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Tissue growth constrains root organ outlines into an isometrically scalable shape

Organ morphologies are diverse but also conserved under shared developmental constraints among species. Any geometrical similarities in the shape behind diversity and the underlying developmental constraints remain unclear. Plant root tip outlines commonly exhibit a dome shape, which likely performs...

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Detalles Bibliográficos
Autores principales: Fujiwara, Motohiro, Goh, Tatsuaki, Tsugawa, Satoru, Nakajima, Keiji, Fukaki, Hidehiro, Fujimoto, Koichi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Company of Biologists Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7929931/
https://www.ncbi.nlm.nih.gov/pubmed/33637613
http://dx.doi.org/10.1242/dev.196253
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author Fujiwara, Motohiro
Goh, Tatsuaki
Tsugawa, Satoru
Nakajima, Keiji
Fukaki, Hidehiro
Fujimoto, Koichi
author_facet Fujiwara, Motohiro
Goh, Tatsuaki
Tsugawa, Satoru
Nakajima, Keiji
Fukaki, Hidehiro
Fujimoto, Koichi
author_sort Fujiwara, Motohiro
collection PubMed
description Organ morphologies are diverse but also conserved under shared developmental constraints among species. Any geometrical similarities in the shape behind diversity and the underlying developmental constraints remain unclear. Plant root tip outlines commonly exhibit a dome shape, which likely performs physiological functions, despite the diversity in size and cellular organization among distinct root classes and/or species. We carried out morphometric analysis of the primary roots of ten angiosperm species and of the lateral roots (LRs) of Arabidopsis, and found that each root outline was isometrically scaled onto a parameter-free catenary curve, a stable structure adopted for arch bridges. Using the physical model for bridges, we analogized that localized and spatially uniform occurrence of oriented cell division and expansion force the LR primordia (LRP) tip to form a catenary curve. These growth rules for the catenary curve were verified by tissue growth simulation of developing LRP development based on time-lapse imaging. Consistently, LRP outlines of mutants compromised in these rules were found to deviate from catenary curves. Our analyses demonstrate that physics-inspired growth rules constrain plant root tips to form isometrically scalable catenary curves.
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spelling pubmed-79299312021-03-09 Tissue growth constrains root organ outlines into an isometrically scalable shape Fujiwara, Motohiro Goh, Tatsuaki Tsugawa, Satoru Nakajima, Keiji Fukaki, Hidehiro Fujimoto, Koichi Development Research Article Organ morphologies are diverse but also conserved under shared developmental constraints among species. Any geometrical similarities in the shape behind diversity and the underlying developmental constraints remain unclear. Plant root tip outlines commonly exhibit a dome shape, which likely performs physiological functions, despite the diversity in size and cellular organization among distinct root classes and/or species. We carried out morphometric analysis of the primary roots of ten angiosperm species and of the lateral roots (LRs) of Arabidopsis, and found that each root outline was isometrically scaled onto a parameter-free catenary curve, a stable structure adopted for arch bridges. Using the physical model for bridges, we analogized that localized and spatially uniform occurrence of oriented cell division and expansion force the LR primordia (LRP) tip to form a catenary curve. These growth rules for the catenary curve were verified by tissue growth simulation of developing LRP development based on time-lapse imaging. Consistently, LRP outlines of mutants compromised in these rules were found to deviate from catenary curves. Our analyses demonstrate that physics-inspired growth rules constrain plant root tips to form isometrically scalable catenary curves. The Company of Biologists Ltd 2021-02-26 /pmc/articles/PMC7929931/ /pubmed/33637613 http://dx.doi.org/10.1242/dev.196253 Text en © 2021. Published by The Company of Biologists Ltd http://creativecommons.org/licenses/by/4.0This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article
Fujiwara, Motohiro
Goh, Tatsuaki
Tsugawa, Satoru
Nakajima, Keiji
Fukaki, Hidehiro
Fujimoto, Koichi
Tissue growth constrains root organ outlines into an isometrically scalable shape
title Tissue growth constrains root organ outlines into an isometrically scalable shape
title_full Tissue growth constrains root organ outlines into an isometrically scalable shape
title_fullStr Tissue growth constrains root organ outlines into an isometrically scalable shape
title_full_unstemmed Tissue growth constrains root organ outlines into an isometrically scalable shape
title_short Tissue growth constrains root organ outlines into an isometrically scalable shape
title_sort tissue growth constrains root organ outlines into an isometrically scalable shape
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7929931/
https://www.ncbi.nlm.nih.gov/pubmed/33637613
http://dx.doi.org/10.1242/dev.196253
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