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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Autores principales: Min-Long Cui, Lucy Copsey, Amelia A Green, J Andrew Bangham, Enrico Coen
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Publicado: Public Library of Science (PLoS) 2010
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Acceso en línea:https://doaj.org/article/bc4ea25f423f46d895c7046470c4e173
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spelling oai:doaj.org-article:bc4ea25f423f46d895c7046470c4e1732021-11-18T05:36:57ZQuantitative control of organ shape by combinatorial gene activity.1544-91731545-788510.1371/journal.pbio.1000538https://doaj.org/article/bc4ea25f423f46d895c7046470c4e1732010-11-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/21085695/?tool=EBIhttps://doaj.org/toc/1544-9173https://doaj.org/toc/1545-7885The 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.Min-Long CuiLucy CopseyAmelia A GreenJ Andrew BanghamEnrico CoenPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Biology, Vol 8, Iss 11, p e1000538 (2010)
institution DOAJ
collection DOAJ
language EN
topic Biology (General)
QH301-705.5
spellingShingle Biology (General)
QH301-705.5
Min-Long Cui
Lucy Copsey
Amelia A Green
J Andrew Bangham
Enrico Coen
Quantitative control of organ shape by combinatorial gene activity.
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.
format article
author Min-Long Cui
Lucy Copsey
Amelia A Green
J Andrew Bangham
Enrico Coen
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)
publishDate 2010
url https://doaj.org/article/bc4ea25f423f46d895c7046470c4e173
work_keys_str_mv AT minlongcui quantitativecontroloforganshapebycombinatorialgeneactivity
AT lucycopsey quantitativecontroloforganshapebycombinatorialgeneactivity
AT ameliaagreen quantitativecontroloforganshapebycombinatorialgeneactivity
AT jandrewbangham quantitativecontroloforganshapebycombinatorialgeneactivity
AT enricocoen quantitativecontroloforganshapebycombinatorialgeneactivity
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