Reaction-Diffusion Pattern in Shoot Apical Meristem of Plants

Reaction-Diffusion Pattern in Shoot Apical Meristem of Plants

A fundamental question in developmental biology is how spatial patterns are self-organized from homogeneous structures. In 1952, Turing proposed the reaction-diffusion model in order to explain this issue. Experimental evidence of reaction-diffusion patterns in living organisms was first provided by...

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Main Authors: Fujita, Hironori, Toyokura, Koichi, Okada, Kiyotaka, Kawaguchi, Masayoshi
Format: Online
Language:English
Published: Public Library of Science 2011
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3066213/
id pubmed-3066213
recordtype oai_dc
spelling pubmed-30662132011-04-08 Reaction-Diffusion Pattern in Shoot Apical Meristem of Plants Fujita, Hironori Toyokura, Koichi Okada, Kiyotaka Kawaguchi, Masayoshi Research Article A fundamental question in developmental biology is how spatial patterns are self-organized from homogeneous structures. In 1952, Turing proposed the reaction-diffusion model in order to explain this issue. Experimental evidence of reaction-diffusion patterns in living organisms was first provided by the pigmentation pattern on the skin of fishes in 1995. However, whether or not this mechanism plays an essential role in developmental events of living organisms remains elusive. Here we show that a reaction-diffusion model can successfully explain the shoot apical meristem (SAM) development of plants. SAM of plants resides in the top of each shoot and consists of a central zone (CZ) and a surrounding peripheral zone (PZ). SAM contains stem cells and continuously produces new organs throughout the lifespan. Molecular genetic studies using Arabidopsis thaliana revealed that the formation and maintenance of the SAM are essentially regulated by the feedback interaction between WUSHCEL (WUS) and CLAVATA (CLV). We developed a mathematical model of the SAM based on a reaction-diffusion dynamics of the WUS-CLV interaction, incorporating cell division and the spatial restriction of the dynamics. Our model explains the various SAM patterns observed in plants, for example, homeostatic control of SAM size in the wild type, enlarged or fasciated SAM in clv mutants, and initiation of ectopic secondary meristems from an initial flattened SAM in wus mutant. In addition, the model is supported by comparing its prediction with the expression pattern of WUS in the wus mutant. Furthermore, the model can account for many experimental results including reorganization processes caused by the CZ ablation and by incision through the meristem center. We thus conclude that the reaction-diffusion dynamics is probably indispensable for the SAM development of plants. Public Library of Science 2011-03-29 /pmc/articles/PMC3066213/ /pubmed/21479227 http://dx.doi.org/10.1371/journal.pone.0018243 Text en Fujita et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
repository_type Open Access Journal
institution_category Foreign Institution
institution US National Center for Biotechnology Information
building NCBI PubMed
collection Online Access
language English
format Online
author Fujita, Hironori
Toyokura, Koichi
Okada, Kiyotaka
Kawaguchi, Masayoshi
spellingShingle Fujita, Hironori
Toyokura, Koichi
Okada, Kiyotaka
Kawaguchi, Masayoshi
Reaction-Diffusion Pattern in Shoot Apical Meristem of Plants
author_facet Fujita, Hironori
Toyokura, Koichi
Okada, Kiyotaka
Kawaguchi, Masayoshi
author_sort Fujita, Hironori
title Reaction-Diffusion Pattern in Shoot Apical Meristem of Plants
title_short Reaction-Diffusion Pattern in Shoot Apical Meristem of Plants
title_full Reaction-Diffusion Pattern in Shoot Apical Meristem of Plants
title_fullStr Reaction-Diffusion Pattern in Shoot Apical Meristem of Plants
title_full_unstemmed Reaction-Diffusion Pattern in Shoot Apical Meristem of Plants
title_sort reaction-diffusion pattern in shoot apical meristem of plants
description A fundamental question in developmental biology is how spatial patterns are self-organized from homogeneous structures. In 1952, Turing proposed the reaction-diffusion model in order to explain this issue. Experimental evidence of reaction-diffusion patterns in living organisms was first provided by the pigmentation pattern on the skin of fishes in 1995. However, whether or not this mechanism plays an essential role in developmental events of living organisms remains elusive. Here we show that a reaction-diffusion model can successfully explain the shoot apical meristem (SAM) development of plants. SAM of plants resides in the top of each shoot and consists of a central zone (CZ) and a surrounding peripheral zone (PZ). SAM contains stem cells and continuously produces new organs throughout the lifespan. Molecular genetic studies using Arabidopsis thaliana revealed that the formation and maintenance of the SAM are essentially regulated by the feedback interaction between WUSHCEL (WUS) and CLAVATA (CLV). We developed a mathematical model of the SAM based on a reaction-diffusion dynamics of the WUS-CLV interaction, incorporating cell division and the spatial restriction of the dynamics. Our model explains the various SAM patterns observed in plants, for example, homeostatic control of SAM size in the wild type, enlarged or fasciated SAM in clv mutants, and initiation of ectopic secondary meristems from an initial flattened SAM in wus mutant. In addition, the model is supported by comparing its prediction with the expression pattern of WUS in the wus mutant. Furthermore, the model can account for many experimental results including reorganization processes caused by the CZ ablation and by incision through the meristem center. We thus conclude that the reaction-diffusion dynamics is probably indispensable for the SAM development of plants.
publisher Public Library of Science
publishDate 2011
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3066213/
_version_ 1611447438643560448

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