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Dev Cell. 2016 Jul 11;38(1):15-32. doi: 10.1016/j.devcel.2016.06.016.

Variable Cell Growth Yields Reproducible OrganDevelopment through Spatiotemporal Averaging.

Author information

1
Weill Institute for Cell and Molecular Biology and Section of Plant Biology, School of Integrative Plant Sciences, Cornell University, Ithaca, NY 14853, USA.
2
Laboratoire de Reproduction et Développement des Plantes, Université de Lyon, ENS de Lyon, UCBL, INRA, CNRS, 46 Allée d'Italie, 69364 Lyon Cedex 07, France; Laboratoire Joliot Curie, CNRS, ENS de Lyon, Université de Lyon, 46 Allée d'Italie, 69364 Lyon Cedex 07, France.
3
Research Institute for Electronic Science, Hokkaido University, Kita 20 Nishi 10, Kita-ku, Sapporo 001-0020, Japan.
4
Department of Comparative Development and Genetics, Max Planck Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, 50829 Köln, Germany.
5
Laboratoire de Reproduction et Développement des Plantes, Université de Lyon, ENS de Lyon, UCBL, INRA, CNRS, 46 Allée d'Italie, 69364 Lyon Cedex 07, France; Laboratoire Joliot Curie, CNRS, ENS de Lyon, Université de Lyon, 46 Allée d'Italie, 69364 Lyon Cedex 07, France. Electronic address: arezki.boudaoud@ens-lyon.fr.
6
Weill Institute for Cell and Molecular Biology and Section of Plant Biology, School of Integrative Plant Sciences, Cornell University, Ithaca, NY 14853, USA. Electronic address: ahr75@cornell.edu.

Abstract

Organ sizes and shapes are strikingly reproducible, despite the variable growth and division of individual cells within them. To reveal which mechanisms enable this precision, we designed a screen for disrupted sepal size and shape uniformity in Arabidopsis and identified mutations in the mitochondrial i-AAA protease FtsH4. Counterintuitively, through live imaging we observed that variability of neighboring cell growth was reduced in ftsh4 sepals. We found that regular organ shape results from spatiotemporal averaging of the cellular variability in wild-type sepals, which is disrupted in the less-variable cells of ftsh4 mutants. We also found that abnormal, increased accumulation of reactive oxygen species (ROS) in ftsh4 mutants disrupts organ size consistency. In wild-type sepals, ROS accumulate in maturing cells and limit organ growth, suggesting that ROS are endogenous signals promoting termination of growth. Our results demonstrate that spatiotemporal averaging of cellular variability is required for precision in organ size.

PMID:
27404356
DOI:
10.1016/j.devcel.2016.06.016
[Indexed for MEDLINE]
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