Halostachys caspica pathogenesis-related protein 10 acts as a cytokinin reservoir to regulate plant growth and development

Pathogenesis-related class 10 (PR-10) proteins play a role in plant growth and development, but the underlying molecular mechanisms are unclear. Here, we isolated a salt-induced PR-10 gene from the halophyte Halostachys caspica and named it HcPR10. HcPR10 was constitutively expressed during developm...

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Main Authors: Yudan Feng, Yanpeng Ren, Hua Zhang, Youqiang Heng, Zhanxin Wang, Yan Wang
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-04-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2023.1116985/full
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author Yudan Feng
Yanpeng Ren
Hua Zhang
Youqiang Heng
Zhanxin Wang
Yan Wang
author_facet Yudan Feng
Yanpeng Ren
Hua Zhang
Youqiang Heng
Zhanxin Wang
Yan Wang
author_sort Yudan Feng
collection DOAJ
description Pathogenesis-related class 10 (PR-10) proteins play a role in plant growth and development, but the underlying molecular mechanisms are unclear. Here, we isolated a salt-induced PR-10 gene from the halophyte Halostachys caspica and named it HcPR10. HcPR10 was constitutively expressed during development and HcPR10 localized to the nucleus and cytoplasm. HcPR10-mediated phenotypes including bolting, earlier flowering, increased branch number and siliques per plant are highly correlated with increased cytokinin levels in transgenic Arabidopsis. Meanwhile, increased levels of cytokinin in plants is temporally correlated with HcPR10 expression patterns. Although the expression of cytokinin biosynthesis genes validated was not upregulated, cytokinin-related genes including chloroplast-related genes, cytokinin metabolism and cytokinin responses genes and flowering-related genes were significantly upregulated in the transgenic Arabidopsis compared to the wild type by transcriptome deep sequencing. Analysis of the crystal structure of HcPR10 revealed a trans-zeatin riboside (a type of cytokinin) located deep in its cavity, with a conserved conformation and protein–ligand interactions, supporting HcRP10 acts as a cytokinin reservoir. Moreover, HcPR10 in Halostachys caspica predominantly accumulated in vascular tissue, the site of long-distance translocation of plant hormones. Collectively, we draw that HcPR10 as a cytokinin reservoir induces cytokinin-related signal transduction in plants, thereby promoting plant growth and development. These findings could provide intriguing insights into the role of HcPR10 proteins in phytohormone regulation in plants and advance our understanding of cytokinin-mediated plant development and could facilitate the breeding of transgenic crops with earlier mature, higher yielding agronomic traits.
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spelling doaj.art-c1133ace20034684b45277abf56c45072023-04-26T05:50:17ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-04-011410.3389/fpls.2023.11169851116985Halostachys caspica pathogenesis-related protein 10 acts as a cytokinin reservoir to regulate plant growth and developmentYudan Feng0Yanpeng Ren1Hua Zhang2Youqiang Heng3Zhanxin Wang4Yan Wang5Xinjiang Key Laboratory of Biological Resources and Genetic Engineering, College of Life Science and Technology, Xinjiang University, Urumqi, ChinaKey Laboratory of Cell Proliferation and Regulation Biology of Ministry of Education, College of Life Sciences, Beijing Normal University, Beijing, ChinaXinjiang Key Laboratory of Biological Resources and Genetic Engineering, College of Life Science and Technology, Xinjiang University, Urumqi, ChinaXinjiang Key Laboratory of Biological Resources and Genetic Engineering, College of Life Science and Technology, Xinjiang University, Urumqi, ChinaKey Laboratory of Cell Proliferation and Regulation Biology of Ministry of Education, College of Life Sciences, Beijing Normal University, Beijing, ChinaXinjiang Key Laboratory of Biological Resources and Genetic Engineering, College of Life Science and Technology, Xinjiang University, Urumqi, ChinaPathogenesis-related class 10 (PR-10) proteins play a role in plant growth and development, but the underlying molecular mechanisms are unclear. Here, we isolated a salt-induced PR-10 gene from the halophyte Halostachys caspica and named it HcPR10. HcPR10 was constitutively expressed during development and HcPR10 localized to the nucleus and cytoplasm. HcPR10-mediated phenotypes including bolting, earlier flowering, increased branch number and siliques per plant are highly correlated with increased cytokinin levels in transgenic Arabidopsis. Meanwhile, increased levels of cytokinin in plants is temporally correlated with HcPR10 expression patterns. Although the expression of cytokinin biosynthesis genes validated was not upregulated, cytokinin-related genes including chloroplast-related genes, cytokinin metabolism and cytokinin responses genes and flowering-related genes were significantly upregulated in the transgenic Arabidopsis compared to the wild type by transcriptome deep sequencing. Analysis of the crystal structure of HcPR10 revealed a trans-zeatin riboside (a type of cytokinin) located deep in its cavity, with a conserved conformation and protein–ligand interactions, supporting HcRP10 acts as a cytokinin reservoir. Moreover, HcPR10 in Halostachys caspica predominantly accumulated in vascular tissue, the site of long-distance translocation of plant hormones. Collectively, we draw that HcPR10 as a cytokinin reservoir induces cytokinin-related signal transduction in plants, thereby promoting plant growth and development. These findings could provide intriguing insights into the role of HcPR10 proteins in phytohormone regulation in plants and advance our understanding of cytokinin-mediated plant development and could facilitate the breeding of transgenic crops with earlier mature, higher yielding agronomic traits.https://www.frontiersin.org/articles/10.3389/fpls.2023.1116985/fullpathogenesis related protein 10growth and developmentcytokinincrystal structureligand interactions
spellingShingle Yudan Feng
Yanpeng Ren
Hua Zhang
Youqiang Heng
Zhanxin Wang
Yan Wang
Halostachys caspica pathogenesis-related protein 10 acts as a cytokinin reservoir to regulate plant growth and development
Frontiers in Plant Science
pathogenesis related protein 10
growth and development
cytokinin
crystal structure
ligand interactions
title Halostachys caspica pathogenesis-related protein 10 acts as a cytokinin reservoir to regulate plant growth and development
title_full Halostachys caspica pathogenesis-related protein 10 acts as a cytokinin reservoir to regulate plant growth and development
title_fullStr Halostachys caspica pathogenesis-related protein 10 acts as a cytokinin reservoir to regulate plant growth and development
title_full_unstemmed Halostachys caspica pathogenesis-related protein 10 acts as a cytokinin reservoir to regulate plant growth and development
title_short Halostachys caspica pathogenesis-related protein 10 acts as a cytokinin reservoir to regulate plant growth and development
title_sort halostachys caspica pathogenesis related protein 10 acts as a cytokinin reservoir to regulate plant growth and development
topic pathogenesis related protein 10
growth and development
cytokinin
crystal structure
ligand interactions
url https://www.frontiersin.org/articles/10.3389/fpls.2023.1116985/full
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