö.); Fax: +46-907866676 (K.Ö.)
| | - Pál Miskolczi
- Department of Forest Genetics and Plant Physiology, Umeå Plant Science Center, Swedish University of Agricultural Sciences, S-901 87 Umeå, Sweden; (P.M.); (S.R.)
| | - Peter Marhavý
- Institute of Science and Technology Austria, Am Campus 1, 3400 Klosterneuburg, Austria; (P.M.); (E.B.)
| | - Alfredo Cruz-Ramírez
- Laboratory of Molecular and Developmental Complexity at Laboratorio Nacional de Genómica para la Biodiversidad, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, (CINVESTAV-IPN), 36590 Irapuato, Mexico;
| | - Eva Benková
- Institute of Science and Technology Austria, Am Campus 1, 3400 Klosterneuburg, Austria; (P.M.); (E.B.)
| | - Stéphanie Robert
- Department of Forest Genetics and Plant Physiology, Umeå Plant Science Center, Swedish University of Agricultural Sciences, S-901 87 Umeå, Sweden; (P.M.); (S.R.)
| | - László Bakó
- Department of Plant Physiology, Umeå Plant Science Center, Umeå University, S-901 87 Umeå, Sweden
- Correspondence: (K.Ö.); (L.B.); Tel.: +46-907867970 (K.Ö.); Fax: +46-907866676 (K.Ö.)
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15
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Pignocchi C, Ivakov A, Feil R, Trick M, Pike M, Wang TL, Lunn JE, Smith AM. Restriction of cytosolic sucrose hydrolysis profoundly alters development, metabolism, and gene expression in Arabidopsis roots. JOURNAL OF EXPERIMENTAL BOTANY 2021; 72:1850-1863. [PMID: 33378456 PMCID: PMC7921298 DOI: 10.1093/jxb/eraa581] [Citation(s) in RCA: 12] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Received: 06/06/2020] [Accepted: 12/10/2020] [Indexed: 05/28/2023]
Abstract
Plant roots depend on sucrose imported from leaves as the substrate for metabolism and growth. Sucrose and hexoses derived from it are also signalling molecules that modulate growth and development, but the importance for signalling of endogenous changes in sugar levels is poorly understood. We report that reduced activity of cytosolic invertase, which converts sucrose to hexoses, leads to pronounced metabolic, growth, and developmental defects in roots of Arabidopsis (Arabidopsis thaliana) seedlings. In addition to altered sugar and downstream metabolite levels, roots of cinv1 cinv2 mutants have reduced elongation rates, cell and meristem size, abnormal meristematic cell division patterns, and altered expression of thousands of genes of diverse functions. Provision of exogenous glucose to mutant roots repairs relatively few of the defects. The extensive transcriptional differences between mutant and wild-type roots have hallmarks of both high sucrose and low hexose signalling. We conclude that the mutant phenotype reflects both low carbon availability for metabolism and growth and complex sugar signals derived from elevated sucrose and depressed hexose levels in the cytosol of mutant roots. Such reciprocal changes in endogenous sucrose and hexose levels potentially provide rich information about sugar status that translates into flexible adjustments of growth and development.
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Affiliation(s)
| | - Alexander Ivakov
- Max Planck Institute of Molecular Plant Physiology, Wissenschaftspark Potsdam-Golm, Am Mühlenberg, Potsdam-Golm, Germany
| | - Regina Feil
- Max Planck Institute of Molecular Plant Physiology, Wissenschaftspark Potsdam-Golm, Am Mühlenberg, Potsdam-Golm, Germany
| | - Martin Trick
- John Innes Centre, Norwich Research Park, Norwich, UK
| | - Marilyn Pike
- John Innes Centre, Norwich Research Park, Norwich, UK
| | - Trevor L Wang
- John Innes Centre, Norwich Research Park, Norwich, UK
| | - John E Lunn
- Max Planck Institute of Molecular Plant Physiology, Wissenschaftspark Potsdam-Golm, Am Mühlenberg, Potsdam-Golm, Germany
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Direct Regulation of DNA Repair by E2F and RB in Mammals and Plants: Core Function or Convergent Evolution? Cancers (Basel) 2021; 13:cancers13050934. [PMID: 33668093 PMCID: PMC7956360 DOI: 10.3390/cancers13050934] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/31/2020] [Revised: 02/10/2021] [Accepted: 02/19/2021] [Indexed: 12/13/2022] Open
Abstract
Simple Summary Retinoblastoma (RB) proteins and E2F transcription factors partner together to regulate the cell cycle in many eukaryotic organisms. In organisms that lack one or both of these proteins, other proteins have taken on the essential function of cell cycle regulation. RB and E2F also have important functions outside of the cell cycle, including DNA repair. This review summarizes the non-canonical functions of RB and E2F in maintaining genome integrity and raises the question of whether such functions have always been present or have evolved more recently. Abstract Members of the E2F transcription factor family regulate the expression of genes important for DNA replication and mitotic cell division in most eukaryotes. Homologs of the retinoblastoma (RB) tumor suppressor inhibit the activity of E2F factors, thus controlling cell cycle progression. Organisms such as budding and fission yeast have lost genes encoding E2F and RB, but have gained genes encoding other proteins that take on E2F and RB cell cycle-related functions. In addition to regulating cell proliferation, E2F and RB homologs have non-canonical functions outside the mitotic cell cycle in a variety of eukaryotes. For example, in both mammals and plants, E2F and RB homologs localize to DNA double-strand breaks (DSBs) and directly promote repair by homologous recombination (HR). Here, we discuss the parallels between mammalian E2F1 and RB and their Arabidopsis homologs, E2FA and RB-related (RBR), with respect to their recruitment to sites of DNA damage and how they help recruit repair factors important for DNA end resection. We also explore the question of whether this role in DNA repair is a conserved ancient function of the E2F and RB homologs in the last eukaryotic common ancestor or whether this function evolved independently in mammals and plants.
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17
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Cabral LM, Masuda HP, Ballesteros HF, de Almeida-Engler J, Alves-Ferreira M, De Toni KLG, Bizotto FM, Ferreira PCG, Hemerly AS. ABAP1 Plays a Role in the Differentiation of Male and Female Gametes in Arabidopsis thaliana. FRONTIERS IN PLANT SCIENCE 2021; 12:642758. [PMID: 33643370 PMCID: PMC7903899 DOI: 10.3389/fpls.2021.642758] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Received: 12/16/2020] [Accepted: 01/22/2021] [Indexed: 05/07/2023]
Abstract
The correct development of a diploid sporophyte body and a haploid gametophyte relies on a strict coordination between cell divisions in space and time. During plant reproduction, these divisions have to be temporally and spatially coordinated with cell differentiation processes, to ensure a successful fertilization. Armadillo BTB Arabidopsis protein 1 (ABAP1) is a plant exclusive protein that has been previously reported to control proliferative cell divisions during leaf growth in Arabidopsis. Here, we show that ABAP1 binds to different transcription factors that regulate male and female gametophyte differentiation, repressing their target genes expression. During male gametogenesis, the ABAP1-TCP16 complex represses CDT1b transcription, and consequently regulates microspore first asymmetric mitosis. In the female gametogenesis, the ABAP1-ADAP complex represses EDA24-like transcription, regulating polar nuclei fusion to form the central cell. Therefore, besides its function during vegetative development, this work shows that ABAP1 is also involved in differentiation processes during plant reproduction, by having a dual role in regulating both the first asymmetric cell division of male gametophyte and the cell differentiation (or cell fusion) of female gametophyte.
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Affiliation(s)
- Luiz M. Cabral
- Instituto de Bioquímica Médica Leopoldo de Meis, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil
- Departamento de Biologia Celular e Molecular, Instituto de Biologia, Universidade Federal Fluminense, Niterói, Brazil
| | - Hana P. Masuda
- Instituto de Bioquímica Médica Leopoldo de Meis, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil
- Centro de Ciências Naturais e Humanas, Universidade Federal do ABC, São Bernardo do Campo, Brazil
| | - Helkin F. Ballesteros
- Instituto de Bioquímica Médica Leopoldo de Meis, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil
| | - Janice de Almeida-Engler
- Institut National de la Recherche Agronomique, Centre National de la Recherche Scientifique, Institut Sophia Agrobiotech, Université Côte d’Azur, Sophia Antipolis, France
| | - Márcio Alves-Ferreira
- Departamento de Genética, Instituto de Biologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil
| | - Karen L. G. De Toni
- Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, Rio de Janeiro, Brazil
| | - Fernanda M. Bizotto
- Centro de Ciências Naturais e Humanas, Universidade Federal do ABC, São Bernardo do Campo, Brazil
| | - Paulo C. G. Ferreira
- Instituto de Bioquímica Médica Leopoldo de Meis, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil
| | - Adriana S. Hemerly
- Instituto de Bioquímica Médica Leopoldo de Meis, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil
- *Correspondence: Adriana S. Hemerly, ;
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18
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Desvoyes B, Gutierrez C. Roles of plant retinoblastoma protein: cell cycle and beyond. EMBO J 2020; 39:e105802. [PMID: 32865261 PMCID: PMC7527812 DOI: 10.15252/embj.2020105802] [Citation(s) in RCA: 65] [Impact Index Per Article: 13.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/31/2020] [Revised: 07/16/2020] [Accepted: 08/06/2020] [Indexed: 12/16/2022] Open
Abstract
The human retinoblastoma (RB1) protein is a tumor suppressor that negatively regulates cell cycle progression through its interaction with members of the E2F/DP family of transcription factors. However, RB-related (RBR) proteins are an early acquisition during eukaryote evolution present in plant lineages, including unicellular algae, ancient plants (ferns, lycophytes, liverworts, mosses), gymnosperms, and angiosperms. The main RBR protein domains and interactions with E2Fs are conserved in all eukaryotes and not only regulate the G1/S transition but also the G2/M transition, as part of DREAM complexes. RBR proteins are also important for asymmetric cell division, stem cell maintenance, and the DNA damage response (DDR). RBR proteins play crucial roles at every developmental phase transition, in association with chromatin factors, as well as during the reproductive phase during female and male gametes production and embryo development. Here, we review the processes where plant RBR proteins play a role and discuss possible avenues of research to obtain a full picture of the multifunctional roles of RBR for plant life.
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19
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Jiang D, Borg M, Lorković ZJ, Montgomery SA, Osakabe A, Yelagandula R, Axelsson E, Berger F. The evolution and functional divergence of the histone H2B family in plants. PLoS Genet 2020; 16:e1008964. [PMID: 32716939 PMCID: PMC7410336 DOI: 10.1371/journal.pgen.1008964] [Citation(s) in RCA: 45] [Impact Index Per Article: 9.0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/11/2020] [Revised: 08/06/2020] [Accepted: 06/29/2020] [Indexed: 02/07/2023] Open
Abstract
Chromatin regulation of eukaryotic genomes depends on the formation of nucleosome complexes between histone proteins and DNA. Histone variants, which are diversified by sequence or expression pattern, can profoundly alter chromatin properties. While variants in histone H2A and H3 families are well characterized, the extent of diversification of histone H2B proteins is less understood. Here, we report a systematic analysis of the histone H2B family in plants, which have undergone substantial divergence during the evolution of each major group in the plant kingdom. By characterising Arabidopsis H2Bs, we substantiate this diversification and reveal potential functional specialization that parallels the phylogenetic structure of emergent clades in eudicots. In addition, we identify a new class of highly divergent H2B variants, H2B.S, that specifically accumulate during chromatin compaction of dry seed embryos in multiple species of flowering plants. Our findings thus identify unsuspected diverse properties among histone H2B proteins in plants that has manifested into potentially novel groups of histone variants. In addition to well-studied variants from core histones families H2A and H3, we report that land plants diversified their H2B family, leading to specialized H2B variants with specific patterns of expression, genomic distributions and properties.
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Affiliation(s)
- Danhua Jiang
- Gregor Mendel Institute, Austrian Academy of Sciences, Vienna BioCenter, Dr. Bohr-Gasse, Vienna, Austria
- State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, The Innovative Academy of Seed Design, Chinese Academy of Sciences, Beijing, China
- University of Chinese Academy of Sciences, Beijing, China
| | - Michael Borg
- Gregor Mendel Institute, Austrian Academy of Sciences, Vienna BioCenter, Dr. Bohr-Gasse, Vienna, Austria
| | - Zdravko J. Lorković
- Gregor Mendel Institute, Austrian Academy of Sciences, Vienna BioCenter, Dr. Bohr-Gasse, Vienna, Austria
| | - Sean A. Montgomery
- Gregor Mendel Institute, Austrian Academy of Sciences, Vienna BioCenter, Dr. Bohr-Gasse, Vienna, Austria
| | - Akihisa Osakabe
- Gregor Mendel Institute, Austrian Academy of Sciences, Vienna BioCenter, Dr. Bohr-Gasse, Vienna, Austria
| | - Ramesh Yelagandula
- Gregor Mendel Institute, Austrian Academy of Sciences, Vienna BioCenter, Dr. Bohr-Gasse, Vienna, Austria
| | - Elin Axelsson
- Gregor Mendel Institute, Austrian Academy of Sciences, Vienna BioCenter, Dr. Bohr-Gasse, Vienna, Austria
| | - Frédéric Berger
- Gregor Mendel Institute, Austrian Academy of Sciences, Vienna BioCenter, Dr. Bohr-Gasse, Vienna, Austria
- * E-mail:
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20
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Zluhan-Martínez E, Pérez-Koldenkova V, Ponce-Castañeda MV, Sánchez MDLP, García-Ponce B, Miguel-Hernández S, Álvarez-Buylla ER, Garay-Arroyo A. Beyond What Your Retina Can See: Similarities of Retinoblastoma Function between Plants and Animals, from Developmental Processes to Epigenetic Regulation. Int J Mol Sci 2020; 21:E4925. [PMID: 32664691 PMCID: PMC7404004 DOI: 10.3390/ijms21144925] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/28/2020] [Revised: 06/29/2020] [Accepted: 07/07/2020] [Indexed: 12/15/2022] Open
Abstract
The Retinoblastoma protein (pRb) is a key cell cycle regulator conserved in a wide variety of organisms. Experimental analysis of pRb's functions in animals and plants has revealed that this protein participates in cell proliferation and differentiation processes. In addition, pRb in animals and its orthologs in plants (RBR), are part of highly conserved protein complexes which suggest the possibility that analogies exist not only between functions carried out by pRb orthologs themselves, but also in the structure and roles of the protein networks where these proteins are involved. Here, we present examples of pRb/RBR participation in cell cycle control, cell differentiation, and in the regulation of epigenetic changes and chromatin remodeling machinery, highlighting the similarities that exist between the composition of such networks in plants and animals.
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Affiliation(s)
- Estephania Zluhan-Martínez
- Laboratorio de Genética Molecular, Epigenética, Desarrollo y Evolución de Plantas, Instituto de Ecología, Universidad Nacional Autónoma de Mexico, 3er Circuito Ext. Junto a J. Botánico, Ciudad Universitaria, UNAM 04510, Mexico; (E.Z.-M.); (M.d.l.P.S.); (B.G.-P.)
- Posgrado en Ciencias Biomédicas, Universidad Nacional Autónoma de México, Av. Universidad 3000, Coyoacán 04510, Mexico
| | - Vadim Pérez-Koldenkova
- Laboratorio Nacional de Microscopía Avanzada, Centro Médico Nacional Siglo XXI, Instituto Mexicano del Seguro Social, Av. Cuauhtémoc, 330. Col. Doctores, Alc. Cuauhtémoc 06720, Mexico;
| | - Martha Verónica Ponce-Castañeda
- Unidad de Investigación Médica en Enfermedades Infecciosas, Centro Médico Nacional SXXI, Instituto Mexicano del Seguro Social, Mexico City 06720, Mexico;
| | - María de la Paz Sánchez
- Laboratorio de Genética Molecular, Epigenética, Desarrollo y Evolución de Plantas, Instituto de Ecología, Universidad Nacional Autónoma de Mexico, 3er Circuito Ext. Junto a J. Botánico, Ciudad Universitaria, UNAM 04510, Mexico; (E.Z.-M.); (M.d.l.P.S.); (B.G.-P.)
| | - Berenice García-Ponce
- Laboratorio de Genética Molecular, Epigenética, Desarrollo y Evolución de Plantas, Instituto de Ecología, Universidad Nacional Autónoma de Mexico, 3er Circuito Ext. Junto a J. Botánico, Ciudad Universitaria, UNAM 04510, Mexico; (E.Z.-M.); (M.d.l.P.S.); (B.G.-P.)
| | - Sergio Miguel-Hernández
- Laboratorio de Citopatología Ambiental, Departamento de Morfología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Campus Zacatenco, Calle Wilfrido Massieu Esquina Cda, Manuel Stampa 07738, Mexico;
| | - Elena R. Álvarez-Buylla
- Laboratorio de Genética Molecular, Epigenética, Desarrollo y Evolución de Plantas, Instituto de Ecología, Universidad Nacional Autónoma de Mexico, 3er Circuito Ext. Junto a J. Botánico, Ciudad Universitaria, UNAM 04510, Mexico; (E.Z.-M.); (M.d.l.P.S.); (B.G.-P.)
| | - Adriana Garay-Arroyo
- Laboratorio de Genética Molecular, Epigenética, Desarrollo y Evolución de Plantas, Instituto de Ecología, Universidad Nacional Autónoma de Mexico, 3er Circuito Ext. Junto a J. Botánico, Ciudad Universitaria, UNAM 04510, Mexico; (E.Z.-M.); (M.d.l.P.S.); (B.G.-P.)
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21
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Singh S, Singh A, Singh A, Yadav S, Bajaj I, Kumar S, Jain A, Sarkar AK. Role of chromatin modification and remodeling in stem cell regulation and meristem maintenance in Arabidopsis. JOURNAL OF EXPERIMENTAL BOTANY 2020; 71:778-792. [PMID: 31793642 DOI: 10.1093/jxb/erz459] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.2] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 06/07/2019] [Accepted: 09/10/2019] [Indexed: 06/10/2023]
Abstract
In higher plants, pluripotent stem cells reside in the specialized microenvironment called stem cell niches (SCNs) harbored at the shoot apical meristem (SAM) and root apical meristem (RAM), which give rise to the aerial and underground parts of a plant, respectively. The model plant Arabidopsis thaliana (Arabidopsis) has been extensively studied to decipher the intricate regulatory mechanisms involving some key transcriptions factors and phytohormones that play pivotal roles in stem cell homeostasis, meristem maintenance, and organ formation. However, there is increasing evidence to show the epigenetic regulation of the chromatin architecture, gene expression exerting an influence on an innate balance between the self-renewal of stem cells, and differentiation of the progeny cells to a specific tissue type or organ. Post-translational histone modifications, ATP-dependent chromatin remodeling, and chromatin assembly/disassembly are some of the key features involved in the modulation of chromatin architecture. Here, we discuss the major epigenetic regulators and illustrate their roles in the regulation of stem cell activity, meristem maintenance, and related organ patterning in Arabidopsis.
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Affiliation(s)
- Sharmila Singh
- National Institute of Plant Genome Research, Aruna Asaf Ali Marg, New Delhi, India
| | - Alka Singh
- National Institute of Plant Genome Research, Aruna Asaf Ali Marg, New Delhi, India
| | - Archita Singh
- National Institute of Plant Genome Research, Aruna Asaf Ali Marg, New Delhi, India
| | - Sandeep Yadav
- National Institute of Plant Genome Research, Aruna Asaf Ali Marg, New Delhi, India
| | - Ishita Bajaj
- National Institute of Plant Genome Research, Aruna Asaf Ali Marg, New Delhi, India
| | - Shailendra Kumar
- Amity School of Architecture and Planning, Amity University, Kant Kalwar, Rajasthan, India
| | - Ajay Jain
- Amity Institute of Biotechnology, Amity University, Kant Kalwar, Rajasthan, India
| | - Ananda K Sarkar
- National Institute of Plant Genome Research, Aruna Asaf Ali Marg, New Delhi, India
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22
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Reynaldo GMR. The Final Origin of Cancer: Molecular Phylogeny. Cell 2020. [DOI: 10.4236/cellbio.2020.92005] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/20/2022]
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23
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Duan Y, Chen Y, Li W, Pan M, Qu X, Shi X, Cai Z, Liu H, Zhao F, Kong L, Ye Y, Wang F, Xue Y, Wu W. RETINOBLASTOMA-RELATED Genes Specifically Control Inner Floral Organ Morphogenesis and Pollen Development in Rice. PLANT PHYSIOLOGY 2019; 181:1600-1614. [PMID: 31548267 PMCID: PMC6878013 DOI: 10.1104/pp.19.00478] [Citation(s) in RCA: 13] [Impact Index Per Article: 2.2] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Received: 04/18/2019] [Accepted: 09/11/2019] [Indexed: 05/25/2023]
Abstract
RETINOBLASTOMA-RELATED (RBR) is an essential gene in plants, but its molecular function outside of its role in cell cycle entry remains poorly understood. We characterized the functions of OsRBR1 and OsRBR2 in plant growth and development in rice using both forward- and reverse-genetics methods. The two genes were coexpressed and performed redundant roles in vegetative organs but exhibited separate functions in flowers. OsRBR1 was highly expressed in the floral meristem and regulated the expression of floral homeotic genes to ensure floral organ formation. Mutation of OsRBR1 caused loss of floral meristem identity, resulting in the replacement of lodicules, stamens, and the pistil with either a panicle-like structure or whorls of lemma-like organs. OsRBR2 was preferentially expressed in stamens and promoted pollen formation. Mutation of OsRBR2 led to deformed anthers without pollen. Similar to the protein interaction between AtRBR and AtMSI1 that is essential for floral development in Arabidopsis, OsMSI1 was identified as an interaction partner of OsRBR1 and OsRBR2. OsMSI1 was ubiquitously expressed and appears to be essential for development in rice (Oryza sativa), as the mutation of OsMSI1 was lethal. These results suggest that OsRBR1 and OsRBR2 function with OsMSI1 in reproductive development in rice. This work characterizes further functions of RBRs and improves current understanding of specific regulatory pathways of floral specification and pollen formation in rice.
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Affiliation(s)
- Yuanlin Duan
- Key Laboratory of Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education and Fujian Provincial Key Laboratory of Crop Breeding by Design, Fujian Agriculture and Forestry University, Fuzhou 350002, China
| | - Yaguang Chen
- Key Laboratory of Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education and Fujian Provincial Key Laboratory of Crop Breeding by Design, Fujian Agriculture and Forestry University, Fuzhou 350002, China
| | - Wenqiang Li
- Key Laboratory of Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education and Fujian Provincial Key Laboratory of Crop Breeding by Design, Fujian Agriculture and Forestry University, Fuzhou 350002, China
| | - Meizhen Pan
- Key Laboratory of Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education and Fujian Provincial Key Laboratory of Crop Breeding by Design, Fujian Agriculture and Forestry University, Fuzhou 350002, China
| | - Xiaojie Qu
- Key Laboratory of Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education and Fujian Provincial Key Laboratory of Crop Breeding by Design, Fujian Agriculture and Forestry University, Fuzhou 350002, China
| | - Xiaoqing Shi
- Key Laboratory of Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education and Fujian Provincial Key Laboratory of Crop Breeding by Design, Fujian Agriculture and Forestry University, Fuzhou 350002, China
| | - Zhengzheng Cai
- Key Laboratory of Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education and Fujian Provincial Key Laboratory of Crop Breeding by Design, Fujian Agriculture and Forestry University, Fuzhou 350002, China
| | - Huaqing Liu
- Fujian Provincial Key Laboratory of Genetic Engineering for Agriculture, Fujian Academy of Agricultural Sciences, Fuzhou, Fujian 350003, China
| | - Fen Zhao
- Key Laboratory of Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education and Fujian Provincial Key Laboratory of Crop Breeding by Design, Fujian Agriculture and Forestry University, Fuzhou 350002, China
| | - Lan Kong
- Key Laboratory of Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education and Fujian Provincial Key Laboratory of Crop Breeding by Design, Fujian Agriculture and Forestry University, Fuzhou 350002, China
| | - Yanfang Ye
- Key Laboratory of Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education and Fujian Provincial Key Laboratory of Crop Breeding by Design, Fujian Agriculture and Forestry University, Fuzhou 350002, China
| | - Feng Wang
- Fujian Provincial Key Laboratory of Genetic Engineering for Agriculture, Fujian Academy of Agricultural Sciences, Fuzhou, Fujian 350003, China
| | - Yongbiao Xue
- State Key Laboratory of Plant Cell and Chromosome Engineering, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences and National Center for Plant Gene Research, Beijing 100101, China
| | - Weiren Wu
- Key Laboratory of Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education and Fujian Provincial Key Laboratory of Crop Breeding by Design, Fujian Agriculture and Forestry University, Fuzhou 350002, China
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24
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Featherston J, Arakaki Y, Hanschen ER, Ferris PJ, Michod RE, Olson BJSC, Nozaki H, Durand PM. The 4-Celled Tetrabaena socialis Nuclear Genome Reveals the Essential Components for Genetic Control of Cell Number at the Origin of Multicellularity in the Volvocine Lineage. Mol Biol Evol 2019; 35:855-870. [PMID: 29294063 DOI: 10.1093/molbev/msx332] [Citation(s) in RCA: 32] [Impact Index Per Article: 5.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/22/2022] Open
Abstract
Multicellularity is the premier example of a major evolutionary transition in individuality and was a foundational event in the evolution of macroscopic biodiversity. The volvocine chlorophyte lineage is well suited for studying this process. Extant members span unicellular, simple colonial, and obligate multicellular taxa with germ-soma differentiation. Here, we report the nuclear genome sequence of one of the most morphologically simple organisms in this lineage-the 4-celled colonial Tetrabaena socialis and compare this to the three other complete volvocine nuclear genomes. Using conservative estimates of gene family expansions a minimal set of expanded gene families was identified that associate with the origin of multicellularity. These families are rich in genes related to developmental processes. A subset of these families is lineage specific, which suggests that at a genomic level the evolution of multicellularity also includes lineage-specific molecular developments. Multiple points of evidence associate modifications to the ubiquitin proteasomal pathway (UPP) with the beginning of coloniality. Genes undergoing positive or accelerating selection in the multicellular volvocines were found to be enriched in components of the UPP and gene families gained at the origin of multicellularity include components of the UPP. A defining feature of colonial/multicellular life cycles is the genetic control of cell number. The genomic data presented here, which includes diversification of cell cycle genes and modifications to the UPP, align the genetic components with the evolution of this trait.
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Affiliation(s)
- Jonathan Featherston
- Evolutionary Studies Institute, University of the Witwatersrand, Johannesburg, South Africa.,Agricultural Research Council, Biotechnology Platform, Pretoria, South Africa
| | - Yoko Arakaki
- Department of Biological Sciences, Graduate School of Science, University of Tokyo, Bunkyo-ku, Tokyo, Hongo, Japan
| | - Erik R Hanschen
- Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ
| | - Patrick J Ferris
- Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ
| | - Richard E Michod
- Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ
| | | | - Hisayoshi Nozaki
- Department of Biological Sciences, Graduate School of Science, University of Tokyo, Bunkyo-ku, Tokyo, Hongo, Japan
| | - Pierre M Durand
- Evolutionary Studies Institute, University of the Witwatersrand, Johannesburg, South Africa
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25
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Umen JG. Sizing up the cell cycle: systems and quantitative approaches in Chlamydomonas. CURRENT OPINION IN PLANT BIOLOGY 2018; 46:96-103. [PMID: 30212737 PMCID: PMC6269190 DOI: 10.1016/j.pbi.2018.08.003] [Citation(s) in RCA: 16] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Received: 07/13/2018] [Revised: 08/14/2018] [Accepted: 08/16/2018] [Indexed: 05/06/2023]
Abstract
The unicellular green alga Chlamydomonas provides a simplified model for defining core cell cycle functions conserved in the green lineage and for understanding multiple fission, a common cell cycle variation found in many algae. Systems-level approaches including a recent groundbreaking screen for conditional lethal cell cycle mutants and genome-wide transcriptome analyses are revealing the complex relationships among cell cycle regulators and helping define roles for CDKA/CDK1 and CDKB, the latter of which is unique to the green lineage and plays a central role in mitotic regulation. Genetic screens and quantitative single-cell analyses have provided insight into cell-size control during multiple fission including the identification of a candidate `sizer' protein. Quantitative single-cell tracking and modeling are promising approaches for gaining additional insight into regulation of cellular and subcellular scaling during the Chlamydomonas cell cycle.
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Affiliation(s)
- James G Umen
- Donald Danforth Plant Science Center, 975 N. Warson Rd., St. Louis, MO 63132, USA.
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26
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Jafari S, Alizadeh H, Davoodi D, Jonoubi P, Majd A, Shobbar ZS, Zamani M. Changes in Cytomorphology, Expression of Retinoblastoma Related Gene, and Superoxide Dismutase Enzyme Activity in Maize Cell Culture Exposed to Silver Nanoparticles. IEEE Trans Nanobioscience 2018; 17:380-386. [PMID: 30028712 DOI: 10.1109/tnb.2018.2856512] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.1] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/10/2022]
Abstract
The ever-increasing use of silver nanoparticles (nAg) in various products necessitates investigation of the behavior of biological systems encountering these particles. In this paper, considering maize as a biological model, the effects of colloidal nAg (<80nm) on its cell culture were investigated. For comparison purposes, silver nitrate was used as a representative of silver ion (Ag+). After stabilization of cell suspensions, they were treated with nAg and Ag+ (1 mg/l), then cell suspension growth was measured and the microscopic analysis and a cell viability test were performed. In addition, the activity of superoxide dismutase (SOD) enzyme was explored. Owing to the key role of retinoblastoma-related protein (RBR) in cell cycle as well as in development and differentiation processes, the relative expression of ZmRBR1 was studied in nAg and Ag+ exposure. Microscopic analyses revealed that cells in suspensions treated by nAg and Ag+ were morphologically classified into five types: embryogenic; larvae-like; long; swollen; and polarized. The results showed an increase in percentages of large and live cells in the treated suspensions. Remarkably, we observed some cells which were differentiated into trichomes along with some stages of trichome development in the treated cell suspensions. Moreover, exposure to nAg and Ag+ did not elevate the activity of SOD enzyme in the treated cells. Also, the relative expression of ZmRBR1 was slightly reduced in the treated cells. The findings of these experimentations indicated that nAg affected maize suspension-cultured cells in the same manner as Ag+.
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27
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Negative regulator of E2F transcription factors links cell cycle checkpoint and DNA damage repair. Proc Natl Acad Sci U S A 2018; 115:E3837-E3845. [PMID: 29610335 DOI: 10.1073/pnas.1720094115] [Citation(s) in RCA: 36] [Impact Index Per Article: 5.1] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/17/2022] Open
Abstract
DNA damage poses a serious threat to genome integrity and greatly affects growth and development. To maintain genome stability, all organisms have evolved elaborate DNA damage response mechanisms including activation of cell cycle checkpoints and DNA repair. Here, we show that the DNA repair protein SNI1, a subunit of the evolutionally conserved SMC5/6 complex, directly links these two processes in Arabidopsis SNI1 binds to the activation domains of E2F transcription factors, the key regulators of cell cycle progression, and represses their transcriptional activities. In turn, E2Fs activate the expression of SNI1, suggesting that E2Fs and SNI1 form a negative feedback loop. Genetically, overexpression of SNI1 suppresses the phenotypes of E2F-overexpressing plants, and loss of E2F function fully suppresses the sni1 mutant, indicating that SNI1 is necessary and sufficient to inhibit E2Fs. Altogether, our study revealed that SNI1 is a negative regulator of E2Fs and plays dual roles in DNA damage responses by linking cell cycle checkpoint and DNA repair.
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28
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Glöckle B, Urban WJ, Nagahara S, Andersen ED, Higashiyama T, Grini PE, Schnittger A. Pollen differentiation as well as pollen tube guidance and discharge are independent of the presence of gametes. Development 2018; 145:dev.152645. [PMID: 29217755 PMCID: PMC5825867 DOI: 10.1242/dev.152645] [Citation(s) in RCA: 12] [Impact Index Per Article: 1.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/28/2017] [Accepted: 11/27/2017] [Indexed: 12/16/2022]
Abstract
After meiosis, an unequal cell division generates the male gamete lineage in flowering plants. The generative cell will undergo a second division, giving rise to the two gametes, i.e. the sperm cells. The other cell will develop into the vegetative cell that plays a crucial role in pollen tube formation and sperm delivery. Recently, the vegetative cell has been suggested to be important for programming of the chromatin state in sperm cells and/or the resulting fertilization products. Blocking the initial unequal division genetically, we first highlight that the default differentiation state after male meiosis is a vegetative fate, which is consistent with earlier work. We find that uni-nucleated mutant microspores differentiated as wild-type vegetative cells, including chromatin remodeling and the transcriptional activation of transposable elements. Moreover, live-cell imaging revealed that this vegetative cell is sufficient for the correct guidance of the pollen tube to the female gametes. Hence, we conclude that vegetative cell differentiation and function does not depend on the formation or presence of the actual gametes but rather on external signals or a cell-autonomous pace keeper. Summary: Cell biological analyses in Arabidopsis show that the vegetative cell differentiates without the presence of the actual gametes, and is solely sufficient for pollen tube germination, guidance, ovule penetration and pollen tube discharge.
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Affiliation(s)
- Barbara Glöckle
- Department of Molecular Mechanisms of Phenotypic Plasticity, Institut de Biologie Moléculaire des Plantes du CNRS, IBMP-CNRS - UPR2357, Université de Strasbourg, 12 Rue du Général Zimmer, 67084 Strasbourg Cedex, France.,Section for Genetics and Evolutionary Biology, Department of Biosciences, University of Oslo, 0316 Oslo, Norway
| | - Wojciech J Urban
- University of Hamburg, Biozentrum Klein Flottbek, Department of Developmental Biology, 22609 Hamburg, Germany
| | - Shiori Nagahara
- Institute of Transformative Bio-Molecules (WPI-ITbM), Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Aichi 464-8601, Japan
| | - Ellen D Andersen
- Section for Genetics and Evolutionary Biology, Department of Biosciences, University of Oslo, 0316 Oslo, Norway
| | - Tetsuya Higashiyama
- Institute of Transformative Bio-Molecules (WPI-ITbM), Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Aichi 464-8601, Japan.,JST ERATO Higashiyama Live-Holonics Project, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Aichi 464-8602, Japan
| | - Paul E Grini
- Section for Genetics and Evolutionary Biology, Department of Biosciences, University of Oslo, 0316 Oslo, Norway
| | - Arp Schnittger
- Department of Molecular Mechanisms of Phenotypic Plasticity, Institut de Biologie Moléculaire des Plantes du CNRS, IBMP-CNRS - UPR2357, Université de Strasbourg, 12 Rue du Général Zimmer, 67084 Strasbourg Cedex, France .,University of Hamburg, Biozentrum Klein Flottbek, Department of Developmental Biology, 22609 Hamburg, Germany
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29
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Biedermann S, Harashima H, Chen P, Heese M, Bouyer D, Sofroni K, Schnittger A. The retinoblastoma homolog RBR1 mediates localization of the repair protein RAD51 to DNA lesions in Arabidopsis. EMBO J 2017; 36:1279-1297. [PMID: 28320735 PMCID: PMC5412766 DOI: 10.15252/embj.201694571] [Citation(s) in RCA: 67] [Impact Index Per Article: 8.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/19/2016] [Revised: 02/17/2017] [Accepted: 02/20/2017] [Indexed: 11/13/2022] Open
Abstract
The retinoblastoma protein (Rb), which typically functions as a transcriptional repressor of E2F‐regulated genes, represents a major control hub of the cell cycle. Here, we show that loss of the Arabidopsis Rb homolog RETINOBLASTOMA‐RELATED 1 (RBR1) leads to cell death, especially upon exposure to genotoxic drugs such as the environmental toxin aluminum. While cell death can be suppressed by reduced cell‐proliferation rates, rbr1 mutant cells exhibit elevated levels of DNA lesions, indicating a direct role of RBR1 in the DNA‐damage response (DDR). Consistent with its role as a transcriptional repressor, we find that RBR1 directly binds to and represses key DDR genes such as RADIATION SENSITIVE 51 (RAD51), leaving it unclear why rbr1 mutants are hypersensitive to DNA damage. However, we find that RBR1 is also required for RAD51 localization to DNA lesions. We further show that RBR1 is itself targeted to DNA break sites in a CDKB1 activity‐dependent manner and partially co‐localizes with RAD51 at damage sites. Taken together, these results implicate RBR1 in the assembly of DNA‐bound repair complexes, in addition to its canonical function as a transcriptional regulator.
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Affiliation(s)
- Sascha Biedermann
- Department of Molecular Mechanisms of Phenotypic Plasticity, Institut de Biologie Moléculaire des Plantes du Centre National de la Recherche Scientifique, Université de Strasbourg, Strasbourg, France.,Department of Developmental Biology, Biozentrum Klein Flottbek University of Hamburg, Hamburg, Germany
| | | | - Poyu Chen
- Department of Developmental Biology, Biozentrum Klein Flottbek University of Hamburg, Hamburg, Germany
| | - Maren Heese
- Department of Developmental Biology, Biozentrum Klein Flottbek University of Hamburg, Hamburg, Germany
| | - Daniel Bouyer
- Institut de Biologie de l'Ecole Normale Supérieure, CNRS UMR 8197-INSERM U 1024, Paris, France
| | - Kostika Sofroni
- Department of Developmental Biology, Biozentrum Klein Flottbek University of Hamburg, Hamburg, Germany
| | - Arp Schnittger
- Department of Molecular Mechanisms of Phenotypic Plasticity, Institut de Biologie Moléculaire des Plantes du Centre National de la Recherche Scientifique, Université de Strasbourg, Strasbourg, France .,Department of Developmental Biology, Biozentrum Klein Flottbek University of Hamburg, Hamburg, Germany
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30
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Brasil JN, Costa CNM, Cabral LM, Ferreira PCG, Hemerly AS. The plant cell cycle: Pre-Replication complex formation and controls. Genet Mol Biol 2017; 40:276-291. [PMID: 28304073 PMCID: PMC5452130 DOI: 10.1590/1678-4685-gmb-2016-0118] [Citation(s) in RCA: 13] [Impact Index Per Article: 1.6] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/01/2016] [Accepted: 08/16/2016] [Indexed: 01/07/2023] Open
Abstract
The multiplication of cells in all living organisms requires a tight regulation of DNA replication. Several mechanisms take place to ensure that the DNA is replicated faithfully and just once per cell cycle in order to originate through mitoses two new daughter cells that contain exactly the same information from the previous one. A key control mechanism that occurs before cells enter S phase is the formation of a pre-replication complex (pre-RC) that is assembled at replication origins by the sequential association of the origin recognition complex, followed by Cdt1, Cdc6 and finally MCMs, licensing DNA to start replication. The identification of pre-RC members in all animal and plant species shows that this complex is conserved in eukaryotes and, more importantly, the differences between kingdoms might reflect their divergence in strategies on cell cycle regulation, as it must be integrated and adapted to the niche, ecosystem, and the organism peculiarities. Here, we provide an overview of the knowledge generated so far on the formation and the developmental controls of the pre-RC mechanism in plants, analyzing some particular aspects in comparison to other eukaryotes.
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Affiliation(s)
- Juliana Nogueira Brasil
- Instituto de Bioquímica Médica Leopoldo de Meis, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil.,Centro Universitário Christus, Fortaleza, CE, Brazil
| | - Carinne N Monteiro Costa
- Instituto de Bioquímica Médica Leopoldo de Meis, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil.,Centro de Genômica e Biologia de Sistemas, Universidade Federal do Pará, Belém, PA, Brazil
| | - Luiz Mors Cabral
- Departamento de Biologia Celular e Molecular, Universidade Federal Fluminense, Niteroi, RJ, Brazil
| | - Paulo C G Ferreira
- Instituto de Bioquímica Médica Leopoldo de Meis, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil
| | - Adriana S Hemerly
- Instituto de Bioquímica Médica Leopoldo de Meis, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil
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31
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Pillitteri LJ, Guo X, Dong J. Asymmetric cell division in plants: mechanisms of symmetry breaking and cell fate determination. Cell Mol Life Sci 2016; 73:4213-4229. [PMID: 27286799 PMCID: PMC5522748 DOI: 10.1007/s00018-016-2290-2] [Citation(s) in RCA: 35] [Impact Index Per Article: 3.9] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/15/2016] [Revised: 06/02/2016] [Accepted: 06/02/2016] [Indexed: 02/07/2023]
Abstract
Asymmetric cell division is a fundamental mechanism that generates cell diversity while maintaining self-renewing stem cell populations in multicellular organisms. Both intrinsic and extrinsic mechanisms underpin symmetry breaking and differential daughter cell fate determination in animals and plants. The emerging picture suggests that plants deal with the problem of symmetry breaking using unique cell polarity proteins, mobile transcription factors, and cell wall components to influence asymmetric divisions and cell fate. There is a clear role for altered auxin distribution and signaling in distinguishing two daughter cells and an emerging role for epigenetic modifications through chromatin remodelers and DNA methylation in plant cell differentiation. The importance of asymmetric cell division in determining final plant form provides the impetus for its study in the areas of both basic and applied science.
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Affiliation(s)
- Lynn Jo Pillitteri
- Department of Biology, Western Washington University, Bellingham, WA, 98225, USA
| | - Xiaoyu Guo
- Waksman Institute of Microbiology, Rutgers the State University of New Jersey, Piscataway, NJ, 08854, USA
| | - Juan Dong
- Waksman Institute of Microbiology, Rutgers the State University of New Jersey, Piscataway, NJ, 08854, USA.
- Department of Plant Biology and Pathology, Rutgers the State University of New Jersey, New Brunswick, NJ, 08901, USA.
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32
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Zhang Y, Zheng L, Hong JH, Gong X, Zhou C, Pérez-Pérez JM, Xu J. TOPOISOMERASE1α Acts through Two Distinct Mechanisms to Regulate Stele and Columella Stem Cell Maintenance. PLANT PHYSIOLOGY 2016; 171:483-93. [PMID: 26969721 PMCID: PMC4854680 DOI: 10.1104/pp.15.01754] [Citation(s) in RCA: 10] [Impact Index Per Article: 1.1] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 11/10/2015] [Accepted: 03/10/2016] [Indexed: 05/11/2023]
Abstract
TOPOISOMERASE1 (TOP1), which releases DNA torsional stress generated during replication through its DNA relaxation activity, plays vital roles in animal and plant development. In Arabidopsis (Arabidopsis thaliana), TOP1 is encoded by two paralogous genes (TOP1α and TOP1β), of which TOP1α displays specific developmental functions that are critical for the maintenance of shoot and floral stem cells. Here, we show that maintenance of two different populations of root stem cells is also dependent on TOP1α-specific developmental functions, which are exerted through two distinct novel mechanisms. In the proximal root meristem, the DNA relaxation activity of TOP1α is critical to ensure genome integrity and survival of stele stem cells (SSCs). Loss of TOP1α function triggers DNA double-strand breaks in S-phase SSCs and results in their death, which can be partially reversed by the replenishment of SSCs mediated by ETHYLENE RESPONSE FACTOR115 In the quiescent center and root cap meristem, TOP1α is epistatic to RETINOBLASTOMA-RELATED (RBR) in the maintenance of undifferentiated state and the number of columella stem cells (CSCs). Loss of TOP1α function in either wild-type or RBR RNAi plants leads to differentiation of CSCs, whereas overexpression of TOP1α mimics and further enhances the effect of RBR reduction that increases the number of CSCs Taken together, these findings provide important mechanistic insights into understanding stem cell maintenance in plants.
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Affiliation(s)
- Yonghong Zhang
- National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan 430070, China (Y.Z., L.Z., C.Z.);Department of Biological Sciences and NUS Centre for BioImaging Sciences, National University of Singapore, Singapore 117543 (J.H.H., X.G., J.X.); andInstituto de Bioingeniería, Universidad Miguel Hernández, 03202 Elche, Spain (J.M.P.-P.)
| | - Lanlan Zheng
- National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan 430070, China (Y.Z., L.Z., C.Z.);Department of Biological Sciences and NUS Centre for BioImaging Sciences, National University of Singapore, Singapore 117543 (J.H.H., X.G., J.X.); andInstituto de Bioingeniería, Universidad Miguel Hernández, 03202 Elche, Spain (J.M.P.-P.)
| | - Jing Han Hong
- National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan 430070, China (Y.Z., L.Z., C.Z.);Department of Biological Sciences and NUS Centre for BioImaging Sciences, National University of Singapore, Singapore 117543 (J.H.H., X.G., J.X.); andInstituto de Bioingeniería, Universidad Miguel Hernández, 03202 Elche, Spain (J.M.P.-P.)
| | - Ximing Gong
- National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan 430070, China (Y.Z., L.Z., C.Z.);Department of Biological Sciences and NUS Centre for BioImaging Sciences, National University of Singapore, Singapore 117543 (J.H.H., X.G., J.X.); andInstituto de Bioingeniería, Universidad Miguel Hernández, 03202 Elche, Spain (J.M.P.-P.)
| | - Chun Zhou
- National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan 430070, China (Y.Z., L.Z., C.Z.);Department of Biological Sciences and NUS Centre for BioImaging Sciences, National University of Singapore, Singapore 117543 (J.H.H., X.G., J.X.); andInstituto de Bioingeniería, Universidad Miguel Hernández, 03202 Elche, Spain (J.M.P.-P.)
| | - José Manuel Pérez-Pérez
- National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan 430070, China (Y.Z., L.Z., C.Z.);Department of Biological Sciences and NUS Centre for BioImaging Sciences, National University of Singapore, Singapore 117543 (J.H.H., X.G., J.X.); andInstituto de Bioingeniería, Universidad Miguel Hernández, 03202 Elche, Spain (J.M.P.-P.)
| | - Jian Xu
- National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan 430070, China (Y.Z., L.Z., C.Z.);Department of Biological Sciences and NUS Centre for BioImaging Sciences, National University of Singapore, Singapore 117543 (J.H.H., X.G., J.X.); andInstituto de Bioingeniería, Universidad Miguel Hernández, 03202 Elche, Spain (J.M.P.-P.)
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33
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Kohno S, Kitajima S, Sasaki N, Takahashi C. Retinoblastoma tumor suppressor functions shared by stem cell and cancer cell strategies. World J Stem Cells 2016; 8:170-84. [PMID: 27114748 PMCID: PMC4835675 DOI: 10.4252/wjsc.v8.i4.170] [Citation(s) in RCA: 12] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 10/28/2015] [Revised: 12/30/2015] [Accepted: 02/14/2016] [Indexed: 02/06/2023] Open
Abstract
Carcinogenic transformation of somatic cells resembles nuclear reprogramming toward the generation of pluripotent stem cells. These events share eternal escape from cellular senescence, continuous self-renewal in limited but certain population of cells, and refractoriness to terminal differentiation while maintaining the potential to differentiate into cells of one or multiple lineages. As represented by several oncogenes those appeared to be first keys to pluripotency, carcinogenesis and nuclear reprogramming seem to share a number of core mechanisms. The retinoblastoma tumor suppressor product retinoblastoma (RB) seems to be critically involved in both events in highly complicated manners. However, disentangling such complicated interactions has enabled us to better understand how stem cell strategies are shared by cancer cells. This review covers recent findings on RB functions related to stem cells and stem cell-like behaviors of cancer cells.
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Affiliation(s)
- Susumu Kohno
- Susumu Kohno, Chiaki Takahashi, Division of Oncology and Molecular Biology, Cancer Research Institute, Kanazawa University, Kanazawa, Ishikawa 920-1192, Japan
| | - Shunsuke Kitajima
- Susumu Kohno, Chiaki Takahashi, Division of Oncology and Molecular Biology, Cancer Research Institute, Kanazawa University, Kanazawa, Ishikawa 920-1192, Japan
| | - Nobunari Sasaki
- Susumu Kohno, Chiaki Takahashi, Division of Oncology and Molecular Biology, Cancer Research Institute, Kanazawa University, Kanazawa, Ishikawa 920-1192, Japan
| | - Chiaki Takahashi
- Susumu Kohno, Chiaki Takahashi, Division of Oncology and Molecular Biology, Cancer Research Institute, Kanazawa University, Kanazawa, Ishikawa 920-1192, Japan
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Harashima H, Sugimoto K. Integration of developmental and environmental signals into cell proliferation and differentiation through RETINOBLASTOMA-RELATED 1. CURRENT OPINION IN PLANT BIOLOGY 2016; 29:95-103. [PMID: 26799131 DOI: 10.1016/j.pbi.2015.12.003] [Citation(s) in RCA: 43] [Impact Index Per Article: 4.8] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 09/29/2015] [Revised: 12/03/2015] [Accepted: 12/06/2015] [Indexed: 05/23/2023]
Abstract
Plants continuously form new organs during post-embryonic development, thus progression of the proliferative cell cycle and subsequent transition into differentiation must be tightly controlled by developmental and environmental cues. Recent studies have begun to uncover how cell proliferation and cell differentiation are coordinated at the molecular level through tight transcriptional regulation of cell cycle and/or developmental regulators. Accumulating evidence suggests that RETINOBLASTOMA-RELATED 1 (RBR1), the Arabidopsis homolog of the human tumor suppressor Retinoblastoma (Rb), functions as a molecular hub linking cell proliferation, differentiation, and environmental response. In this review we will discuss recent findings on cell cycle regulation, highlighting the emerging roles of RBR1 as a key integrator of internal differentiation cues and external stimuli into the cell cycle machinery.
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Affiliation(s)
- Hirofumi Harashima
- RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro, Tsurumi, Yokohama, Kanagawa 230-0045, Japan
| | - Keiko Sugimoto
- RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro, Tsurumi, Yokohama, Kanagawa 230-0045, Japan.
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Schwarz EM, Roeder AHK. Transcriptomic Effects of the Cell Cycle Regulator LGO in Arabidopsis Sepals. FRONTIERS IN PLANT SCIENCE 2016; 7:1744. [PMID: 27920789 PMCID: PMC5118908 DOI: 10.3389/fpls.2016.01744] [Citation(s) in RCA: 14] [Impact Index Per Article: 1.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Received: 07/16/2016] [Accepted: 11/04/2016] [Indexed: 05/03/2023]
Abstract
Endoreduplication is a specialized cell cycle in which DNA replication occurs, but mitosis is skipped creating enlarged polyploid cells. Endoreduplication is associated with the differentiation of many specialized cell types. In the Arabidopsis thaliana sepal epidermis endoreduplicated giant cells form interspersed between smaller cells. Both the transcription factor Arabidopsis thaliana MERISTEM LAYER1 (ATML1) and the plant-specific cyclin dependent kinase inhibitor LOSS OF GIANT CELLS FROM ORGANS (LGO)/SIAMESE RELATED1 (SMR1) are required for the formation of giant cells. Overexpression of LGO is sufficient to produce sepals covered in highly endoreduplicated giant cells. Here we ask whether overexpression of LGO changes the transcriptome of these mature sepals. We show that overexpression of LGO in the epidermis (LGOoe) drives giant cell formation even in atml1 mutant sepals. Using RNA-seq we show that LGOoe has significant effects on the mature sepal transcriptome that are primarily ATML1-independent changes of gene activity. Genes activated by LGOoe, directly or indirectly, predominantly encode proteins involved in defense responses, including responses to wounding, insects (a predator of Arabidopsis), and fungus. They also encode components of the glucosinolate biosynthesis pathway, a key biochemical pathway in defense against herbivores. LGOoe-activated genes include previously known marker genes of systemic acquired resistance such as PR1 through PR5. The defensive functions promoted by LGOoe in sepals overlap with functions recently shown to be transcriptionally activated by hyperimmune cpr5 mutants in a LGO-dependent manner. Our findings show that the cell cycle regulator LGO can directly or indirectly drive specific states of gene expression; in particular, they are consistent with recent findings showing LGO to be necessary for transcriptional activation of many defense genes in Arabidopsis.
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Affiliation(s)
- Erich M. Schwarz
- Department of Molecular Biology and Genetics, Cornell University, IthacaNY, USA
| | - Adrienne H. K. Roeder
- Weill Institute for Cell and Molecular Biology and Section of Plant Biology, School of Integrative Plant Sciences, Cornell University, IthacaNY, USA
- *Correspondence: Adrienne H. K. Roeder,
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Thirugnanasambantham K, Saravanan S, Karikalan K, Bharanidharan R, Lalitha P, Ilango S, HairulIslam VI. Identification of evolutionarily conserved Momordica charantia microRNAs using computational approach and its utility in phylogeny analysis. Comput Biol Chem 2015; 58:25-39. [DOI: 10.1016/j.compbiolchem.2015.04.011] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/06/2015] [Revised: 04/04/2015] [Accepted: 04/24/2015] [Indexed: 11/25/2022]
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Transcriptional response to copper excess and identification of genes involved in heavy metal tolerance in the extremophilic microalga Chlamydomonas acidophila. Extremophiles 2015; 19:657-72. [DOI: 10.1007/s00792-015-0746-1] [Citation(s) in RCA: 14] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/19/2014] [Accepted: 03/23/2015] [Indexed: 01/05/2023]
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Scofield S, Jones A, Murray JAH. The plant cell cycle in context. JOURNAL OF EXPERIMENTAL BOTANY 2014; 65:2557-62. [PMID: 25025122 DOI: 10.1093/jxb/eru188] [Citation(s) in RCA: 41] [Impact Index Per Article: 3.7] [Reference Citation Analysis] [MESH Headings] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 05/12/2023]
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Desvoyes B, Fernández-Marcos M, Sequeira-Mendes J, Otero S, Vergara Z, Gutierrez C. Looking at plant cell cycle from the chromatin window. FRONTIERS IN PLANT SCIENCE 2014; 5:369. [PMID: 25120553 PMCID: PMC4110626 DOI: 10.3389/fpls.2014.00369] [Citation(s) in RCA: 32] [Impact Index Per Article: 2.9] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Received: 05/26/2014] [Accepted: 07/11/2014] [Indexed: 05/03/2023]
Abstract
The cell cycle is defined by a series of complex events, finely coordinated through hormonal, developmental and environmental signals, which occur in a unidirectional manner and end up in producing two daughter cells. Accumulating evidence reveals that chromatin is not a static entity throughout the cell cycle. In fact, there are many changes that include nucleosome remodeling, histone modifications, deposition and exchange, among others. Interestingly, it is possible to correlate the occurrence of several of these chromatin-related events with specific processes necessary for cell cycle progression, e.g., licensing of DNA replication origins, the E2F-dependent transcriptional wave in G1, the activation of replication origins in S-phase, the G2-specific transcription of genes required for mitosis or the chromatin packaging occurring in mitosis. Therefore, an emerging view is that chromatin dynamics must be considered as an intrinsic part of cell cycle regulation. In this article, we review the main features of several key chromatin events that occur at defined times throughout the cell cycle and discuss whether they are actually controlling the transit through specific cell cycle stages.
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Affiliation(s)
| | | | | | | | | | - Crisanto Gutierrez
- *Correspondence: Crisanto Gutierrez, Centro de Biologia Molecular Severo Ochoa, Consejo Superior de Investigaciones Cientificas, Universidad Autónoma de Madrid, Nicolas Cabrera 1, Cantoblanco, Madrid 28049, Spain e-mail:
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