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Cell size and growth regulation in the Arabidopsis thaliana apical stem cell niche

Willis, Lisa and Refahi, Yassin and Wightman, Raymond and Landrein, Benoit and Teles, José and Huang, Kerwyn Casey and Meyerowitz, Elliot M. and Jönsson, Henrik (2016) Cell size and growth regulation in the Arabidopsis thaliana apical stem cell niche. Proceedings of the National Academy of Sciences of the United States of America, 113 (51). E8238-E8246. ISSN 0027-8424. PMCID PMC5187701. http://resolver.caltech.edu/CaltechAUTHORS:20161206-073720144

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Abstract

Cell size and growth kinetics are fundamental cellular properties with important physiological implications. Classical studies on yeast, and recently on bacteria, have identified rules for cell size regulation in single cells, but in the more complex environment of multicellular tissues, data have been lacking. In this study, to characterize cell size and growth regulation in a multicellular context, we developed a 4D imaging pipeline and applied it to track and quantify epidermal cells over 3–4 d in Arabidopsis thaliana shoot apical meristems. We found that a cell size checkpoint is not the trigger for G2/M or cytokinesis, refuting the unexamined assumption that meristematic cells trigger cell cycle phases upon reaching a critical size. Our data also rule out models in which cells undergo G2/M at a fixed time after birth, or by adding a critical size increment between G2/M transitions. Rather, cell size regulation was intermediate between the critical size and critical increment paradigms, meaning that cell size fluctuations decay by ∼75% in one generation compared with 100% (critical size) and 50% (critical increment). Notably, this behavior was independent of local cell–cell contact topologies and of position within the tissue. Cells grew exponentially throughout the first >80% of the cell cycle, but following an asymmetrical division, the small daughter grew at a faster exponential rate than the large daughter, an observation that potentially challenges present models of growth regulation. These growth and division behaviors place strong constraints on quantitative mechanistic descriptions of the cell cycle and growth control.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1073/pnas.1616768113 DOIArticle
http://www.pnas.org/content/113/51/E8238PublisherArticle
http://www.pnas.org/content/113/51/E8238/suppl/DCSupplementalPublisherSupporting Information
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5187701/PubMed CentralArticle
ORCID:
AuthorORCID
Meyerowitz, Elliot M.0000-0003-4798-5153
Jönsson, Henrik0000-0003-2340-588X
Additional Information:© 2016 National Academy of Sciences. Freely available online through the PNAS open access option. Edited by Natasha V. Raikhel, Center for Plant Cell Biology, Riverside, CA, and approved November 3, 2016 (received for review October 11, 2016). Published online before print December 5, 2016. We thank Pau Formosa-Jordan, Daniel McKay, Charles Melnyk, Arun Sampathkumar, and Bruno Martins for stimulating discussions; David Ehrhardt for comments on the manuscript; and Christophe Godin and Gregoire Malandain for use of MARS/ALT software. The data reported in this paper are tabulated in SI Appendix, Tables S1–S10 and archived at the D-Space Repository database (Cambridge University). This work was supported by the Gatsby Charitable Foundation through Grant GAT3395-PR4 (to H.J.) and Fellowships GAT3272/C and GAT3273-PR1 (to E.M.M.), Swedish Research Council Grant VR2013:4632 and Knut and Alice Wallenberg Foundation Grant KAW2012.0050 (to H.J.), the Howard Hughes Medical Institute and Gordon and Betty Moore Foundation Grant GBMF3406 (to E.M.M.), and National Science Foundation Faculty Early Career Development (CAREER) Program Award MCB-1149328 (to K.C.H.). Author contributions: L.W., Y.R., and H.J. designed research; L.W., Y.R., R.W., B.L., and J.T. performed research; L.W., Y.R., R.W., J.T., and H.J. contributed new reagents/analytic tools; L.W., Y.R., J.T., K.C.H., E.M.M., and H.J. analyzed data; and L.W., Y.R., R.W., K.C.H., E.M.M., and H.J. wrote the paper. The authors declare no conflict of interest. This article is a PNAS Direct Submission. This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1616768113/-/DCSupplemental.
Funders:
Funding AgencyGrant Number
Gatsby Charitable FoundationGAT3395-PR4
Gatsby Charitable FoundationGAT3272/C
Gatsby Charitable FoundationGAT3273-PR1
Swedish Research CouncilVR2013:4632
Knut and Alice Wallenberg FoundationKAW2012.0050
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Gordon and Betty Moore FoundationGBMF3406
NSFMCB-1149328
Subject Keywords:cell size; cell growth; cell cycle; homeostasis; plant stem cells
PubMed Central ID:PMC5187701
Record Number:CaltechAUTHORS:20161206-073720144
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20161206-073720144
Official Citation:Lisa Willis, Yassin Refahi, Raymond Wightman, Benoit Landrein, José Teles, Kerwyn Casey Huang, Elliot M. Meyerowitz, and Henrik Jönsson Cell size and growth regulation in the Arabidopsis thaliana apical stem cell niche PNAS 2016 113 (51) E8238-E8246; published ahead of print December 5, 2016, doi:10.1073/pnas.1616768113
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:72581
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:06 Dec 2016 19:50
Last Modified:19 Sep 2017 16:53

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