Cell cycle acceleration and changes in essential nuclear functions induced by simulated microgravity in a synchronized Arabidopsis cell culture

K.Y. Kamal; R. Herranz; J.J.W.A. van Loon; F.J. Medina

doi:10.1111/pce.13422

Cell cycle acceleration and changes in essential nuclear functions induced by simulated microgravity in a synchronized Arabidopsis cell culture

K.Y. Kamal, R. Herranz, J.J.W.A. van Loon, F.J. Medina

Maxillofacial Surgery (VUmc)

Research output: Contribution to Journal › Article › Academic › peer-review

Abstract

Zero gravity is an environmental challenge unknown to organisms throughout evolution on Earth. Nevertheless, plants are sensitive to altered gravity, as exemplified by changes in meristematic cell proliferation and growth. We found that synchronized Arabidopsis‐cultured cells exposed to simulated microgravity showed a shortened cell cycle, caused by a shorter G2/M phase and a slightly longer G1 phase. The analysis of selected marker genes and proteins by quantitative polymerase chain reaction and flow cytometry in synchronic G1 and G2 subpopulations indicated changes in gene expression of core cell cycle regulators and chromatin‐modifying factors, confirming that microgravity induced misregulation of G2/M and G1/S checkpoints and chromatin remodelling. Changes in chromatin‐based regulation included higher DNA methylation and lower histone acetylation, increased chromatin condensation, and overall depletion of nuclear transcription. Estimation of ribosome biogenesis rate using nucleolar parameters and selected nucleolar genes and proteins indicated reduced nucleolar activity under simulated microgravity, especially at G2/M. These results expand our knowledge of how meristematic cells are affected by real and simulated microgravity. Counteracting this cellular stress is necessary for plant culture in space exploration.

Original language	English
Pages (from-to)	480-494
Journal	Plant, Cell and Environment
Volume	42
Issue number	2
DOIs	https://doi.org/10.1111/pce.13422
Publication status	Published - Feb 2019

Bibliographical note

Cited By :1

Export Date: 22 October 2019

CODEN: PLCED

Funding

Secretaría de Estado de Investigación, Desarrollo e Innovación, Grant/Award Numbers: AYA2012‐33982 and ESP2015‐64323‐ R; ESA, Grant/Award Numbers: 4200022650 and TEC‐MMG/2012/263; CSIC, Grant/ Award Number: JAEPre_2010_01894; Ministry of Economy, Industry and Competitiveness The skillful technical assistance of Mrs. Mercedes Carnota (CIB-CSIC) with different lab procedures is gratefully acknowledged, as well as the Technical Services of Genomics, Flow Cytometry, and Confocal Microscopy of CIB-CSIC for the assistance with the procedures and analyses of their respective specialities. We also thank Mr. Alan Dowson for his support at the TEC-MMG LIS lab (ESA-ESTEC) and Dr. Crisanto Gutierrez at CBM (UAM-CSIC) and Dr. Julio S?ez-V?squez (CNRS, University of Perpignan, Via Domitia, France) for the generous supply of MM2d cultures and antinucleolin antibody, respectively. This work was supported by the Spanish ?Plan Estatal de Investigaci?n Cient?fica y T?cnica y de Innovaci?n? of the Ministry of Economy, Industry and Competitiveness (Grants AYA2012-33982 and ESP2015-64323-R, cofunded by ERDF), by a predoctoral fellowship to Kh.?Y.?K. from CSIC, Spain (JAE-PreDoc Program, Ref. JAEPre_2010_01894), the ESA-ELIPS Program (ESA SEGMGSPE_Ph1 Project, contract number 4200022650), and ESA support via contract TEC-MMG/2012/263. This work is part of a PhD Thesis dissertation presented by Kh.?Y.?K. at the Complutense University of Madrid. The skillful technical assistance of Mrs. Mercedes Carnota (CIB‐CSIC) with different lab procedures is gratefully acknowledged, as well as the Technical Services of Genomics, Flow Cytometry, and Confocal Microscopy of CIB‐CSIC for the assistance with the procedures and analyses of their respective specialities. We also thank Mr. Alan Dowson for his support at the TEC‐MMG LIS lab (ESA‐ESTEC) and Dr. Crisanto Gutierrez at CBM (UAM‐CSIC) and Dr. Julio Sáez‐Vásquez (CNRS, University of Perpignan, Via Domitia, France) for the generous supply of MM2d cultures and antinucleolin antibody, respectively. This work was supported by the Spanish “Plan Estatal de Investigación Científica y Técnica y de Innovación” of the Ministry of Economy, Industry and Competitiveness (Grants AYA2012‐33982 and ESP2015‐64323‐R, cofunded by ERDF), by a predoctoral fellowship to Kh. Y. K. from CSIC, Spain (JAE‐PreDoc Program, Ref. JAEPre_2010_01894), the ESA‐ELIPS Program (ESA SEGMGSPE_Ph1 Project, contract number 4200022650), and ESA support via contract TEC‐MMG/2012/263. This work is part of a PhD Thesis dissertation presented by Kh. Y. K. at the Complutense University of Madrid.

Funders	Funder number
CSIC, Spain
ESA-ESTEC
UAM-CSIC
University of Perpignan
Ecological Society of America
Universidad Complutense de Madrid
Consejo Superior de Investigaciones Científicas	JAEPre_2010_01894
Centre National de la Recherche Scientifique
Secretaría de Estado de Investigación, Desarrollo e Innovación	AYA2012‐33982
Comisión Asesora de Investigación Científica y Técnica
European Regional Development Fund
Ecological Society of Australia	4200022650, TEC‐MMG/2012/263
Ministerio de Economía, Industria y Competitividad, Gobierno de España	ESP2015‐64323‐R

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10.1111/pce.13422

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title = "Cell cycle acceleration and changes in essential nuclear functions induced by simulated microgravity in a synchronized Arabidopsis cell culture",

abstract = "Zero gravity is an environmental challenge unknown to organisms throughout evolution on Earth. Nevertheless, plants are sensitive to altered gravity, as exemplified by changes in meristematic cell proliferation and growth. We found that synchronized Arabidopsis‐cultured cells exposed to simulated microgravity showed a shortened cell cycle, caused by a shorter G2/M phase and a slightly longer G1 phase. The analysis of selected marker genes and proteins by quantitative polymerase chain reaction and flow cytometry in synchronic G1 and G2 subpopulations indicated changes in gene expression of core cell cycle regulators and chromatin‐modifying factors, confirming that microgravity induced misregulation of G2/M and G1/S checkpoints and chromatin remodelling. Changes in chromatin‐based regulation included higher DNA methylation and lower histone acetylation, increased chromatin condensation, and overall depletion of nuclear transcription. Estimation of ribosome biogenesis rate using nucleolar parameters and selected nucleolar genes and proteins indicated reduced nucleolar activity under simulated microgravity, especially at G2/M. These results expand our knowledge of how meristematic cells are affected by real and simulated microgravity. Counteracting this cellular stress is necessary for plant culture in space exploration.",

author = "K.Y. Kamal and R. Herranz and {van Loon}, J.J.W.A. and F.J. Medina",

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T1 - Cell cycle acceleration and changes in essential nuclear functions induced by simulated microgravity in a synchronized Arabidopsis cell culture

AU - Kamal, K.Y.

AU - Herranz, R.

AU - van Loon, J.J.W.A.

AU - Medina, F.J.

N1 - Cited By :1 Export Date: 22 October 2019 CODEN: PLCED

PY - 2019/2

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N2 - Zero gravity is an environmental challenge unknown to organisms throughout evolution on Earth. Nevertheless, plants are sensitive to altered gravity, as exemplified by changes in meristematic cell proliferation and growth. We found that synchronized Arabidopsis‐cultured cells exposed to simulated microgravity showed a shortened cell cycle, caused by a shorter G2/M phase and a slightly longer G1 phase. The analysis of selected marker genes and proteins by quantitative polymerase chain reaction and flow cytometry in synchronic G1 and G2 subpopulations indicated changes in gene expression of core cell cycle regulators and chromatin‐modifying factors, confirming that microgravity induced misregulation of G2/M and G1/S checkpoints and chromatin remodelling. Changes in chromatin‐based regulation included higher DNA methylation and lower histone acetylation, increased chromatin condensation, and overall depletion of nuclear transcription. Estimation of ribosome biogenesis rate using nucleolar parameters and selected nucleolar genes and proteins indicated reduced nucleolar activity under simulated microgravity, especially at G2/M. These results expand our knowledge of how meristematic cells are affected by real and simulated microgravity. Counteracting this cellular stress is necessary for plant culture in space exploration.

AB - Zero gravity is an environmental challenge unknown to organisms throughout evolution on Earth. Nevertheless, plants are sensitive to altered gravity, as exemplified by changes in meristematic cell proliferation and growth. We found that synchronized Arabidopsis‐cultured cells exposed to simulated microgravity showed a shortened cell cycle, caused by a shorter G2/M phase and a slightly longer G1 phase. The analysis of selected marker genes and proteins by quantitative polymerase chain reaction and flow cytometry in synchronic G1 and G2 subpopulations indicated changes in gene expression of core cell cycle regulators and chromatin‐modifying factors, confirming that microgravity induced misregulation of G2/M and G1/S checkpoints and chromatin remodelling. Changes in chromatin‐based regulation included higher DNA methylation and lower histone acetylation, increased chromatin condensation, and overall depletion of nuclear transcription. Estimation of ribosome biogenesis rate using nucleolar parameters and selected nucleolar genes and proteins indicated reduced nucleolar activity under simulated microgravity, especially at G2/M. These results expand our knowledge of how meristematic cells are affected by real and simulated microgravity. Counteracting this cellular stress is necessary for plant culture in space exploration.

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DO - 10.1111/pce.13422

M3 - Article

SN - 0140-7791

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JO - Plant, Cell and Environment

JF - Plant, Cell and Environment

IS - 2

ER -

Cell cycle acceleration and changes in essential nuclear functions induced by simulated microgravity in a synchronized Arabidopsis cell culture

Abstract

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