PMID- 30383040 OWN - NLM STAT- MEDLINE DCOM- 20190617 LR - 20210310 IS - 1545-7885 (Electronic) IS - 1544-9173 (Print) IS - 1544-9173 (Linking) VI - 16 IP - 11 DP - 2018 Nov TI - Spatiotemporal coordination of cell division and growth during organ morphogenesis. PG - e2005952 LID - 10.1371/journal.pbio.2005952 [doi] LID - e2005952 AB - A developing plant organ exhibits complex spatiotemporal patterns of growth, cell division, cell size, cell shape, and organ shape. Explaining these patterns presents a challenge because of their dynamics and cross-correlations, which can make it difficult to disentangle causes from effects. To address these problems, we used live imaging to determine the spatiotemporal patterns of leaf growth and division in different genetic and tissue contexts. In the simplifying background of the speechless (spch) mutant, which lacks stomatal lineages, the epidermal cell layer exhibits defined patterns of division, cell size, cell shape, and growth along the proximodistal and mediolateral axes. The patterns and correlations are distinctive from those observed in the connected subepidermal layer and also different from the epidermal layer of wild type. Through computational modelling we show that the results can be accounted for by a dual control model in which spatiotemporal control operates on both growth and cell division, with cross-connections between them. The interactions between resulting growth and division patterns lead to a dynamic distributions of cell sizes and shapes within a deforming leaf. By modulating parameters of the model, we illustrate how phenotypes with correlated changes in cell size, cell number, and organ size may be generated. The model thus provides an integrated view of growth and division that can act as a framework for further experimental study. FAU - Fox, Samantha AU - Fox S AUID- ORCID: 0000-0003-1271-6412 AD - Department of Cell and Developmental Biology, John Innes Centre, Norwich, England, United Kingdom. FAU - Southam, Paul AU - Southam P AD - Department of Cell and Developmental Biology, John Innes Centre, Norwich, England, United Kingdom. FAU - Pantin, Florent AU - Pantin F AD - Department of Cell and Developmental Biology, John Innes Centre, Norwich, England, United Kingdom. AD - School of Computational Sciences, University of East Anglia, Norwich, England, United Kingdom. FAU - Kennaway, Richard AU - Kennaway R AD - Department of Cell and Developmental Biology, John Innes Centre, Norwich, England, United Kingdom. FAU - Robinson, Sarah AU - Robinson S AD - Department of Cell and Developmental Biology, John Innes Centre, Norwich, England, United Kingdom. FAU - Castorina, Giulia AU - Castorina G AD - Department of Cell and Developmental Biology, John Innes Centre, Norwich, England, United Kingdom. FAU - Sanchez-Corrales, Yara E AU - Sanchez-Corrales YE AD - Department of Cell and Developmental Biology, John Innes Centre, Norwich, England, United Kingdom. FAU - Sablowski, Robert AU - Sablowski R AD - Department of Cell and Developmental Biology, John Innes Centre, Norwich, England, United Kingdom. FAU - Chan, Jordi AU - Chan J AD - Department of Cell and Developmental Biology, John Innes Centre, Norwich, England, United Kingdom. FAU - Grieneisen, Veronica AU - Grieneisen V AD - Department of Computational and Systems Biology, John Innes Centre, Norwich, England, United Kingdom. FAU - Maree, Athanasius F M AU - Maree AFM AD - Department of Computational and Systems Biology, John Innes Centre, Norwich, England, United Kingdom. FAU - Bangham, J Andrew AU - Bangham JA AD - School of Computational Sciences, University of East Anglia, Norwich, England, United Kingdom. FAU - Coen, Enrico AU - Coen E AD - Department of Cell and Developmental Biology, John Innes Centre, Norwich, England, United Kingdom. LA - eng GR - BBS/E/J/000C0646/BB_/Biotechnology and Biological Sciences Research Council/United Kingdom GR - BBS/E/J/00000594/BB_/Biotechnology and Biological Sciences Research Council/United Kingdom GR - BBS/E/J/000PR9788/BB_/Biotechnology and Biological Sciences Research Council/United Kingdom GR - BB/F005997/1/BB_/Biotechnology and Biological Sciences Research Council/United Kingdom GR - BBS/E/J/000PR9773/BB_/Biotechnology and Biological Sciences Research Council/United Kingdom GR - BB/M023117/1/BB_/Biotechnology and Biological Sciences Research Council/United Kingdom GR - BB/F005555/1/BB_/Biotechnology and Biological Sciences Research Council/United Kingdom GR - BB/J004588/1/BB_/Biotechnology and Biological Sciences Research Council/United Kingdom GR - BB/P013511/1/BB_/Biotechnology and Biological Sciences Research Council/United Kingdom GR - BBS/E/J/000C0645/BB_/Biotechnology and Biological Sciences Research Council/United Kingdom GR - BBS/E/J/00000152/BB_/Biotechnology and Biological Sciences Research Council/United Kingdom GR - BB/L008920/1/BB_/Biotechnology and Biological Sciences Research Council/United Kingdom PT - Journal Article PT - Research Support, Non-U.S. Gov't DEP - 20181101 PL - United States TA - PLoS Biol JT - PLoS biology JID - 101183755 RN - 0 (Arabidopsis Proteins) RN - 0 (Basic Helix-Loop-Helix Transcription Factors) RN - 0 (SPEECHLESS protein, Arabidopsis) SB - IM CIN - Trends Plant Sci. 2019 May;24(5):386-388. PMID: 30905523 MH - Arabidopsis/genetics/growth & development MH - Arabidopsis Proteins/genetics/physiology MH - Basic Helix-Loop-Helix Transcription Factors/genetics/physiology MH - Cell Differentiation/genetics/physiology MH - Cell Division/*physiology MH - Cell Proliferation/*physiology MH - Cell Size MH - Gene Expression Regulation, Plant/genetics MH - Models, Biological MH - Plant Development/*physiology MH - Plant Leaves/growth & development MH - Plant Stomata/genetics/growth & development MH - Spatio-Temporal Analysis PMC - PMC6211367 COIS- The authors have declared that no competing interests exist. EDAT- 2018/11/02 06:00 MHDA- 2019/06/18 06:00 PMCR- 2018/11/01 CRDT- 2018/11/02 06:00 PHST- 2018/03/08 00:00 [received] PHST- 2018/09/20 00:00 [accepted] PHST- 2018/11/02 06:00 [entrez] PHST- 2018/11/02 06:00 [pubmed] PHST- 2019/06/18 06:00 [medline] PHST- 2018/11/01 00:00 [pmc-release] AID - pbio.2005952 [pii] AID - 10.1371/journal.pbio.2005952 [doi] PST - epublish SO - PLoS Biol. 2018 Nov 1;16(11):e2005952. doi: 10.1371/journal.pbio.2005952. eCollection 2018 Nov.