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The auxin signalling network translates dynamic input into robust patterning at the shoot apex

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Vernoux, Teva, Brunoud, Géraldine, Farcot, Etienne, Morin, Valérie, Van den Daele, Hilde, Legrand, Jonathan, Oliva, Marina, Das, Pradeep +16 more·2011·Molecular Systems Biology
DOI 10.1038/msb.2011.39PMC PMC3167386
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Abstract

The plant hormone auxin is thought to provide positional information for patterning during development. It is still unclear, however, precisely how auxin is distributed across tissues and how the hormone is sensed in space and time. The control of gene expression in response to auxin involves a complex network of over 50 potentially interacting transcriptional activators and repressors, the auxin response factors (ARFs) and Aux/IAAs. Here, we perform a large-scale analysis of the Aux/IAA-ARF pathway in the shoot apex of Arabidopsis, where dynamic auxin-based patterning controls organogenesis. A comprehensive expression map and full interactome uncovered an unexpectedly simple distribution and structure of this pathway in the shoot apex. A mathematical model of the Aux/IAA-ARF network predicted a strong buffering capacity along with spatial differences in auxin sensitivity. We then tested and confirmed these predictions using a novel auxin signalling sensor that reports input into the signalling pathway, in conjunction with the published DR5 transcriptional output reporter. Our results provide evidence that the auxin signalling network is essential to create robust patterns at the shoot apex.

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  • The boundary between the floral meristem and the inflorescence meristem constitutes a low-auxin environment.

    “Therefore, the boundary between the floral meristem and the inflorescence meristem also constitutes a lowauxin environment (Heisler et al., 2005;Vernoux et al., 2011).”

    From <i>Divide et impera</i>: boundaries shape the plant body and initiate new meristems (2016) · cites this paper as Vernoux et al., 2011

    The Results report low auxin-signalling input in cells immediately surrounding flower primordia. The Discussion says sensor accumulation at organ frontiers likely indicates low auxin concentration in those surrounding cells. This supports the proposed location, but the unqualified claim of a low-auxin environment is stronger than the paper’s qualified inference about concentration. (LLM, conf=0.82)

    Experimental — accuracy not yet measured

  • Ectopic auxin minima were detected in abaxial leaf axils using DII-Venus.

    “Notably, we also detected ectopic auxin minima in abaxial leaf axils by using the auxin concentration sensor DII-Venus [46], whose strong abaxial axil signal indicates low auxin concentrations (S3F–S3I Fig).”

    From Two-Step Regulation of a Meristematic Cell Population Acting in Shoot Branching in Arabidopsis (2016) · cites this paper as [46]

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Authors
Vernoux, T., Brunoud, G., Farcot, E., Morin, V., Van den Daele, H., Legrand, J., Oliva, M., Das, P., Larrieu, A., Wells, D., Guédon, Y., Armitage, L., Picard, F., Guyomarc'h, S., Cellier, C., Parry, G., Koumproglou, R., Doonan, J. H., Estelle, M., Godin, C., Kepinski, S., Bennett, M., De Veylder, L., & Traas, J.
Affiliations
  • Lyon 1 Université (FR)
  • Centre de Coopération Internationale en Recherche Agronomique pour le Développement (FR)
  • University of Nottingham (GB)
  • University of Leeds (GB)
  • University of California San Diego (US)
  • John Innes Centre (GB)
Corresponding author
Vernoux, Teva
ORCID
Venue
Molecular Systems Biology
Publisher
Springer Science and Business Media LLC
Published
2011-07-05
Volume
7
Issue
1
Pages
508-508
ISSN
1744-4292 (ISSN-L)
DOI
10.1038/msb.2011.39
PMC
PMC3167386
OpenAlex
W2148572458
Cited by
576
References
2
Citations by year
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FWCI
60.56
Type
journal article
Language
en
Open access
Licence
Locations
  • Molecular Systems Biology (publishedVersion, cc-by-nc-nd)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • UWA Profiles and Research Repository (UWA) (publishedVersion, other-oa)
  • PubMed (publishedVersion)
  • White Rose Research Online (University of Leeds, The University of Sheffield, University of York) (acceptedVersion)
  • Repository@Nottingham (University of Nottingham) (submittedVersion, cc-by-nc-nd)
  • HAL (submittedVersion, cc-by)
  • Agritrop (Cirad) (submittedVersion)
  • Ghent University Academic Bibliography (Ghent University) (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
  • Agence Nationale de la Recherche (ANR-07-JCJC-0115, ANR-08-BLAN-0304)
  • Kementerian Pendidikan Nasional
  • Vlaamse regering
  • Biotechnology and Biological Sciences Research Council (BB/F007418/1, BBS/E/J/0000A216, BB/F013981/1)
  • National Institute of General Medical Sciences (R01GM043644)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Parasitism and Resistance
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Keywords
auxin signaling, shoot apex, organogenesis, positional information, transcriptional repressor, transcriptional activator, protein-protein interaction network, mathematical modeling, buffering capacity, auxin sensitivity, DR5 reporter, Arabidopsis thaliana
MeSH terms
DNA-Binding Proteins, Indoleacetic Acids, Models, Theoretical, Nuclear Proteins, Plant Growth Regulators, Transcription, Genetic, Signal Transduction, Cluster Analysis, Genes, Plant, Arabidopsis, In Situ Hybridization, Fluorescence, Gene Expression Regulation, Plant, Meristem, Plant Shoots, Microscopy, Confocal, Arabidopsis Proteins, Plants, Genetically Modified, Organogenesis

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