Coordination of robust single cell rhythms in the Arabidopsis circadian clock via spatial waves of gene expression

The Arabidopsis circadian clock orchestrates gene regulation across the day/night cycle. Although a multiple feedback loop circuit has been shown to generate the 24-hr rhythm, it remains unclear how robust the clock is in individual cells, or how clock timing is coordinated across the plant. Here we...

Full description

Bibliographic Details
Main Authors: Peter D Gould, Mirela Domijan, Mark Greenwood, Isao T Tokuda, Hannah Rees, Laszlo Kozma-Bognar, Anthony JW Hall, James CW Locke
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2018-04-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/31700
id doaj-471394de120b4eee82cc6463b716b138
record_format Article
spelling doaj-471394de120b4eee82cc6463b716b1382021-05-05T15:49:31ZengeLife Sciences Publications LtdeLife2050-084X2018-04-01710.7554/eLife.31700Coordination of robust single cell rhythms in the Arabidopsis circadian clock via spatial waves of gene expressionPeter D Gould0Mirela Domijan1https://orcid.org/0000-0003-3853-9119Mark Greenwood2Isao T Tokuda3https://orcid.org/0000-0001-6212-0022Hannah Rees4Laszlo Kozma-Bognar5https://orcid.org/0000-0002-8289-193XAnthony JW Hall6James CW Locke7https://orcid.org/0000-0003-0670-1943Institute of Integrative Biology, University of Liverpool, Liverpool, United KingdomSainsbury Laboratory, University of Cambridge, Cambridge, United Kingdom; Department of Mathematical Sciences, University of Liverpool, Liverpool, United KingdomInstitute of Integrative Biology, University of Liverpool, Liverpool, United Kingdom; Sainsbury Laboratory, University of Cambridge, Cambridge, United Kingdom; Department of Biochemistry, University of Cambridge, Cambridge, United KingdomDepartment of Mechanical Engineering, Ritsumeikan University, Kusatsu, JapanInstitute of Integrative Biology, University of Liverpool, Liverpool, United KingdomBiological Research Centre, Hungarian Academy of Sciences, Szeged, Hungary; Department of Genetics, University of Szeged, Szeged, HungaryInstitute of Integrative Biology, University of Liverpool, Liverpool, United Kingdom; Earlham Institute, Norwich Research Park, Norwich, United KingdomSainsbury Laboratory, University of Cambridge, Cambridge, United Kingdom; Department of Biochemistry, University of Cambridge, Cambridge, United Kingdom; Microsoft Research, Cambridge, United KingdomThe Arabidopsis circadian clock orchestrates gene regulation across the day/night cycle. Although a multiple feedback loop circuit has been shown to generate the 24-hr rhythm, it remains unclear how robust the clock is in individual cells, or how clock timing is coordinated across the plant. Here we examine clock activity at the single cell level across Arabidopsis seedlings over several days under constant environmental conditions. Our data reveal robust single cell oscillations, albeit desynchronised. In particular, we observe two waves of clock activity; one going down, and one up the root. We also find evidence of cell-to-cell coupling of the clock, especially in the root tip. A simple model shows that cell-to-cell coupling and our measured period differences between cells can generate the observed waves. Our results reveal the spatial structure of the plant clock and suggest that unlike the centralised mammalian clock, the Arabidopsis clock has multiple coordination points.https://elifesciences.org/articles/31700single celltime-lapse microscopycircadian clockcell-to-cell coupling
collection DOAJ
language English
format Article
sources DOAJ
author Peter D Gould
Mirela Domijan
Mark Greenwood
Isao T Tokuda
Hannah Rees
Laszlo Kozma-Bognar
Anthony JW Hall
James CW Locke
spellingShingle Peter D Gould
Mirela Domijan
Mark Greenwood
Isao T Tokuda
Hannah Rees
Laszlo Kozma-Bognar
Anthony JW Hall
James CW Locke
Coordination of robust single cell rhythms in the Arabidopsis circadian clock via spatial waves of gene expression
eLife
single cell
time-lapse microscopy
circadian clock
cell-to-cell coupling
author_facet Peter D Gould
Mirela Domijan
Mark Greenwood
Isao T Tokuda
Hannah Rees
Laszlo Kozma-Bognar
Anthony JW Hall
James CW Locke
author_sort Peter D Gould
title Coordination of robust single cell rhythms in the Arabidopsis circadian clock via spatial waves of gene expression
title_short Coordination of robust single cell rhythms in the Arabidopsis circadian clock via spatial waves of gene expression
title_full Coordination of robust single cell rhythms in the Arabidopsis circadian clock via spatial waves of gene expression
title_fullStr Coordination of robust single cell rhythms in the Arabidopsis circadian clock via spatial waves of gene expression
title_full_unstemmed Coordination of robust single cell rhythms in the Arabidopsis circadian clock via spatial waves of gene expression
title_sort coordination of robust single cell rhythms in the arabidopsis circadian clock via spatial waves of gene expression
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2018-04-01
description The Arabidopsis circadian clock orchestrates gene regulation across the day/night cycle. Although a multiple feedback loop circuit has been shown to generate the 24-hr rhythm, it remains unclear how robust the clock is in individual cells, or how clock timing is coordinated across the plant. Here we examine clock activity at the single cell level across Arabidopsis seedlings over several days under constant environmental conditions. Our data reveal robust single cell oscillations, albeit desynchronised. In particular, we observe two waves of clock activity; one going down, and one up the root. We also find evidence of cell-to-cell coupling of the clock, especially in the root tip. A simple model shows that cell-to-cell coupling and our measured period differences between cells can generate the observed waves. Our results reveal the spatial structure of the plant clock and suggest that unlike the centralised mammalian clock, the Arabidopsis clock has multiple coordination points.
topic single cell
time-lapse microscopy
circadian clock
cell-to-cell coupling
url https://elifesciences.org/articles/31700
work_keys_str_mv AT peterdgould coordinationofrobustsinglecellrhythmsinthearabidopsiscircadianclockviaspatialwavesofgeneexpression
AT mireladomijan coordinationofrobustsinglecellrhythmsinthearabidopsiscircadianclockviaspatialwavesofgeneexpression
AT markgreenwood coordinationofrobustsinglecellrhythmsinthearabidopsiscircadianclockviaspatialwavesofgeneexpression
AT isaottokuda coordinationofrobustsinglecellrhythmsinthearabidopsiscircadianclockviaspatialwavesofgeneexpression
AT hannahrees coordinationofrobustsinglecellrhythmsinthearabidopsiscircadianclockviaspatialwavesofgeneexpression
AT laszlokozmabognar coordinationofrobustsinglecellrhythmsinthearabidopsiscircadianclockviaspatialwavesofgeneexpression
AT anthonyjwhall coordinationofrobustsinglecellrhythmsinthearabidopsiscircadianclockviaspatialwavesofgeneexpression
AT jamescwlocke coordinationofrobustsinglecellrhythmsinthearabidopsiscircadianclockviaspatialwavesofgeneexpression
_version_ 1721459771644575744