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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 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 geneFruits 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.show moreshow less

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Author details:Tilly Eldridge, Lukasz Langowski, Nicola Stacey, Friederike Jantzen, Laila Moubayidin, Adrien SicardORCiD, Paul Southam, Richard Kennaway, Michael LenhardORCiDGND, Enrico S. Coen, Lars Ostergaard
DOI:https://doi.org/10.1242/dev.135327
ISSN:0950-1991
ISSN:1477-9129
Pubmed ID:https://pubmed.ncbi.nlm.nih.gov/27624834
Title of parent work (English):Development : Company of Biologists
Publisher:Company of Biologists Limited
Place of publishing:Cambridge
Publication type:Article
Language:English
Year of first publication:2016
Publication year:2016
Release date:2020/03/22
Tag:Anisotropic growth; Arabidopsis; Brassicaceae; Capsella; Fruit shape; Modelling
Volume:143
Number of pages:13
First page:3394
Last Page:3406
Funding institution:John Innes Foundation [BB/M004112/1, BB/K008617/1]; Biotechnology and Biological Sciences Research Council (BBSRC); Institute Strategic Programme grant from the BBSRC [BB/J004553/1]; BBSRC
Organizational units:Mathematisch-Naturwissenschaftliche Fakultät / Institut für Biochemie und Biologie
Peer review:Referiert
External remark:Zweitveröffentlichung in der Schriftenreihe Postprints der Universität Potsdam : Mathematisch-Naturwissenschaftliche Reihe ; 986
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