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ETR1 Integrates Response to Ethylene and Cytokinins into a Single Multistep Phosphorelay Pathway to Control Root Growth

Zdarska, Marketa and Rubiato Cuyacot, Abigail and Tarr, Paul T. and Yamoune, Amel and Szmitkowska, Agnieszka and Hrdinová, Vendula and Gelová, Zuzana and Meyerowitz, Elliot M. and Hejátko, Jan (2019) ETR1 Integrates Response to Ethylene and Cytokinins into a Single Multistep Phosphorelay Pathway to Control Root Growth. Molecular Plant, 12 (10). pp. 1338-1352. ISSN 1674-2052. PMCID PMC8040967. doi:10.1016/j.molp.2019.05.012. https://resolver.caltech.edu/CaltechAUTHORS:20190607-133806981

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Abstract

Cytokinins and ethylene control plant development via sensors from the histidine kinase (HK) family. However, downstream signaling pathways for the key phytohormones are distinct. Here we report not only cytokinin but also ethylene is able to control root apical meristem (RAM) size through activation of the multistep phosphorelay (MSP) pathway. We find both cytokinin and ethylene-dependent RAM shortening requires ethylene binding to ETR1 and its HK activity. The receiver domain of ETR1 interacts with MSP signaling intermediates acting downstream of cytokinin receptors, further substantiating the role of ETR1 in MSP signaling. Our studies find both cytokinin and ethylene induce the MSP in similar and distinct cell types with ETR1-mediated ethylene signaling controlling MSP output specifically in the root transition zone. We identified members of the MSP pathway specific and common to both hormones and show that ETR1-regulated ARR3 controls RAM size. ETR1-mediated MSP spatially differs from canonical CTR1/EIN2/EIN3 ethylene signaling and is independent of EIN2, indicating that both pathways can be spatially and functionally separated. Furthermore, we demonstrate that canonical ethylene signaling controls MSP responsiveness to cytokinin specifically in the root transition zone, presumably via regulation of ARR10, one of the positive regulators of MSP signaling in Arabidopsis.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1016/j.molp.2019.05.012DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8040967PubMed CentralArticle
ORCID:
AuthorORCID
Tarr, Paul T.0000-0003-2977-3683
Gelová, Zuzana0000-0003-4783-1752
Meyerowitz, Elliot M.0000-0003-4798-5153
Hejátko, Jan0000-0002-2622-6046
Additional Information:© 2019 The Author. Published by the Molecular Plant Shanghai Editorial Office in association with Cell Press, an imprint of Elsevier Inc., on behalf of CSPB and IPPE, SIBS, CAS. Received 7 September 2018, Revised 17 April 2019, Accepted 28 May 2019, Available online 7 June 2019. The work was supported by the Czech Science Foundation (19-23108Y, 15-22000S) and the Ministry of Education, Youth and Sports of the Czech Republic under the projects CEITEC 2020 (LQ1601), CZ.02.1.01/0.0/0.0/16_026/0008446 and LTAUSA18161. We acknowledge the core facility CELLIM of CEITEC supported by the Czech-BioImaging large RI project (LM2015062 funded by MEYS CR) for their support with obtaining scientific data presented in this paper. Plant Sciences Core Facility of CEITEC MU is acknowledged for the cultivation of experimental plants used in this paper. Work performed in E.M.’s laboratory was supported by NIH NIGMS grant R01 GM104244, Howard Hughes Medical Institute, and the Gordon and Betty Moore Foundation through grant GBMF3406. Author Contributions: M.Z. and J.H. conceived the research; M.Z., A.R.C., P.T.T., A.S., V.H., Z.G., and A.Y. performed the research; M.Z., A.R.C., P.T.T., V.H., A.Y., E.M.M., and J.H. analyzed the data; M.Z., P.T.T., E.M.M., and J.H. wrote the paper. No conflict of interest declared.
Funders:
Funding AgencyGrant Number
Grantová Agentura České Republiky (GACR)19-23108Y
Grantová Agentura České Republiky (GACR)15-22000S
Ministry of Education, Youth and Sports (Czech Republic)LQ1601
Ministry of Education, Youth and Sports (Czech Republic)CZ.02.1.01/0.0/0.0/16_026/0008446
Ministry of Education, Youth and Sports (Czech Republic)LTAUSA18161
Ministry of Education, Youth and Sports (Czech Republic)LM2015062
NIHR01 GM104244
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Gordon and Betty Moore FoundationGBMF3406
Subject Keywords:cytokinin; ethylene; crosstalk; signaling; root development
Issue or Number:10
PubMed Central ID:PMC8040967
DOI:10.1016/j.molp.2019.05.012
Record Number:CaltechAUTHORS:20190607-133806981
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20190607-133806981
Official Citation:Marketa Zdarska, Abigail Rubiato Cuyacot, Paul T. Tarr, Amel Yamoune, Agnieszka Szmitkowska, Vendula Hrdinová, Zuzana Gelová, Elliot M. Meyerowitz, Jan Hejátko, ETR1 Integrates Response to Ethylene and Cytokinins into a Single Multistep Phosphorelay Pathway to Control Root Growth, Molecular Plant, Volume 12, Issue 10, 2019, Pages 1338-1352, ISSN 1674-2052, https://doi.org/10.1016/j.molp.2019.05.012. (http://www.sciencedirect.com/science/article/pii/S1674205219301984)
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:96207
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:07 Jun 2019 21:09
Last Modified:19 Apr 2021 17:29

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