Coordination of Tissue Cell Polarity by Auxin Transport and Signaling
Abstract
Plants coordinate the polarity of hundreds of cells during vein formation, but how they do so is unclear. The prevailing hypothesis proposes that GNOM, a regulator of membrane trafficking, positions PIN-FORMED auxin transporters to the correct side of the plasma membrane; the resulting cell-to-cell, polar transport of auxin would coordinate tissue cell polarity and induce vein formation. Contrary to predictions of the hypothesis, we find that vein formation occurs in the absence of PIN-FORMED or any other intercellular auxin-transporter; that the residual auxin-transport-independent vein-patterning activity relies on auxin signaling; and that a GNOM-dependent signal acts upstream of both auxin transport and signaling to coordinate tissue cell polarity and induce vein formation. Our results reveal synergism between auxin transport and signaling, and their unsuspected control by GNOM in the coordination of tissue cell polarity during vein patterning, one of the most informative expressions of tissue cell polarization in plants.
Additional Information
© 2019, Verna 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: August 13, 2019. Accepted: November 1, 2019. Version of Record published: December 3, 2019 (version 1) We dedicate this article to Ida Ruberti, an inspiring example of scientific depth, integrity, and elegance; Ida passed away on June 8, 2019. We thank the Arabidopsis Biological Resource Center for emb30-8, gn-13, gn-18, pin1-1, eir1-1, pin6, pin8-1, pgp1-100, mdr1-101, ucu2-4, aux1-355, lax1-064, axr1-3 and axr1-12; Hidehiro Fukaki for fwr and gnSALK_103014; Sandra Richter and Gerd Jürgens for gnB/E and gnR5; Satoshi Naramoto and Hiroo Fukuda for van7/emb30-7; Eva Benková and Jiří Friml for PIN1::PIN1:GFP; Jian Xu and Ben Scheres for PIN1::PIN1:YFP and PIN2::PIN2:GFP; Jian Xu, Miyo Morita, and Masao Tasaka for PIN3::PIN3:GFP; Ikram Blilou and Ben Scheres for Atpin1:: En134, pin3-3, pin4-2 and pin7En; Venkatesan Sundaresan for toz-1; Thomas Berleth for mpG12; Markus Geisler and Jiří Friml for ABCB1::ABCB1:GFP and ABCB19::ABCB19:GFP; Cris Kuhlemeier for aux1-21;lax1;2–1;3; Michael Prigge and Mark Estelle for tir1-1;afb2-3; and Marcus Heisler and Elliot Meyerowitz for DR5rev::nYFP. This work was supported by Discovery Grants of the Natural Sciences and Engineering Research Council of Canada (NSERC) to ES. CV was supported, in part, by a University of Alberta Doctoral Recruitment Scholarship. MGS was supported, in part, by an NSERC CGS-M Scholarship and an NSERC CGS-D Scholarship. The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication. Author contributions: Carla Verna, Sree Janani Ravichandran, Megan G Sawchuk, Nguyen Manh Linh, Conceptualization, Formal analysis, Validation, Investigation, Visualization, Methodology, Writing—original draft, Writing—review and editing; Enrico Scarpella, Conceptualization, Resources, Formal analysis, Supervision, Funding acquisition, Validation, Investigation, Visualization, Methodology, Writing—original draft, Project administration, Writing—review and editing. Data availability: All data generated or analyzed during this study are included in the manuscript and supporting files.Attached Files
Published - elife-51061-v1.pdf
Submitted - 680090.full.pdf
Supplemental Material - Figures_1-14.zip
Supplemental Material - Tables.zip
Supplemental Material - elife-51061-supp1-v1.docx
Supplemental Material - elife-51061-supp2-v1.pdf
Supplemental Material - elife-51061-transrepform-v1.docx
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Additional details
- PMCID
- PMC6890459
- Eprint ID
- 97176
- Resolver ID
- CaltechAUTHORS:20190716-120637201
- Natural Sciences and Engineering Research Council of Canada (NSERC)
- University of Alberta
- Created
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2019-07-16Created from EPrint's datestamp field
- Updated
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2023-06-02Created from EPrint's last_modified field