ATANN3 Is Involved in Extracellular ATP-Regulated Auxin Distribution in <i>Arabidopsis thaliana</i> Seedlings

Extracellular ATP (eATP) plays multiple roles in plant growth and development, and stress responses. It has been revealed that eATP suppresses growth and alters the growth orientation of the root and hypocotyl of <i>Arabidopsis thaliana</i> by affecting auxin transport and localization i...

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Main Authors: Jiawei Xu, Lijuan Han, Shuyan Xia, Ruojia Zhu, Erfang Kang, Zhonglin Shang
Format: Article
Language:English
Published: MDPI AG 2023-01-01
Series:Plants
Subjects:
Online Access:https://www.mdpi.com/2223-7747/12/2/330
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author Jiawei Xu
Lijuan Han
Shuyan Xia
Ruojia Zhu
Erfang Kang
Zhonglin Shang
author_facet Jiawei Xu
Lijuan Han
Shuyan Xia
Ruojia Zhu
Erfang Kang
Zhonglin Shang
author_sort Jiawei Xu
collection DOAJ
description Extracellular ATP (eATP) plays multiple roles in plant growth and development, and stress responses. It has been revealed that eATP suppresses growth and alters the growth orientation of the root and hypocotyl of <i>Arabidopsis thaliana</i> by affecting auxin transport and localization in these organs. However, the mechanism of the eATP-stimulated auxin distribution remains elusive. Annexins are involved in multiple aspects of plant cellular metabolism, while their role in response to apoplastic signals remains unclear. Here, by using the loss-of-function mutations, we investigated the role of AtANN3 in the eATP-regulated root and hypocotyl growth. Firstly, the inhibitory effects of eATP on root and hypocotyl elongation were weakened or impaired in the <i>AtANN3</i> null mutants (<i>atann3–1</i> and <i>atann3–2</i>). Meanwhile, the distribution of DR5-GUS and DR5-GFP indicated that the eATP-induced asymmetric distribution of auxin in the root tips or hypocotyl cells occurred in wild-type control plants, while in <i>atann3–1</i> mutant seedlings, it was not observed. Further, the eATP-induced asymmetric distribution of PIN2-GFP in root-tip cells or that of PIN3-GFP in hypocotyl cells was reduced in <i>atann3–1</i> seedlings. Finally, the eATP-induced asymmetric distribution of cytoplasmic vesicles in root-tip cells was impaired in <i>atann3–1</i> seedlings. Based on these results, we suggest that AtANN3 may be involved in eATP-regulated seedling growth by regulating the distribution of auxin and auxin transporters in vegetative organs.
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spelling doaj.art-d942619b8aa544e3a8d11b9c091cc0db2023-12-01T00:05:00ZengMDPI AGPlants2223-77472023-01-0112233010.3390/plants12020330ATANN3 Is Involved in Extracellular ATP-Regulated Auxin Distribution in <i>Arabidopsis thaliana</i> SeedlingsJiawei Xu0Lijuan Han1Shuyan Xia2Ruojia Zhu3Erfang Kang4Zhonglin Shang5Ministry of Education Key Laboratory of Molecular and Cellular Biology, College of Life Sciences, Hebei Normal University, Shijiazhuang 050024, ChinaMinistry of Education Key Laboratory of Molecular and Cellular Biology, College of Life Sciences, Hebei Normal University, Shijiazhuang 050024, ChinaMinistry of Education Key Laboratory of Molecular and Cellular Biology, College of Life Sciences, Hebei Normal University, Shijiazhuang 050024, ChinaMinistry of Education Key Laboratory of Molecular and Cellular Biology, College of Life Sciences, Hebei Normal University, Shijiazhuang 050024, ChinaMinistry of Education Key Laboratory of Molecular and Cellular Biology, College of Life Sciences, Hebei Normal University, Shijiazhuang 050024, ChinaMinistry of Education Key Laboratory of Molecular and Cellular Biology, College of Life Sciences, Hebei Normal University, Shijiazhuang 050024, ChinaExtracellular ATP (eATP) plays multiple roles in plant growth and development, and stress responses. It has been revealed that eATP suppresses growth and alters the growth orientation of the root and hypocotyl of <i>Arabidopsis thaliana</i> by affecting auxin transport and localization in these organs. However, the mechanism of the eATP-stimulated auxin distribution remains elusive. Annexins are involved in multiple aspects of plant cellular metabolism, while their role in response to apoplastic signals remains unclear. Here, by using the loss-of-function mutations, we investigated the role of AtANN3 in the eATP-regulated root and hypocotyl growth. Firstly, the inhibitory effects of eATP on root and hypocotyl elongation were weakened or impaired in the <i>AtANN3</i> null mutants (<i>atann3–1</i> and <i>atann3–2</i>). Meanwhile, the distribution of DR5-GUS and DR5-GFP indicated that the eATP-induced asymmetric distribution of auxin in the root tips or hypocotyl cells occurred in wild-type control plants, while in <i>atann3–1</i> mutant seedlings, it was not observed. Further, the eATP-induced asymmetric distribution of PIN2-GFP in root-tip cells or that of PIN3-GFP in hypocotyl cells was reduced in <i>atann3–1</i> seedlings. Finally, the eATP-induced asymmetric distribution of cytoplasmic vesicles in root-tip cells was impaired in <i>atann3–1</i> seedlings. Based on these results, we suggest that AtANN3 may be involved in eATP-regulated seedling growth by regulating the distribution of auxin and auxin transporters in vegetative organs.https://www.mdpi.com/2223-7747/12/2/330extracellular ATP (eATP)<i>Arabidopsis thaliana</i>AtANN3auxinseedling growth
spellingShingle Jiawei Xu
Lijuan Han
Shuyan Xia
Ruojia Zhu
Erfang Kang
Zhonglin Shang
ATANN3 Is Involved in Extracellular ATP-Regulated Auxin Distribution in <i>Arabidopsis thaliana</i> Seedlings
Plants
extracellular ATP (eATP)
<i>Arabidopsis thaliana</i>
AtANN3
auxin
seedling growth
title ATANN3 Is Involved in Extracellular ATP-Regulated Auxin Distribution in <i>Arabidopsis thaliana</i> Seedlings
title_full ATANN3 Is Involved in Extracellular ATP-Regulated Auxin Distribution in <i>Arabidopsis thaliana</i> Seedlings
title_fullStr ATANN3 Is Involved in Extracellular ATP-Regulated Auxin Distribution in <i>Arabidopsis thaliana</i> Seedlings
title_full_unstemmed ATANN3 Is Involved in Extracellular ATP-Regulated Auxin Distribution in <i>Arabidopsis thaliana</i> Seedlings
title_short ATANN3 Is Involved in Extracellular ATP-Regulated Auxin Distribution in <i>Arabidopsis thaliana</i> Seedlings
title_sort atann3 is involved in extracellular atp regulated auxin distribution in i arabidopsis thaliana i seedlings
topic extracellular ATP (eATP)
<i>Arabidopsis thaliana</i>
AtANN3
auxin
seedling growth
url https://www.mdpi.com/2223-7747/12/2/330
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