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Research Article

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

Lisa Willis, Yassin Refahi, Raymond Wightman, Benoit Landrein, José Teles, Kerwyn Casey Huang, Elliot M. Meyerowitz, and View ORCID ProfileHenrik Jönsson
PNAS December 20, 2016 113 (51) E8238-E8246; first published December 5, 2016; https://doi.org/10.1073/pnas.1616768113
Lisa Willis
aThe Sainsbury Laboratory, University of Cambridge, Cambridge CB2 1LR, United Kingdom;
bDepartment of Bioengineering, Stanford University, Stanford, CA 94305;
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Yassin Refahi
aThe Sainsbury Laboratory, University of Cambridge, Cambridge CB2 1LR, United Kingdom;
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Raymond Wightman
aThe Sainsbury Laboratory, University of Cambridge, Cambridge CB2 1LR, United Kingdom;
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Benoit Landrein
aThe Sainsbury Laboratory, University of Cambridge, Cambridge CB2 1LR, United Kingdom;
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José Teles
aThe Sainsbury Laboratory, University of Cambridge, Cambridge CB2 1LR, United Kingdom;
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Kerwyn Casey Huang
bDepartment of Bioengineering, Stanford University, Stanford, CA 94305;
cDepartment of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA 94305;
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Elliot M. Meyerowitz
aThe Sainsbury Laboratory, University of Cambridge, Cambridge CB2 1LR, United Kingdom;
dHoward Hughes Medical Institute, California Institute of Technology, Pasadena, CA 91125;
eDivision of Biology and Biological Engineering 156-29, California Institute of Technology, Pasadena, CA 91125;
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Henrik Jönsson
aThe Sainsbury Laboratory, University of Cambridge, Cambridge CB2 1LR, United Kingdom;
fComputational Biology and Biological Physics, Lund University, 223 62 Lund, Sweden;
gDepartment of Applied Mathematics and Theoretical Physics, Centre for Mathematical Sciences, University of Cambridge, Cambridge CB3 0DZ, United Kingdom
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  • ORCID record for Henrik Jönsson
  • For correspondence: henrik.jonsson@slcu.cam.ac.uk
  1. Edited by Natasha V. Raikhel, Center for Plant Cell Biology, Riverside, CA, and approved November 3, 2016 (received for review October 11, 2016)

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Significance

How does a cell decide when to divide or initiate DNA replication? How does it regulate its own growth? These fundamental questions are not well understood in most organisms; this lack of understanding is particularly true for multicellular eukaryotes. Following classical studies in yeast, we have quantified the key aspects of cell growth and division dynamics in the Arabidopsis apical stem cell niche. Our results disprove various theories for plant stem cell size/cell cycle regulation, such as that cell cycle progression is triggered when a prefixed critical size is attained, and constitute the necessary first step in the development of integrative mechanistic theories for the coordinated regulation of cell cycle progression, cell growth, and cell size in plants.

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.

  • cell size
  • cell growth
  • cell cycle
  • homeostasis
  • plant stem cells

Footnotes

  • ↵1L.W. and Y.R. contributed equally to this work.

  • ↵2To whom correspondence should be addressed. Email: henrik.jonsson{at}slcu.cam.ac.uk.
  • 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.

Freely available online through the PNAS open access option.

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Cell size and growth regulation in Arabidopsis
Lisa Willis, Yassin Refahi, Raymond Wightman, Benoit Landrein, José Teles, Kerwyn Casey Huang, Elliot M. Meyerowitz, Henrik Jönsson
Proceedings of the National Academy of Sciences Dec 2016, 113 (51) E8238-E8246; DOI: 10.1073/pnas.1616768113

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Cell size and growth regulation in Arabidopsis
Lisa Willis, Yassin Refahi, Raymond Wightman, Benoit Landrein, José Teles, Kerwyn Casey Huang, Elliot M. Meyerowitz, Henrik Jönsson
Proceedings of the National Academy of Sciences Dec 2016, 113 (51) E8238-E8246; DOI: 10.1073/pnas.1616768113
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