PIN2-mediated self-organizing transient auxin flow contributes to auxin maxima at the tip of Arabidopsis cotyledons

Abstract Directional auxin transport and formation of auxin maxima are critical for embryogenesis, organogenesis, pattern formation, and growth coordination in plants, but the mechanisms underpinning the initiation and establishment of these auxin dynamics are not fully understood. Here we show that...

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Main Authors: Patricio Pérez-Henríquez, Shingo Nagawa, Zhongchi Liu, Xue Pan, Marta Michniewicz, Wenxin Tang, Carolyn Rasmussen, Xinping Cui, Jaimie Van Norman, Lucia Strader, Zhenbiao Yang
Format: Article
Language:English
Published: Nature Portfolio 2025-02-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-55480-8
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author Patricio Pérez-Henríquez
Shingo Nagawa
Zhongchi Liu
Xue Pan
Marta Michniewicz
Wenxin Tang
Carolyn Rasmussen
Xinping Cui
Jaimie Van Norman
Lucia Strader
Zhenbiao Yang
author_facet Patricio Pérez-Henríquez
Shingo Nagawa
Zhongchi Liu
Xue Pan
Marta Michniewicz
Wenxin Tang
Carolyn Rasmussen
Xinping Cui
Jaimie Van Norman
Lucia Strader
Zhenbiao Yang
author_sort Patricio Pérez-Henríquez
collection DOAJ
description Abstract Directional auxin transport and formation of auxin maxima are critical for embryogenesis, organogenesis, pattern formation, and growth coordination in plants, but the mechanisms underpinning the initiation and establishment of these auxin dynamics are not fully understood. Here we show that a self-initiating and -terminating transient auxin flow along the marginal cells (MCs) contributes to the formation of an auxin maximum at the tip of Arabidopsis cotyledon that globally coordinates the interdigitation of puzzle-shaped pavement cells in the cotyledon epidermis. Prior to the interdigitation, indole butyric acid (IBA) is converted to indole acetic acid (IAA) to induce PIN2 accumulation and polarization in the marginal cells, leading to auxin flow toward and accumulation at the cotyledon tip. Once IAA levels at the cotyledon tip reaches a maximum, it activates pavement cell interdigitation as well as the accumulation of the IBA transporter TOB1 in MCs, which sequesters IBA to the vacuole and reduces IBA availability and IAA levels. The reduction of IAA levels results in PIN2 down-regulation and cessation of the auxin flow. Hence, our results elucidate a self-activating and self-terminating transient polar auxin transport system in cotyledons, contributing to the formation of localized auxin maxima that spatiotemporally coordinate pavement cell interdigitation.
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institution Kabale University
issn 2041-1723
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publishDate 2025-02-01
publisher Nature Portfolio
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series Nature Communications
spelling doaj-art-07ee4e4f198646f09e9b60dcf491d9232025-02-09T12:46:29ZengNature PortfolioNature Communications2041-17232025-02-0116111310.1038/s41467-024-55480-8PIN2-mediated self-organizing transient auxin flow contributes to auxin maxima at the tip of Arabidopsis cotyledonsPatricio Pérez-Henríquez0Shingo Nagawa1Zhongchi Liu2Xue Pan3Marta Michniewicz4Wenxin Tang5Carolyn Rasmussen6Xinping Cui7Jaimie Van Norman8Lucia Strader9Zhenbiao Yang10Institute of Integrated Genome Biology, and Department of Botany and Plant Sciences, University of CaliforniaHaixia Institute of Science and Technology, Fujian Agriculture and Forestry UniversityFaculty of Synthetic Biology, Shenzhen University of Advanced TechnologyInstitute of Integrated Genome Biology, and Department of Botany and Plant Sciences, University of CaliforniaDepartment of Biology, Washington UniversityHaixia Institute of Science and Technology, Fujian Agriculture and Forestry UniversityInstitute of Integrated Genome Biology, and Department of Botany and Plant Sciences, University of CaliforniaDepartment of Statistics, University of CaliforniaInstitute of Integrated Genome Biology, and Department of Botany and Plant Sciences, University of CaliforniaDepartment of Biology, Washington UniversityInstitute of Integrated Genome Biology, and Department of Botany and Plant Sciences, University of CaliforniaAbstract Directional auxin transport and formation of auxin maxima are critical for embryogenesis, organogenesis, pattern formation, and growth coordination in plants, but the mechanisms underpinning the initiation and establishment of these auxin dynamics are not fully understood. Here we show that a self-initiating and -terminating transient auxin flow along the marginal cells (MCs) contributes to the formation of an auxin maximum at the tip of Arabidopsis cotyledon that globally coordinates the interdigitation of puzzle-shaped pavement cells in the cotyledon epidermis. Prior to the interdigitation, indole butyric acid (IBA) is converted to indole acetic acid (IAA) to induce PIN2 accumulation and polarization in the marginal cells, leading to auxin flow toward and accumulation at the cotyledon tip. Once IAA levels at the cotyledon tip reaches a maximum, it activates pavement cell interdigitation as well as the accumulation of the IBA transporter TOB1 in MCs, which sequesters IBA to the vacuole and reduces IBA availability and IAA levels. The reduction of IAA levels results in PIN2 down-regulation and cessation of the auxin flow. Hence, our results elucidate a self-activating and self-terminating transient polar auxin transport system in cotyledons, contributing to the formation of localized auxin maxima that spatiotemporally coordinate pavement cell interdigitation.https://doi.org/10.1038/s41467-024-55480-8
spellingShingle Patricio Pérez-Henríquez
Shingo Nagawa
Zhongchi Liu
Xue Pan
Marta Michniewicz
Wenxin Tang
Carolyn Rasmussen
Xinping Cui
Jaimie Van Norman
Lucia Strader
Zhenbiao Yang
PIN2-mediated self-organizing transient auxin flow contributes to auxin maxima at the tip of Arabidopsis cotyledons
Nature Communications
title PIN2-mediated self-organizing transient auxin flow contributes to auxin maxima at the tip of Arabidopsis cotyledons
title_full PIN2-mediated self-organizing transient auxin flow contributes to auxin maxima at the tip of Arabidopsis cotyledons
title_fullStr PIN2-mediated self-organizing transient auxin flow contributes to auxin maxima at the tip of Arabidopsis cotyledons
title_full_unstemmed PIN2-mediated self-organizing transient auxin flow contributes to auxin maxima at the tip of Arabidopsis cotyledons
title_short PIN2-mediated self-organizing transient auxin flow contributes to auxin maxima at the tip of Arabidopsis cotyledons
title_sort pin2 mediated self organizing transient auxin flow contributes to auxin maxima at the tip of arabidopsis cotyledons
url https://doi.org/10.1038/s41467-024-55480-8
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