Genetic Control of Organ Shape and Tissue Polarity
Amelia A. Green1¤, J. Richard Kennaway2, Andrew I. Hanna2, J. Andrew Bangham2*, Enrico Coen1*
1 Department of Cell and Developmental Biology, John Innes Centre, Norwich, United Kingdom, 2 University of East Anglia, School of Computing Sciences, Norwich, United Kingdom
Abstract
The mechanisms by which genes control organ shape are poorly understood. In principle, genes may control shape by modifying local rates and/or orientations of deformation. Distinguishing between these possibilities has been difficult because of interactions between patterns, orientations, and mechanical constraints during growth. Here we show how a combination of growth analysis, molecular genetics, and modelling can be used to dissect the factors contributing to shape. Using the Snapdragon (Antirrhinum) flower as an example, we show how shape development reflects local rates and orientations of tissue growth that vary spatially and temporally to form a dynamic growth field. This growth field is under the control of several dorsoventral genes that influence flower shape. The action of these genes can be modelled by assuming they modulate specified growth rates parallel or perpendicular to local orientations, established by a few key organisers of tissue polarity. Models in which dorsoventral genes only influence specified growth rates do not fully account for the observed growth fields and shapes. However, the data can be readily explained by a model in which dorsoventral genes also modify organisers of tissue polarity. In particular, genetic control of tissue polarity organisers at ventral petal junctions and distal boundaries allows both the shape and growth field of the flower to be accounted for in wild type and mutants. The results suggest that genetic control of tissue polarity organisers has played a key role in the development and evolution of shape.
Author Summary
Genes are known to control the shape of biological structures, like flowers, hearts, and limbs, yet how they do this is poorly understood. A working hypothesis is that genes control shape by modulating local rates at which growing tissue deforms. Evaluating this idea has been difficult, however, because of the dynamic interactions that occur within growing and deforming tissue. To address this problem, we used a combination of experimental and mathematical modelling approaches to study how genes control shape in the Snapdragon flower. This system has the advantages of having well defined genes that influence shape and being accessible to growth analysis. We first tried to explain the experimental data with a model in which genes influence local rates of tissue growth. While this model could capture many aspects of flower development, it failed to account for some key features. These could be most readily explained if genes also affect an internal field of orientations along which growth is directed, established by organisers of tissue polarity. Our analysis therefore revealed a previously unsuspected role of shape genes in the control of tissue polarity, highlighting the importance of this process for the development and evolution of tissue forms.
Citation: Green AA, Kennaway JR, Hanna AI, Bangham JA, Coen E (2010) Genetic Control of Organ Shape and Tissue Polarity. PLoS Biol 8(11): e1000537. doi:10.1371/journal.pbio.1000537
Academic Editor: Ottoline Leyser, University of York, United Kingdom
Received: June 14, 2010; Accepted: September 28, 2010; Published: November 9, 2010
Copyright: © 2010 Green et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This work was funded by the BBSRC (BB/F005997/1). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Abbreviations: ω, rotation rate for a region; θ, the principal orientation of growth for a region; A surface, one surface of the canvas; B surface, the other surface of the canvas; GPT-framework, Growing Polarised Tissue framework; GRN, Gene Regulatory Network; Kmax, growth rate along the principal orientation of growth for a region; Kmin, growth rate perpendicular to the principal orientation of growth for a region; Knor, specified growth rate in tissue thickness for a region; Kpar, specified growth rate for a region, in the plane of the canvas, parallel to the local polarity; Kper, specified growth rate for a region, in the plane of the canvas, perpendicular to the local polarity; KRN, growth rate (K) Regulatory Network; LTS, LATERALS (an identity factor in the corolla model); OPT, Optical Projection Tomography; +organiser, a region of the canvas that organises polarity with arrows pointing away from it; −organiser, a region of the canvas that organises polarity with arrows pointing towards it; POL, POLARISER (a signalling factor in the GPT-framework that is used to implement polarity propagation—the gradient of POL defines local polarity); PRN, Polarity Regulatory Network
* E-mail: enrico.coen@bbsrc.ac.uk (EC); a.bangham@uea.ac.uk (JAB)
¤ Current address: Department of Systems Biology, Harvard Medical School, Boston, Massachusetts, United States of America
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Computer model of the growth of a snapdragon flower, produced by the groups of Professor Andrew Bangham of the University of East Anglia and Professor Enrico Coen of the John Innes Centre
FREE PDF GRÁTIS [OPEN ACCESS]
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Computer model of the growth of a snapdragon flower, produced by the groups of Professor Andrew Bangham of the University of East Anglia and Professor Enrico Coen of the John Innes Centre
