Quantitative analysis of regulatory flexibility under changing environmental conditions

Abstract The circadian clock controls 24‐h rhythms in many biological processes, allowing appropriate timing of biological rhythms relative to dawn and dusk. Known clock circuits include multiple, interlocked feedback loops. Theory suggested that multiple loops contribute the flexibility for molecul...

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Main Authors: Kieron D Edwards, Ozgur E Akman, Kirsten Knox, Peter J Lumsden, Adrian W Thomson, Paul E Brown, Alexandra Pokhilko, Laszlo Kozma‐Bognar, Ferenc Nagy, David A Rand, Andrew J Millar
Format: Article
Language:English
Published: Springer Nature 2010-11-01
Series:Molecular Systems Biology
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Online Access:https://doi.org/10.1038/msb.2010.81
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author Kieron D Edwards
Ozgur E Akman
Kirsten Knox
Peter J Lumsden
Adrian W Thomson
Paul E Brown
Alexandra Pokhilko
Laszlo Kozma‐Bognar
Ferenc Nagy
David A Rand
Andrew J Millar
author_facet Kieron D Edwards
Ozgur E Akman
Kirsten Knox
Peter J Lumsden
Adrian W Thomson
Paul E Brown
Alexandra Pokhilko
Laszlo Kozma‐Bognar
Ferenc Nagy
David A Rand
Andrew J Millar
author_sort Kieron D Edwards
collection DOAJ
description Abstract The circadian clock controls 24‐h rhythms in many biological processes, allowing appropriate timing of biological rhythms relative to dawn and dusk. Known clock circuits include multiple, interlocked feedback loops. Theory suggested that multiple loops contribute the flexibility for molecular rhythms to track multiple phases of the external cycle. Clear dawn‐ and dusk‐tracking rhythms illustrate the flexibility of timing in Ipomoea nil. Molecular clock components in Arabidopsis thaliana showed complex, photoperiod‐dependent regulation, which was analysed by comparison with three contrasting models. A simple, quantitative measure, Dusk Sensitivity, was introduced to compare the behaviour of clock models with varying loop complexity. Evening‐expressed clock genes showed photoperiod‐dependent dusk sensitivity, as predicted by the three‐loop model, whereas the one‐ and two‐loop models tracked dawn and dusk, respectively. Output genes for starch degradation achieved dusk‐tracking expression through light regulation, rather than a dusk‐tracking rhythm. Model analysis predicted which biochemical processes could be manipulated to extend dusk tracking. Our results reveal how an operating principle of biological regulators applies specifically to the plant circadian clock.
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publishDate 2010-11-01
publisher Springer Nature
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series Molecular Systems Biology
spelling doaj-art-cf71725a5e234aefa766d930f55e26a42025-08-24T12:00:46ZengSpringer NatureMolecular Systems Biology1744-42922010-11-016111110.1038/msb.2010.81Quantitative analysis of regulatory flexibility under changing environmental conditionsKieron D Edwards0Ozgur E Akman1Kirsten Knox2Peter J Lumsden3Adrian W Thomson4Paul E Brown5Alexandra Pokhilko6Laszlo Kozma‐Bognar7Ferenc Nagy8David A Rand9Andrew J Millar10School of Biological Sciences, University of EdinburghCentre for Systems Biology at EdinburghSchool of Biological Sciences, University of EdinburghUniversity of Central LancashireSchool of Biological Sciences, University of EdinburghWarwick Systems Biology Centre, University of WarwickSchool of Biological Sciences, University of EdinburghBiological Research Centre of the Hungarian Academy of SciencesSchool of Biological Sciences, University of EdinburghWarwick Systems Biology Centre, University of WarwickSchool of Biological Sciences, University of EdinburghAbstract The circadian clock controls 24‐h rhythms in many biological processes, allowing appropriate timing of biological rhythms relative to dawn and dusk. Known clock circuits include multiple, interlocked feedback loops. Theory suggested that multiple loops contribute the flexibility for molecular rhythms to track multiple phases of the external cycle. Clear dawn‐ and dusk‐tracking rhythms illustrate the flexibility of timing in Ipomoea nil. Molecular clock components in Arabidopsis thaliana showed complex, photoperiod‐dependent regulation, which was analysed by comparison with three contrasting models. A simple, quantitative measure, Dusk Sensitivity, was introduced to compare the behaviour of clock models with varying loop complexity. Evening‐expressed clock genes showed photoperiod‐dependent dusk sensitivity, as predicted by the three‐loop model, whereas the one‐ and two‐loop models tracked dawn and dusk, respectively. Output genes for starch degradation achieved dusk‐tracking expression through light regulation, rather than a dusk‐tracking rhythm. Model analysis predicted which biochemical processes could be manipulated to extend dusk tracking. Our results reveal how an operating principle of biological regulators applies specifically to the plant circadian clock.https://doi.org/10.1038/msb.2010.81Arabidopsis thalianabiological clocksdynamical systemsgene regulatory networksmathematical modelsphotoperiodism
spellingShingle Kieron D Edwards
Ozgur E Akman
Kirsten Knox
Peter J Lumsden
Adrian W Thomson
Paul E Brown
Alexandra Pokhilko
Laszlo Kozma‐Bognar
Ferenc Nagy
David A Rand
Andrew J Millar
Quantitative analysis of regulatory flexibility under changing environmental conditions
Molecular Systems Biology
Arabidopsis thaliana
biological clocks
dynamical systems
gene regulatory networks
mathematical models
photoperiodism
title Quantitative analysis of regulatory flexibility under changing environmental conditions
title_full Quantitative analysis of regulatory flexibility under changing environmental conditions
title_fullStr Quantitative analysis of regulatory flexibility under changing environmental conditions
title_full_unstemmed Quantitative analysis of regulatory flexibility under changing environmental conditions
title_short Quantitative analysis of regulatory flexibility under changing environmental conditions
title_sort quantitative analysis of regulatory flexibility under changing environmental conditions
topic Arabidopsis thaliana
biological clocks
dynamical systems
gene regulatory networks
mathematical models
photoperiodism
url https://doi.org/10.1038/msb.2010.81
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