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Fruit shape diversity in the Brassicaceae is generated by varying patterns of anisotropy

Fruits exhibit a vast array of different 3D shapes, from simple spheres and cylinders to more complex curved forms; however, the mechanism by which growth is oriented and coordinated to generate this diversity of forms is unclear. Here, we compare the growth patterns and orientations for two very di...

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Autores principales: Eldridge, Tilly, Łangowski, Łukasz, Stacey, Nicola, Jantzen, Friederike, Moubayidin, Laila, Sicard, Adrien, Southam, Paul, Kennaway, Richard, Lenhard, Michael, Coen, Enrico S., Østergaard, Lars
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Company of Biologists Ltd 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5047655/
https://www.ncbi.nlm.nih.gov/pubmed/27624834
http://dx.doi.org/10.1242/dev.135327
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author Eldridge, Tilly
Łangowski, Łukasz
Stacey, Nicola
Jantzen, Friederike
Moubayidin, Laila
Sicard, Adrien
Southam, Paul
Kennaway, Richard
Lenhard, Michael
Coen, Enrico S.
Østergaard, Lars
author_facet Eldridge, Tilly
Łangowski, Łukasz
Stacey, Nicola
Jantzen, Friederike
Moubayidin, Laila
Sicard, Adrien
Southam, Paul
Kennaway, Richard
Lenhard, Michael
Coen, Enrico S.
Østergaard, Lars
author_sort Eldridge, Tilly
collection PubMed
description Fruits exhibit a vast array of different 3D shapes, from simple spheres and cylinders to more complex curved forms; however, the mechanism by which growth is oriented and coordinated to generate this diversity of forms is unclear. Here, we compare the growth patterns and orientations for two very different fruit shapes in the Brassicaceae: the heart-shaped Capsella rubella silicle and the near-cylindrical Arabidopsis thaliana silique. We show, through a combination of clonal and morphological analyses, that the different shapes involve different patterns of anisotropic growth during three phases. These experimental data can be accounted for by a tissue-level model in which specified growth rates vary in space and time and are oriented by a proximodistal polarity field. The resulting tissue conflicts lead to deformation of the tissue as it grows. The model allows us to identify tissue-specific and temporally specific activities required to obtain the individual shapes. One such activity may be provided by the valve-identity gene FRUITFULL, which we show through comparative mutant analysis to modulate fruit shape during post-fertilisation growth of both species. Simple modulations of the model presented here can also broadly account for the variety of shapes in other Brassicaceae species, thus providing a simplified framework for fruit development and shape diversity.
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spelling pubmed-50476552016-10-06 Fruit shape diversity in the Brassicaceae is generated by varying patterns of anisotropy Eldridge, Tilly Łangowski, Łukasz Stacey, Nicola Jantzen, Friederike Moubayidin, Laila Sicard, Adrien Southam, Paul Kennaway, Richard Lenhard, Michael Coen, Enrico S. Østergaard, Lars Development Research Article Fruits exhibit a vast array of different 3D shapes, from simple spheres and cylinders to more complex curved forms; however, the mechanism by which growth is oriented and coordinated to generate this diversity of forms is unclear. Here, we compare the growth patterns and orientations for two very different fruit shapes in the Brassicaceae: the heart-shaped Capsella rubella silicle and the near-cylindrical Arabidopsis thaliana silique. We show, through a combination of clonal and morphological analyses, that the different shapes involve different patterns of anisotropic growth during three phases. These experimental data can be accounted for by a tissue-level model in which specified growth rates vary in space and time and are oriented by a proximodistal polarity field. The resulting tissue conflicts lead to deformation of the tissue as it grows. The model allows us to identify tissue-specific and temporally specific activities required to obtain the individual shapes. One such activity may be provided by the valve-identity gene FRUITFULL, which we show through comparative mutant analysis to modulate fruit shape during post-fertilisation growth of both species. Simple modulations of the model presented here can also broadly account for the variety of shapes in other Brassicaceae species, thus providing a simplified framework for fruit development and shape diversity. The Company of Biologists Ltd 2016-09-15 /pmc/articles/PMC5047655/ /pubmed/27624834 http://dx.doi.org/10.1242/dev.135327 Text en © 2016. Published by The Company of Biologists Ltd http://creativecommons.org/licenses/by/3.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article
Eldridge, Tilly
Łangowski, Łukasz
Stacey, Nicola
Jantzen, Friederike
Moubayidin, Laila
Sicard, Adrien
Southam, Paul
Kennaway, Richard
Lenhard, Michael
Coen, Enrico S.
Østergaard, Lars
Fruit shape diversity in the Brassicaceae is generated by varying patterns of anisotropy
title Fruit shape diversity in the Brassicaceae is generated by varying patterns of anisotropy
title_full Fruit shape diversity in the Brassicaceae is generated by varying patterns of anisotropy
title_fullStr Fruit shape diversity in the Brassicaceae is generated by varying patterns of anisotropy
title_full_unstemmed Fruit shape diversity in the Brassicaceae is generated by varying patterns of anisotropy
title_short Fruit shape diversity in the Brassicaceae is generated by varying patterns of anisotropy
title_sort fruit shape diversity in the brassicaceae is generated by varying patterns of anisotropy
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5047655/
https://www.ncbi.nlm.nih.gov/pubmed/27624834
http://dx.doi.org/10.1242/dev.135327
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