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Cell type boundaries organize plant development

Pia Caggiano, Monica and Yu, Xiulian and Bhatia, Neha and Larsson, André and Ram, Hasthi and Ohno, Carolyn K. and Sappl, Pia and Meyerowitz, Elliot M. and Jönsson, Henrik and Heisler, Marcus G. (2017) Cell type boundaries organize plant development. eLife, 6 . Art. No. e27421. ISSN 2050-084X. PMCID PMC5617630. https://resolver.caltech.edu/CaltechAUTHORS:20170918-104527805

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Abstract

In plants the dorsoventral boundary of leaves defines an axis of symmetry through the centre of the organ separating the top (dorsal) and bottom (ventral) tissues. Although the positioning of this boundary is critical for leaf morphogenesis, how the boundary is established and how it influences development remains unclear. Using live-imaging and perturbation experiments we show that leaf orientation, morphology and position are pre-patterned by HD-ZIPIII and KAN gene expression in the shoot, leading to a model in which dorsoventral genes coordinate to regulate plant development by localizing auxin response between their expression domains. However we also find that auxin levels feedback on dorsoventral patterning by spatially organizing HD-ZIPIII and KAN expression in the shoot periphery. By demonstrating that the regulation of these genes by auxin also governs their response to wounds, our results also provide a parsimonious explanation for the influence of wounds on leaf dorsoventrality.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.7554/eLife.27421DOIArticle
https://elifesciences.org/articles/27421PublisherArticle
https://doi.org/10.1101/126466DOIDiscussion Paper
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5617630/PubMed CentralArticle
ORCID:
AuthorORCID
Bhatia, Neha0000-0002-2165-5183
Meyerowitz, Elliot M.0000-0003-4798-5153
Jönsson, Henrik0000-0003-2340-588X
Heisler, Marcus G.0000-0001-5644-8398
Additional Information:© 2017 Caggiano et al. This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited. Received: 03 April 2017; Accepted: 11 September 2017; Published: 12 September 2017. We thank M E Byrne for helpful feedback and ideas on the manuscript. We thank J Bowman for helpful discussions as well as for plasmids containing REVr and PHVr cDNAs. We thank D Weijers and C Y Liao for a plasmid containing pDR5v2::ntdTomato; K Nakajima for the T-DNA construct of miR166Ap::GFPER, Dr Atsushi Miyawaki from RIKEN Brain Science Institute for the VENUS fluorescent protein which was obtained through an MTA. We thank Professor Kenichiro Hayashi, Okayama University of Science for providing Auxinole. The EMM laboratory is supported by funds from the Howard Hughes Medical Institute and the Gordon and Betty Moore Foundation (through grant GBMF3406). The research leading to these results received funding from the Australian Research Council (MGH) and European Research Council under the European Union’s Seventh Framework Programme (FP/2007–2013)/ERC Grant Agreement n. 261081 (MGH), as well as the People Programme (Marie Curie Actions) under REA grant agreement n. 255089 (PS). The work was also supported by: the European Molecular Biology Laboratory (XY, MPC, CO, PS, NB, HR and MGH); the EMBL International PhD Programme (XY, NB and MPC); Gatsby Charitable Foundation (GAT3395/PR4) (HJ) and Swedish Research Council (VR2013-4632) (HJ). The authors declare no competing financial interests. Supplement contains additional data and movie. We declare there are no competing interests. Author Contributions: Monica Pia Caggiano, Xiulian Yu, Conceptualization, Data curation, Formal analysis, Investigation, Visualization, Methodology, Writing—original draft, Writing—review and editing; Neha Bhatia, Conceptualization, Data curation, Formal analysis, Visualization, Methodology, Writing—original draft, Writing—review and editing; André Larsson, Software, Formal analysis, Investigation, Visualization, Methodology, Writing—original draft; Hasthi Ram, Investigation, Visualization, Methodology, Writing—original draft, Writing—review and editing; Carolyn K Ohno, Resources, Investigation, Methodology, Writing—original draft, Project administration; Pia Sappl, Investigation, Methodology; Elliot M Meyerowitz, Supervision, Funding acquisition, Project administration, Writing—review and editing; Henrik Jönsson, Conceptualization, Software, Supervision, Funding acquisition, Investigation, Visualization, Methodology, Writing—original draft, Project administration, Writing—review and editing; Marcus G Heisler, Conceptualization, Supervision, Funding acquisition, Methodology, Writing—original draft, Project administration, Writing—review and editing.
Funders:
Funding AgencyGrant Number
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Gordon and Betty Moore FoundationGBMF3406
Australian Research CouncilUNSPECIFIED
European Research Council (ERC)261081
European Research Council (ERC)255089
European Molecular Biology Laboratory (EMBL)UNSPECIFIED
Gatsby Charitable FoundationGAT3395/PR4
Swedish Research CouncilVR2013-4632
PubMed Central ID:PMC5617630
Record Number:CaltechAUTHORS:20170918-104527805
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20170918-104527805
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:81524
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:18 Sep 2017 20:32
Last Modified:03 Oct 2019 18:43

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