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Spatial regularity control of phyllotaxis pattern generated by the mutual interaction between auxin and PIN1

Phyllotaxis, the arrangement of leaves on a plant stem, is well known because of its beautiful geometric configuration, which is derived from the constant spacing between leaf primordia. This phyllotaxis is established by mutual interaction between a diffusible plant hormone auxin and its efflux car...

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Autores principales: Fujita, Hironori, Kawaguchi, Masayoshi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5882125/
https://www.ncbi.nlm.nih.gov/pubmed/29614066
http://dx.doi.org/10.1371/journal.pcbi.1006065
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author Fujita, Hironori
Kawaguchi, Masayoshi
author_facet Fujita, Hironori
Kawaguchi, Masayoshi
author_sort Fujita, Hironori
collection PubMed
description Phyllotaxis, the arrangement of leaves on a plant stem, is well known because of its beautiful geometric configuration, which is derived from the constant spacing between leaf primordia. This phyllotaxis is established by mutual interaction between a diffusible plant hormone auxin and its efflux carrier PIN1, which cooperatively generate a regular pattern of auxin maxima, small regions with high auxin concentrations, leading to leaf primordia. However, the molecular mechanism of the regular pattern of auxin maxima is still largely unknown. To better understand how the phyllotaxis pattern is controlled, we investigated mathematical models based on the auxin–PIN1 interaction through linear stability analysis and numerical simulations, focusing on the spatial regularity control of auxin maxima. As in previous reports, we first confirmed that this spatial regularity can be reproduced by a highly simplified and abstract model. However, this model lacks the extracellular region and is not appropriate for considering the molecular mechanism. Thus, we investigated how auxin maxima patterns are affected under more realistic conditions. We found that the spatial regularity is eliminated by introducing the extracellular region, even in the presence of direct diffusion between cells or between extracellular spaces, and this strongly suggests the existence of an unknown molecular mechanism. To unravel this mechanism, we assumed a diffusible molecule to verify various feedback interactions with auxin–PIN1 dynamics. We revealed that regular patterns can be restored by a diffusible molecule that mediates the signaling from auxin to PIN1 polarization. Furthermore, as in the one-dimensional case, similar results are observed in the two-dimensional space. These results provide a great insight into the theoretical and molecular basis for understanding the phyllotaxis pattern. Our theoretical analysis strongly predicts a diffusible molecule that is pivotal for the phyllotaxis pattern but is yet to be determined experimentally.
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spelling pubmed-58821252018-04-13 Spatial regularity control of phyllotaxis pattern generated by the mutual interaction between auxin and PIN1 Fujita, Hironori Kawaguchi, Masayoshi PLoS Comput Biol Research Article Phyllotaxis, the arrangement of leaves on a plant stem, is well known because of its beautiful geometric configuration, which is derived from the constant spacing between leaf primordia. This phyllotaxis is established by mutual interaction between a diffusible plant hormone auxin and its efflux carrier PIN1, which cooperatively generate a regular pattern of auxin maxima, small regions with high auxin concentrations, leading to leaf primordia. However, the molecular mechanism of the regular pattern of auxin maxima is still largely unknown. To better understand how the phyllotaxis pattern is controlled, we investigated mathematical models based on the auxin–PIN1 interaction through linear stability analysis and numerical simulations, focusing on the spatial regularity control of auxin maxima. As in previous reports, we first confirmed that this spatial regularity can be reproduced by a highly simplified and abstract model. However, this model lacks the extracellular region and is not appropriate for considering the molecular mechanism. Thus, we investigated how auxin maxima patterns are affected under more realistic conditions. We found that the spatial regularity is eliminated by introducing the extracellular region, even in the presence of direct diffusion between cells or between extracellular spaces, and this strongly suggests the existence of an unknown molecular mechanism. To unravel this mechanism, we assumed a diffusible molecule to verify various feedback interactions with auxin–PIN1 dynamics. We revealed that regular patterns can be restored by a diffusible molecule that mediates the signaling from auxin to PIN1 polarization. Furthermore, as in the one-dimensional case, similar results are observed in the two-dimensional space. These results provide a great insight into the theoretical and molecular basis for understanding the phyllotaxis pattern. Our theoretical analysis strongly predicts a diffusible molecule that is pivotal for the phyllotaxis pattern but is yet to be determined experimentally. Public Library of Science 2018-04-03 /pmc/articles/PMC5882125/ /pubmed/29614066 http://dx.doi.org/10.1371/journal.pcbi.1006065 Text en © 2018 Fujita, Kawaguchi http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Fujita, Hironori
Kawaguchi, Masayoshi
Spatial regularity control of phyllotaxis pattern generated by the mutual interaction between auxin and PIN1
title Spatial regularity control of phyllotaxis pattern generated by the mutual interaction between auxin and PIN1
title_full Spatial regularity control of phyllotaxis pattern generated by the mutual interaction between auxin and PIN1
title_fullStr Spatial regularity control of phyllotaxis pattern generated by the mutual interaction between auxin and PIN1
title_full_unstemmed Spatial regularity control of phyllotaxis pattern generated by the mutual interaction between auxin and PIN1
title_short Spatial regularity control of phyllotaxis pattern generated by the mutual interaction between auxin and PIN1
title_sort spatial regularity control of phyllotaxis pattern generated by the mutual interaction between auxin and pin1
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5882125/
https://www.ncbi.nlm.nih.gov/pubmed/29614066
http://dx.doi.org/10.1371/journal.pcbi.1006065
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