Quantitative control of organ shape by combinatorial gene activity.

The development of organs with particular shapes, like wings or flowers, depends on regional activity of transcription factors and signalling molecules. However, the mechanisms that link these molecular activities to the morphogenetic events underlying shape are poorly understood. Here we describe a...

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Main Authors: Min-Long Cui, Lucy Copsey, Amelia A Green, J Andrew Bangham, Enrico Coen
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2010-11-01
Series:PLoS Biology
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/21085695/?tool=EBI
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spelling doaj-bc4ea25f423f46d895c7046470c4e1732021-07-02T17:09:28ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852010-11-01811e100053810.1371/journal.pbio.1000538Quantitative control of organ shape by combinatorial gene activity.Min-Long CuiLucy CopseyAmelia A GreenJ Andrew BanghamEnrico CoenThe development of organs with particular shapes, like wings or flowers, depends on regional activity of transcription factors and signalling molecules. However, the mechanisms that link these molecular activities to the morphogenetic events underlying shape are poorly understood. Here we describe a combination of experimental and computational approaches that address this problem, applying them to a group of genes controlling flower shape in the Snapdragon (Antirrhinum). Four transcription factors are known to play a key role in the control of floral shape and asymmetry in Snapdragon. We use quantitative shape analysis of mutants for these factors to define principal components underlying flower shape variation. We show that each transcription factor has a specific effect on the shape and size of regions within the flower, shifting the position of the flower in shape space. These shifts are further analysed by generating double mutants and lines that express some of the genes ectopically. By integrating these observations with known gene expression patterns and interactions, we arrive at a combinatorial scheme for how regional effects on shape are genetically controlled. We evaluate our scheme by incorporating the proposed interactions into a generative model, where the developing flower is treated as a material sheet that grows according to how genes modify local polarities and growth rates. The petal shapes generated by the model show a good quantitative match with those observed experimentally for each petal in numerous genotypes, thus validating the hypothesised scheme. This article therefore shows how complex shapes can be accounted for by combinatorial effects of transcription factors on regional growth properties. This finding has implications not only for how shapes develop but also for how they may have evolved through tinkering with transcription factors and their targets.https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/21085695/?tool=EBI
collection DOAJ
language English
format Article
sources DOAJ
author Min-Long Cui
Lucy Copsey
Amelia A Green
J Andrew Bangham
Enrico Coen
spellingShingle Min-Long Cui
Lucy Copsey
Amelia A Green
J Andrew Bangham
Enrico Coen
Quantitative control of organ shape by combinatorial gene activity.
PLoS Biology
author_facet Min-Long Cui
Lucy Copsey
Amelia A Green
J Andrew Bangham
Enrico Coen
author_sort Min-Long Cui
title Quantitative control of organ shape by combinatorial gene activity.
title_short Quantitative control of organ shape by combinatorial gene activity.
title_full Quantitative control of organ shape by combinatorial gene activity.
title_fullStr Quantitative control of organ shape by combinatorial gene activity.
title_full_unstemmed Quantitative control of organ shape by combinatorial gene activity.
title_sort quantitative control of organ shape by combinatorial gene activity.
publisher Public Library of Science (PLoS)
series PLoS Biology
issn 1544-9173
1545-7885
publishDate 2010-11-01
description The development of organs with particular shapes, like wings or flowers, depends on regional activity of transcription factors and signalling molecules. However, the mechanisms that link these molecular activities to the morphogenetic events underlying shape are poorly understood. Here we describe a combination of experimental and computational approaches that address this problem, applying them to a group of genes controlling flower shape in the Snapdragon (Antirrhinum). Four transcription factors are known to play a key role in the control of floral shape and asymmetry in Snapdragon. We use quantitative shape analysis of mutants for these factors to define principal components underlying flower shape variation. We show that each transcription factor has a specific effect on the shape and size of regions within the flower, shifting the position of the flower in shape space. These shifts are further analysed by generating double mutants and lines that express some of the genes ectopically. By integrating these observations with known gene expression patterns and interactions, we arrive at a combinatorial scheme for how regional effects on shape are genetically controlled. We evaluate our scheme by incorporating the proposed interactions into a generative model, where the developing flower is treated as a material sheet that grows according to how genes modify local polarities and growth rates. The petal shapes generated by the model show a good quantitative match with those observed experimentally for each petal in numerous genotypes, thus validating the hypothesised scheme. This article therefore shows how complex shapes can be accounted for by combinatorial effects of transcription factors on regional growth properties. This finding has implications not only for how shapes develop but also for how they may have evolved through tinkering with transcription factors and their targets.
url https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/21085695/?tool=EBI
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