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Nitrate modulates stem cell dynamics in Arabidopsis shoot meristems through cytokinins

Landrein, Benoit and Formosa-Jordan, Pau and Malivert, Alice and Schuster, Christoph and Melnyk, Charles W. and Yang, Weibing and Turnbull, Colin and Meyerowitz, Elliot M. and Locke, James C. W. and Jönsson, Henrik (2018) Nitrate modulates stem cell dynamics in Arabidopsis shoot meristems through cytokinins. Proceedings of the National Academy of Sciences of the United States of America, 115 (6). pp. 1382-1387. ISSN 0027-8424. PMCID PMC5819446. https://resolver.caltech.edu/CaltechAUTHORS:20180123-145437847

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Abstract

The shoot apical meristem (SAM) is responsible for the generation of all the aerial parts of plants. Given its critical role, dynamical changes in SAM activity should play a central role in the adaptation of plant architecture to the environment. Using quantitative microscopy, grafting experiments, and genetic perturbations, we connect the plant environment to the SAM by describing the molecular mechanism by which cytokinins signal the level of nutrient availability to the SAM. We show that a systemic signal of cytokinin precursors mediates the adaptation of SAM size and organogenesis rate to the availability of mineral nutrients by modulating the expression of WUSCHEL, a key regulator of stem cell homeostasis. In time-lapse experiments, we further show that this mechanism allows meristems to adapt to rapid changes in nitrate concentration, and thereby modulate their rate of organ production to the availability of mineral nutrients within a few days. Our work sheds light on the role of the stem cell regulatory network by showing that it not only maintains meristem homeostasis but also allows plants to adapt to rapid changes in the environment.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1073/pnas.1718670115DOIArticle
http://www.pnas.org/content/115/6/1382PublisherArticle
http://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1718670115/-/DCSupplementalPublisherSupplemental Material
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5819446PubMed CentralArticle
https://doi.org/10.1101/200303DOIDiscussion Paper
ORCID:
AuthorORCID
Meyerowitz, Elliot M.0000-0003-4798-5153
Jönsson, Henrik0000-0003-2340-588X
Alternate Title:Nitrate modulates stem cell dynamics by regulating WUSCHEL expression through cytokinins
Additional Information:© 2018 National Academy of Sciences. This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND). Contributed by Elliot M. Meyerowitz, December 20, 2017 (sent for review October 26, 2017; reviewed by Aaron M. Rashotte and Robert Sablowski). Published online before print January 23, 2018. We thank Tanya Waldie and Maaike de Jong for sharing their knowledge on developmental plasticity and for help with the transient nitrate treatments, Jeremy Gruel for fruitful discussions on stem cell regulation, Paul Tarr for providing material and for comments on the manuscript, Jason Daff for his horticulture expertise, Raymond Wightman for help with imaging, and Hugo Tavares for help with statistical analysis. We also thank Chillie Zeng, Mark Bennett, and Rosa Lopez-Cobollo from Imperial College London for their help during the preparation and the analysis of cytokinin species by mass spectrometry. This work is supported by the Gatsby Charitable Foundation [fellowship GAT3395/DAA (to E.M.M.), GAT3272/GLC (to J.C.W.L.), and GAT3395-PR4 (to H.J.)]. E.M.M. also acknowledges support from the Howard Hughes Medical Institute and the Gordon and Betty Moore Foundation (through Grant GBMF3406). Research in the laboratory of J.C.W.L. was made possible by the award of a European Research Council under the European Union’s Seventh Framework Programme (FP/2007-2013)/ERC Grant Agreement 338060. P.F.-J. acknowledges a postdoctoral fellowship provided by the Herchel Smith Foundation. Author contributions: B.L., C.W.M., E.M.M., J.C.W.L., and H.J. designed research; B.L., A.M., C.S., C.W.M., and W.Y. performed research; B.L., P.F.-J., A.M., C.S., C.T., E.M.M., J.C.W.L., and H.J. analyzed data; and B.L., E.M.M., J.C.W.L., and H.J. wrote the paper. Reviewers: A.M.R., Auburn University; and R.S., John Innes Centre. The authors declare no conflict of interest. This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1718670115/-/DCSupplemental.
Funders:
Funding AgencyGrant Number
Gatsby Charitable FoundationGAT3395/DAA
Gatsby Charitable FoundationGAT3272/GLC
Gatsby Charitable FoundationGAT3395-PR4
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Gordon and Betty Moore FoundationGBMF3406
European Research Council (ERC)338060
Herchel Smith FoundationUNSPECIFIED
Subject Keywords:Arabidopsis; shoot apical meristem; plant nutrition; plant development; cytokinin hormones
Issue or Number:6
PubMed Central ID:PMC5819446
Record Number:CaltechAUTHORS:20180123-145437847
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20180123-145437847
Official Citation:Nitrate modulation of Arabidopsis shoot stem cells Benoit Landrein, Pau Formosa-Jordan, Alice Malivert, Christoph Schuster, Charles W. Melnyk, Weibing Yang, Colin Turnbull, Elliot M. Meyerowitz, James C. W. Locke, Henrik Jönsson. Proceedings of the National Academy of Sciences Feb 2018, 115 (6) 1382-1387; DOI: 10.1073/pnas.1718670115
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:84482
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:23 Jan 2018 23:09
Last Modified:03 Oct 2019 19:19

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