Transcriptomic analysis reveals the functions of H2S as a gasotransmitter independently of Cys in Arabidopsis

Numerous studies have revealed the gasotransmitter functions of hydrogen sulfide (H2S) in various biological processes. However, the involvement of H2S in sulfur metabolism and/or Cys synthesis makes its role as a signaling molecule ambiguous. The generation of endogenous H2S in plants is closely re...

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Main Authors: Huihui Fang, Zhenyuan Yu, Kehong Xing, Lingyi Zhou, Yuke Shao, Xiaofang Zhang, Yanxi Pei, Lu Zhang
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-06-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2023.1184991/full
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author Huihui Fang
Zhenyuan Yu
Kehong Xing
Lingyi Zhou
Yuke Shao
Xiaofang Zhang
Yanxi Pei
Lu Zhang
author_facet Huihui Fang
Zhenyuan Yu
Kehong Xing
Lingyi Zhou
Yuke Shao
Xiaofang Zhang
Yanxi Pei
Lu Zhang
author_sort Huihui Fang
collection DOAJ
description Numerous studies have revealed the gasotransmitter functions of hydrogen sulfide (H2S) in various biological processes. However, the involvement of H2S in sulfur metabolism and/or Cys synthesis makes its role as a signaling molecule ambiguous. The generation of endogenous H2S in plants is closely related to the metabolism of Cys, which play roles in a variety of signaling pathway occurring in various cellular processes. Here, we found that exogenous H2S fumigation and Cys treatment modulated the production rate and content of endogenous H2S and Cys to various degrees. Furthermore, we provided comprehensive transcriptomic analysis to support the gasotransmitter role of H2S besides as a substrate for Cys synthesis. Comparison of the differentially expressed genes (DEGs) between H2S and Cys treated seedlings indicated that H2S fumigation and Cys treatment caused different influences on gene profiles during seedlings development. A total of 261 genes were identified to respond to H2S fumigation, among which 72 genes were co-regulated by Cys treatment. GO and KEGG enrichment analysis of the 189 genes, H2S but not Cys regulated DEGs, indicated that these genes mainly involved in plant hormone signal transduction, plant-pathogen interaction, phenylpropanoid biosynthesis, and MAPK signaling pathway. Most of these genes encoded proteins having DNA binding and transcription factor activities that play roles in a variety of plant developmental and environmental responses. Many stress-responsive genes and some Ca2+ signal associated genes were also included. Consequently, H2S regulated gene expression through its role as a gasotransmitter, rather than just as a substrate for Cys biogenesis, and these 189 genes were far more likely to function in H2S signal transduction independently of Cys. Our data will provide insights for revealing and enriching H2S signaling networks.
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spelling doaj.art-212091a30598423486afe3a80b0991fe2023-06-02T06:01:41ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-06-011410.3389/fpls.2023.11849911184991Transcriptomic analysis reveals the functions of H2S as a gasotransmitter independently of Cys in ArabidopsisHuihui Fang0Zhenyuan Yu1Kehong Xing2Lingyi Zhou3Yuke Shao4Xiaofang Zhang5Yanxi Pei6Lu Zhang7Key Laboratory of Quality and Safety Control for Subtropical Fruit and Vegetable, Ministry of Agriculture and Rural Affairs, Collaborative Innovation Center for Efficient and Green Production of Agriculture in Mountainous Areas of Zhejiang, College of Horticulture Science, Zhejiang Agriculture and Forestry University, Hangzhou, Zhejiang, ChinaKey Laboratory of Quality and Safety Control for Subtropical Fruit and Vegetable, Ministry of Agriculture and Rural Affairs, Collaborative Innovation Center for Efficient and Green Production of Agriculture in Mountainous Areas of Zhejiang, College of Horticulture Science, Zhejiang Agriculture and Forestry University, Hangzhou, Zhejiang, ChinaKey Laboratory of Quality and Safety Control for Subtropical Fruit and Vegetable, Ministry of Agriculture and Rural Affairs, Collaborative Innovation Center for Efficient and Green Production of Agriculture in Mountainous Areas of Zhejiang, College of Horticulture Science, Zhejiang Agriculture and Forestry University, Hangzhou, Zhejiang, ChinaKey Laboratory of Quality and Safety Control for Subtropical Fruit and Vegetable, Ministry of Agriculture and Rural Affairs, Collaborative Innovation Center for Efficient and Green Production of Agriculture in Mountainous Areas of Zhejiang, College of Horticulture Science, Zhejiang Agriculture and Forestry University, Hangzhou, Zhejiang, ChinaKey Laboratory of Quality and Safety Control for Subtropical Fruit and Vegetable, Ministry of Agriculture and Rural Affairs, Collaborative Innovation Center for Efficient and Green Production of Agriculture in Mountainous Areas of Zhejiang, College of Horticulture Science, Zhejiang Agriculture and Forestry University, Hangzhou, Zhejiang, ChinaKey Laboratory of Quality and Safety Control for Subtropical Fruit and Vegetable, Ministry of Agriculture and Rural Affairs, Collaborative Innovation Center for Efficient and Green Production of Agriculture in Mountainous Areas of Zhejiang, College of Horticulture Science, Zhejiang Agriculture and Forestry University, Hangzhou, Zhejiang, ChinaSchool of Life Science and Shanxi Key Laboratory for Research and Development of Regional Plants, Shanxi University, Taiyuan, Shanxi, ChinaZhejiang Provincial Key Laboratory of Bioremediation of Soil Contamination, College of Environment and Resources, College of Carbon Neutrality, Zhejiang Agriculture and Forestry University, Hangzhou, Zhejiang, ChinaNumerous studies have revealed the gasotransmitter functions of hydrogen sulfide (H2S) in various biological processes. However, the involvement of H2S in sulfur metabolism and/or Cys synthesis makes its role as a signaling molecule ambiguous. The generation of endogenous H2S in plants is closely related to the metabolism of Cys, which play roles in a variety of signaling pathway occurring in various cellular processes. Here, we found that exogenous H2S fumigation and Cys treatment modulated the production rate and content of endogenous H2S and Cys to various degrees. Furthermore, we provided comprehensive transcriptomic analysis to support the gasotransmitter role of H2S besides as a substrate for Cys synthesis. Comparison of the differentially expressed genes (DEGs) between H2S and Cys treated seedlings indicated that H2S fumigation and Cys treatment caused different influences on gene profiles during seedlings development. A total of 261 genes were identified to respond to H2S fumigation, among which 72 genes were co-regulated by Cys treatment. GO and KEGG enrichment analysis of the 189 genes, H2S but not Cys regulated DEGs, indicated that these genes mainly involved in plant hormone signal transduction, plant-pathogen interaction, phenylpropanoid biosynthesis, and MAPK signaling pathway. Most of these genes encoded proteins having DNA binding and transcription factor activities that play roles in a variety of plant developmental and environmental responses. Many stress-responsive genes and some Ca2+ signal associated genes were also included. Consequently, H2S regulated gene expression through its role as a gasotransmitter, rather than just as a substrate for Cys biogenesis, and these 189 genes were far more likely to function in H2S signal transduction independently of Cys. Our data will provide insights for revealing and enriching H2S signaling networks.https://www.frontiersin.org/articles/10.3389/fpls.2023.1184991/fullhydrogen sulfidegasotransmittercysteinetranscriptome sequencingArabidopsis
spellingShingle Huihui Fang
Zhenyuan Yu
Kehong Xing
Lingyi Zhou
Yuke Shao
Xiaofang Zhang
Yanxi Pei
Lu Zhang
Transcriptomic analysis reveals the functions of H2S as a gasotransmitter independently of Cys in Arabidopsis
Frontiers in Plant Science
hydrogen sulfide
gasotransmitter
cysteine
transcriptome sequencing
Arabidopsis
title Transcriptomic analysis reveals the functions of H2S as a gasotransmitter independently of Cys in Arabidopsis
title_full Transcriptomic analysis reveals the functions of H2S as a gasotransmitter independently of Cys in Arabidopsis
title_fullStr Transcriptomic analysis reveals the functions of H2S as a gasotransmitter independently of Cys in Arabidopsis
title_full_unstemmed Transcriptomic analysis reveals the functions of H2S as a gasotransmitter independently of Cys in Arabidopsis
title_short Transcriptomic analysis reveals the functions of H2S as a gasotransmitter independently of Cys in Arabidopsis
title_sort transcriptomic analysis reveals the functions of h2s as a gasotransmitter independently of cys in arabidopsis
topic hydrogen sulfide
gasotransmitter
cysteine
transcriptome sequencing
Arabidopsis
url https://www.frontiersin.org/articles/10.3389/fpls.2023.1184991/full
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