Meristematic cell proliferation and ribosome biogenesis are decoupled in diamagnetically levitated Arabidopsis seedlings

A.I. Manzano, O.J. Larkin, Camelia E. Dijkstra, P. Anthony, M.R. Davey, L. Eaves, R.J.A. Hill, R. Herranz, F.J. Medina

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    Abstract

    Background: Cell growth and cell proliferation are intimately linked in the presence of Earth's gravity, but are decoupled under the microgravity conditions present in orbiting spacecraft. New technologies to simulate microgravity conditions for long-duration experiments, with stable environmental conditions, in Earth-based laboratories are required to further our understanding of the effect of extraterrestrial conditions on the growth, development and health of living matter. Results: We studied the response of transgenic seedlings of Arabidopsis thaliana, containing either the CycB1-GUS proliferation marker or the DR5-GUS auxin-mediated growth marker, to diamagnetic levitation in the bore of a superconducting solenoid magnet. As a control, a second set of seedlings were exposed to a strong magnetic field, but not to levitation forces. A third set was exposed to a strong field and simulated hypergravity (2 g). Cell proliferation and cell growth cytological parameters were measured for each set of seedlings. Nucleolin immunodetection was used as a marker of cell growth. Collectively, the data indicate that these two fundamental cellular processes are decoupled in root meristems, as in microgravity: cell proliferation was enhanced whereas cell growth markers were depleted. These results also demonstrated delocalisation of auxin signalling in the root tip despite the fact that levitation of the seedling as a whole does not prevent the sedimentation of statoliths in the root cells. Conclusions: In our model system, we found that diamagnetic levitation led to changes that are very similar to those caused by real- [e.g. on board the International Space Station (ISS)] or mechanically-simulated microgravity [e.g. using a Random Positioning Machine (RPM)]. These changes decoupled meristematic cell proliferation from ribosome biogenesis, and altered auxin polar transport.
    Original languageEnglish
    Pages (from-to)124
    JournalBMC Plant Biology
    Volume13
    DOIs
    Publication statusPublished - 2013

    Fingerprint

    microgravity
    ribosomes
    cell growth
    cell proliferation
    Arabidopsis
    auxins
    seedlings
    solenoids
    root meristems
    magnetic fields
    root tips
    gravity
    growth and development
    Arabidopsis thaliana
    genetically modified organisms
    environmental factors
    duration
    biogenesis
    cells

    Bibliographical note

    This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

    Keywords

    • plant growth
    • plant cells
    • microgravity
    • hypergravity
    • hypogravity
    • diamagnetic levitation

    Cite this

    Manzano, A. I., Larkin, O. J., Dijkstra, C. E., Anthony, P., Davey, M. R., Eaves, L., ... Medina, F. J. (2013). Meristematic cell proliferation and ribosome biogenesis are decoupled in diamagnetically levitated Arabidopsis seedlings. BMC Plant Biology, 13, 124. https://doi.org/10.1186/1471-2229-13-124

    Meristematic cell proliferation and ribosome biogenesis are decoupled in diamagnetically levitated Arabidopsis seedlings. / Manzano, A.I.; Larkin, O.J.; Dijkstra, Camelia E.; Anthony, P.; Davey, M.R.; Eaves, L.; Hill, R.J.A.; Herranz, R.; Medina, F.J.

    In: BMC Plant Biology, Vol. 13, 2013, p. 124.

    Research output: Contribution to journalArticle

    Manzano, AI, Larkin, OJ, Dijkstra, CE, Anthony, P, Davey, MR, Eaves, L, Hill, RJA, Herranz, R & Medina, FJ 2013, 'Meristematic cell proliferation and ribosome biogenesis are decoupled in diamagnetically levitated Arabidopsis seedlings' BMC Plant Biology, vol. 13, pp. 124. https://doi.org/10.1186/1471-2229-13-124
    Manzano, A.I. ; Larkin, O.J. ; Dijkstra, Camelia E. ; Anthony, P. ; Davey, M.R. ; Eaves, L. ; Hill, R.J.A. ; Herranz, R. ; Medina, F.J. / Meristematic cell proliferation and ribosome biogenesis are decoupled in diamagnetically levitated Arabidopsis seedlings. In: BMC Plant Biology. 2013 ; Vol. 13. pp. 124.
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    T1 - Meristematic cell proliferation and ribosome biogenesis are decoupled in diamagnetically levitated Arabidopsis seedlings

    AU - Manzano, A.I.

    AU - Larkin, O.J.

    AU - Dijkstra, Camelia E.

    AU - Anthony, P.

    AU - Davey, M.R.

    AU - Eaves, L.

    AU - Hill, R.J.A.

    AU - Herranz, R.

    AU - Medina, F.J.

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    N2 - Background: Cell growth and cell proliferation are intimately linked in the presence of Earth's gravity, but are decoupled under the microgravity conditions present in orbiting spacecraft. New technologies to simulate microgravity conditions for long-duration experiments, with stable environmental conditions, in Earth-based laboratories are required to further our understanding of the effect of extraterrestrial conditions on the growth, development and health of living matter. Results: We studied the response of transgenic seedlings of Arabidopsis thaliana, containing either the CycB1-GUS proliferation marker or the DR5-GUS auxin-mediated growth marker, to diamagnetic levitation in the bore of a superconducting solenoid magnet. As a control, a second set of seedlings were exposed to a strong magnetic field, but not to levitation forces. A third set was exposed to a strong field and simulated hypergravity (2 g). Cell proliferation and cell growth cytological parameters were measured for each set of seedlings. Nucleolin immunodetection was used as a marker of cell growth. Collectively, the data indicate that these two fundamental cellular processes are decoupled in root meristems, as in microgravity: cell proliferation was enhanced whereas cell growth markers were depleted. These results also demonstrated delocalisation of auxin signalling in the root tip despite the fact that levitation of the seedling as a whole does not prevent the sedimentation of statoliths in the root cells. Conclusions: In our model system, we found that diamagnetic levitation led to changes that are very similar to those caused by real- [e.g. on board the International Space Station (ISS)] or mechanically-simulated microgravity [e.g. using a Random Positioning Machine (RPM)]. These changes decoupled meristematic cell proliferation from ribosome biogenesis, and altered auxin polar transport.

    AB - Background: Cell growth and cell proliferation are intimately linked in the presence of Earth's gravity, but are decoupled under the microgravity conditions present in orbiting spacecraft. New technologies to simulate microgravity conditions for long-duration experiments, with stable environmental conditions, in Earth-based laboratories are required to further our understanding of the effect of extraterrestrial conditions on the growth, development and health of living matter. Results: We studied the response of transgenic seedlings of Arabidopsis thaliana, containing either the CycB1-GUS proliferation marker or the DR5-GUS auxin-mediated growth marker, to diamagnetic levitation in the bore of a superconducting solenoid magnet. As a control, a second set of seedlings were exposed to a strong magnetic field, but not to levitation forces. A third set was exposed to a strong field and simulated hypergravity (2 g). Cell proliferation and cell growth cytological parameters were measured for each set of seedlings. Nucleolin immunodetection was used as a marker of cell growth. Collectively, the data indicate that these two fundamental cellular processes are decoupled in root meristems, as in microgravity: cell proliferation was enhanced whereas cell growth markers were depleted. These results also demonstrated delocalisation of auxin signalling in the root tip despite the fact that levitation of the seedling as a whole does not prevent the sedimentation of statoliths in the root cells. Conclusions: In our model system, we found that diamagnetic levitation led to changes that are very similar to those caused by real- [e.g. on board the International Space Station (ISS)] or mechanically-simulated microgravity [e.g. using a Random Positioning Machine (RPM)]. These changes decoupled meristematic cell proliferation from ribosome biogenesis, and altered auxin polar transport.

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