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Calcium signals are necessary to establish auxin transporter polarity in a plant stem cell niche

Li, Ting and Yan, An and Bhatia, Neha and Altinok, Alphan and Afik, Eldad and Durand-Smet, Pauline and Tarr, Paul T. and Schroeder, Julian I. and Heisler, Marcus G. and Meyerowitz, Elliot M. (2019) Calcium signals are necessary to establish auxin transporter polarity in a plant stem cell niche. Nature Communications, 10 . Art. No. 726. ISSN 2041-1723. PMCID PMC6374474. http://resolver.caltech.edu/CaltechAUTHORS:20190213-155805773

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Abstract

In plants mechanical signals pattern morphogenesis through the polar transport of the hormone auxin and through regulation of interphase microtubule (MT) orientation. To date, the mechanisms by which such signals induce changes in cell polarity remain unknown. Through a combination of time-lapse imaging, and chemical and mechanical perturbations, we show that mechanical stimulation of the SAM causes transient changes in cytoplasmic calcium ion concentration (Ca^(2+)) and that transient Ca^(2+) response is required for downstream changes in PIN-FORMED 1 (PIN1) polarity. We also find that dynamic changes in Ca^(2+) occur during development of the SAM and this Ca^(2+) response is required for changes in PIN1 polarity, though not sufficient. In contrast, we find that Ca^(2+) is not necessary for the response of MTs to mechanical perturbations revealing that Ca^(2+) specifically acts downstream of mechanics to regulate PIN1 polarity response.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1038/s41467-019-08575-6DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6374474PubMed CentralArticle
ORCID:
AuthorORCID
Li, Ting0000-0001-8273-5593
Yan, An0000-0002-4676-5442
Bhatia, Neha0000-0002-2165-5183
Afik, Eldad0000-0002-8887-2166
Heisler, Marcus G.0000-0001-5644-8398
Meyerowitz, Elliot M.0000-0003-4798-5153
Additional Information:© 2019 The Author(s). This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. Received 08 June 2018; Accepted 15 January 2019; Published 13 February 2019. Code availability: The corresponding open-source Python code, previously introduced in Refs. 56,57 on natural-cubic-smoothing-splines can be found at https://github.com/eldad-a/natural-cubic-smoothing-splines. All other code, including the programming code for quantitative analysis of the meristem calcium oscillations and waves upon mechanical perturbation, are available from the corresponding authors upon request. Data availability: All data are available from the corresponding author upon request, including all of the microscope time lapse files. The source data underlying Supplementary Figs. 1a, b, 4c, 5a–f, 7e–j, 8a, b, 10, 11i–l, 12k–l and Supplementary Tables 1 and 2 are provided as a Source Data file. We are grateful to Dr. Arun Sampathkumar for support in establishing the calcium confocal imaging process, Dr. Hanako Yashiro for the support in intact plant imaging and Dr. Ivo Grosse for the useful discussions and input on statistical analysis. We thank Dr. Francesca Peri for kindly providing the DNA for GCaMP6f and Dr. Rainer Waadt for R-GECO1 constructs and advice. We also thank Dr. Changfu Yao and Meyerowitz and Heisler lab members for suggestions and discussions. The authors’ work was funded by the Howard Hughes Medical Institute and by NASA grant NNX17AD53G to E.M.M., by the European Research Council (ERC) grant 261081 to M.G.H., in part by NIH grant GM060396 to J.I.S., Marie Skłodowska-Curie Action fellowship to P.D-.S., and a California Institute of Technology Biology and Biological Engineering Fellowship and a Zuckerman STEM Leadership Program postdoctoral scholarship to E.A. Author Contributions: T.L., A.Y., N.B., J.I.S, M.G.H., and E.M.M. conceived the experiments. T.L., N.B., A.Y., P.D-.S. performed experiments. A.A. analyzed Ca^(2+) wave imaging data. E.A. analyzed Ca^(2+) oscillation patterns. P.D-.S. invented, built, and provided the indentation and compression devices. P.T.T. contributed reagents. T.L., A.Y., N.B., M.H., and E.M.M. wrote the manuscript. All authors read and approved the manuscript. The authors declare no competing interests.
Funders:
Funding AgencyGrant Number
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
NASANNX17AD53G
European Research Council (ERC)261081
NIHGM060396
Marie Curie FellowshipUNSPECIFIED
Caltech Division of Biology and Biological EngineeringUNSPECIFIED
Zuckerman STEM Leadership ProgramUNSPECIFIED
PubMed Central ID:PMC6374474
Record Number:CaltechAUTHORS:20190213-155805773
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20190213-155805773
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:92907
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:14 Feb 2019 17:41
Last Modified:19 Feb 2019 17:44

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