Integration of hormonal signaling networks and mobile microRNAs is required for vascular patterning in Arabidopsis roots

Handle URI:
http://hdl.handle.net/10754/598640
Title:
Integration of hormonal signaling networks and mobile microRNAs is required for vascular patterning in Arabidopsis roots
Authors:
Muraro, D.; Mellor, N.; Pound, M. P.; Help, H.; Lucas, M.; Chopard, J.; Byrne, H. M.; Godin, C.; Hodgman, T. C.; King, J. R.; Pridmore, T. P.; Helariutta, Y.; Bennett, M. J.; Bishopp, A.
Abstract:
As multicellular organisms grow, positional information is continually needed to regulate the pattern in which cells are arranged. In the Arabidopsis root, most cell types are organized in a radially symmetric pattern; however, a symmetry-breaking event generates bisymmetric auxin and cytokinin signaling domains in the stele. Bidirectional cross-talk between the stele and the surrounding tissues involving a mobile transcription factor, SHORT ROOT (SHR), and mobile microRNA species also determines vascular pattern, but it is currently unclear how these signals integrate. We use a multicellular model to determine a minimal set of components necessary for maintaining a stable vascular pattern. Simulations perturbing the signaling network show that, in addition to the mutually inhibitory interaction between auxin and cytokinin, signaling through SHR, microRNA165/6, and PHABULOSA is required to maintain a stable bisymmetric pattern. We have verified this prediction by observing loss of bisymmetry in shr mutants. The model reveals the importance of several features of the network, namely the mutual degradation of microRNA165/6 and PHABULOSA and the existence of an additional negative regulator of cytokinin signaling. These components form a plausible mechanism capable of patterning vascular tissues in the absence of positional inputs provided by the transport of hormones from the shoot.
Citation:
Muraro D, Mellor N, Pound MP, Help H, Lucas M, et al. (2013) Integration of hormonal signaling networks and mobile microRNAs is required for vascular patterning in Arabidopsis roots. Proceedings of the National Academy of Sciences 111: 857–862. Available: http://dx.doi.org/10.1073/pnas.1221766111.
Publisher:
Proceedings of the National Academy of Sciences
Journal:
Proceedings of the National Academy of Sciences
KAUST Grant Number:
KUK-013-04
Issue Date:
31-Dec-2013
DOI:
10.1073/pnas.1221766111
PubMed ID:
24381155
PubMed Central ID:
PMC3896157
Type:
Article
ISSN:
0027-8424; 1091-6490
Sponsors:
We thank Leah Band for helpful comments. We acknowledge the Biotechnology and Biological Sciences Research Council and the Engineering and Physical Sciences Research Council for funding. H. M. B. was funded, in part, by King Abdullah University of Science and Technology (KAUST) Award KUK-013-04, J.R.K. was funded by the Royal Society and Wolfson Foundation, and A. B. was funded by a Royal Society University Research Fellowship. J.G and C. G. were funded by the Institut de Biologie Computationnelle de Montpellier and the Morphogenetics Inria Project-Lab.
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Full metadata record

DC FieldValue Language
dc.contributor.authorMuraro, D.en
dc.contributor.authorMellor, N.en
dc.contributor.authorPound, M. P.en
dc.contributor.authorHelp, H.en
dc.contributor.authorLucas, M.en
dc.contributor.authorChopard, J.en
dc.contributor.authorByrne, H. M.en
dc.contributor.authorGodin, C.en
dc.contributor.authorHodgman, T. C.en
dc.contributor.authorKing, J. R.en
dc.contributor.authorPridmore, T. P.en
dc.contributor.authorHelariutta, Y.en
dc.contributor.authorBennett, M. J.en
dc.contributor.authorBishopp, A.en
dc.date.accessioned2016-02-25T13:33:37Zen
dc.date.available2016-02-25T13:33:37Zen
dc.date.issued2013-12-31en
dc.identifier.citationMuraro D, Mellor N, Pound MP, Help H, Lucas M, et al. (2013) Integration of hormonal signaling networks and mobile microRNAs is required for vascular patterning in Arabidopsis roots. Proceedings of the National Academy of Sciences 111: 857–862. Available: http://dx.doi.org/10.1073/pnas.1221766111.en
dc.identifier.issn0027-8424en
dc.identifier.issn1091-6490en
dc.identifier.pmid24381155en
dc.identifier.doi10.1073/pnas.1221766111en
dc.identifier.urihttp://hdl.handle.net/10754/598640en
dc.description.abstractAs multicellular organisms grow, positional information is continually needed to regulate the pattern in which cells are arranged. In the Arabidopsis root, most cell types are organized in a radially symmetric pattern; however, a symmetry-breaking event generates bisymmetric auxin and cytokinin signaling domains in the stele. Bidirectional cross-talk between the stele and the surrounding tissues involving a mobile transcription factor, SHORT ROOT (SHR), and mobile microRNA species also determines vascular pattern, but it is currently unclear how these signals integrate. We use a multicellular model to determine a minimal set of components necessary for maintaining a stable vascular pattern. Simulations perturbing the signaling network show that, in addition to the mutually inhibitory interaction between auxin and cytokinin, signaling through SHR, microRNA165/6, and PHABULOSA is required to maintain a stable bisymmetric pattern. We have verified this prediction by observing loss of bisymmetry in shr mutants. The model reveals the importance of several features of the network, namely the mutual degradation of microRNA165/6 and PHABULOSA and the existence of an additional negative regulator of cytokinin signaling. These components form a plausible mechanism capable of patterning vascular tissues in the absence of positional inputs provided by the transport of hormones from the shoot.en
dc.description.sponsorshipWe thank Leah Band for helpful comments. We acknowledge the Biotechnology and Biological Sciences Research Council and the Engineering and Physical Sciences Research Council for funding. H. M. B. was funded, in part, by King Abdullah University of Science and Technology (KAUST) Award KUK-013-04, J.R.K. was funded by the Royal Society and Wolfson Foundation, and A. B. was funded by a Royal Society University Research Fellowship. J.G and C. G. were funded by the Institut de Biologie Computationnelle de Montpellier and the Morphogenetics Inria Project-Lab.en
dc.publisherProceedings of the National Academy of Sciencesen
dc.subjectPlant developmenten
dc.subjectMathematical Modelingen
dc.subject.meshModels, Biologicalen
dc.titleIntegration of hormonal signaling networks and mobile microRNAs is required for vascular patterning in Arabidopsis rootsen
dc.typeArticleen
dc.identifier.journalProceedings of the National Academy of Sciencesen
dc.identifier.pmcidPMC3896157en
dc.contributor.institutionCentre for Plant Integrative Biology, School of Biosciences, University of Nottingham, Loughborough LE12 5RD, United Kingdom.en
kaust.grant.numberKUK-013-04en

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