Integrated Transcriptome and Proteome Analysis Reveals the Regulatory Mechanism of Root Growth by Protein Disulfide Isomerase in Arabidopsis

Protein disulfide isomerase (PDI, EC 5.3.4.1) is a thiol-disulfide oxidoreductase that plays a crucial role in catalyzing the oxidation and rearrangement of disulfides in substrate proteins. In plants, PDI is primarily involved in regulating seed germination and development, facilitating the oxidati...

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Main Authors: Yanan Liu, Peng Song, Meilin Yan, Jinmei Luo, Yingjuan Wang, Fenggui Fan
Format: Article
Language:English
Published: MDPI AG 2024-03-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/25/7/3596
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author Yanan Liu
Peng Song
Meilin Yan
Jinmei Luo
Yingjuan Wang
Fenggui Fan
author_facet Yanan Liu
Peng Song
Meilin Yan
Jinmei Luo
Yingjuan Wang
Fenggui Fan
author_sort Yanan Liu
collection DOAJ
description Protein disulfide isomerase (PDI, EC 5.3.4.1) is a thiol-disulfide oxidoreductase that plays a crucial role in catalyzing the oxidation and rearrangement of disulfides in substrate proteins. In plants, PDI is primarily involved in regulating seed germination and development, facilitating the oxidative folding of storage proteins in the endosperm, and also contributing to the formation of pollen. However, the role of PDI in root growth has not been previously studied. This research investigated the impact of PDI gene deficiency in plants by using 16F16 [2-(2-Chloroacetyl)-2,3,4,9-tetrahydro-1-methyl-1H-pyrido[3,4-b]indole-1-carboxylic acid methyl ester], a small-molecule inhibitor of PDI, to remove functional redundancy. The results showed that the growth of Arabidopsis roots was significantly inhibited when treated with 16F16. To further investigate the effects of 16F16 treatment, we conducted expression profiling of treated roots using RNA sequencing and a Tandem Mass Tag (TMT)-based quantitative proteomics approach at both the transcriptomic and proteomic levels. Our analysis revealed 994 differentially expressed genes (DEGs) at the transcript level, which were predominantly enriched in pathways associated with “phenylpropane biosynthesis”, “plant hormone signal transduction”, “plant−pathogen interaction” and “starch and sucrose metabolism” pathways. Additionally, we identified 120 differentially expressed proteins (DEPs) at the protein level. These proteins were mainly enriched in pathways such as “phenylpropanoid biosynthesis”, “photosynthesis”, “biosynthesis of various plant secondary metabolites”, and “biosynthesis of secondary metabolites” pathways. The comprehensive transcriptome and proteome analyses revealed a regulatory network for root shortening in Arabidopsis seedlings under 16F16 treatment, mainly involving phenylpropane biosynthesis and plant hormone signal transduction pathways. This study enhances our understanding of the significant role of PDIs in Arabidopsis root growth and provides insights into the regulatory mechanisms of root shortening following 16F16 treatment.
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spelling doaj.art-bcc6418eb57c4eb19bbb07a1520d48122024-04-12T13:19:12ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672024-03-01257359610.3390/ijms25073596Integrated Transcriptome and Proteome Analysis Reveals the Regulatory Mechanism of Root Growth by Protein Disulfide Isomerase in ArabidopsisYanan Liu0Peng Song1Meilin Yan2Jinmei Luo3Yingjuan Wang4Fenggui Fan5State Key Laboratory of Biotechnology of Shannxi Province, College of Life Science, Northwest University, Xi’an 710069, ChinaState Key Laboratory of Biotechnology of Shannxi Province, College of Life Science, Northwest University, Xi’an 710069, ChinaState Key Laboratory of Biotechnology of Shannxi Province, College of Life Science, Northwest University, Xi’an 710069, ChinaState Key Laboratory of Biotechnology of Shannxi Province, College of Life Science, Northwest University, Xi’an 710069, ChinaState Key Laboratory of Biotechnology of Shannxi Province, College of Life Science, Northwest University, Xi’an 710069, ChinaState Key Laboratory of Biotechnology of Shannxi Province, College of Life Science, Northwest University, Xi’an 710069, ChinaProtein disulfide isomerase (PDI, EC 5.3.4.1) is a thiol-disulfide oxidoreductase that plays a crucial role in catalyzing the oxidation and rearrangement of disulfides in substrate proteins. In plants, PDI is primarily involved in regulating seed germination and development, facilitating the oxidative folding of storage proteins in the endosperm, and also contributing to the formation of pollen. However, the role of PDI in root growth has not been previously studied. This research investigated the impact of PDI gene deficiency in plants by using 16F16 [2-(2-Chloroacetyl)-2,3,4,9-tetrahydro-1-methyl-1H-pyrido[3,4-b]indole-1-carboxylic acid methyl ester], a small-molecule inhibitor of PDI, to remove functional redundancy. The results showed that the growth of Arabidopsis roots was significantly inhibited when treated with 16F16. To further investigate the effects of 16F16 treatment, we conducted expression profiling of treated roots using RNA sequencing and a Tandem Mass Tag (TMT)-based quantitative proteomics approach at both the transcriptomic and proteomic levels. Our analysis revealed 994 differentially expressed genes (DEGs) at the transcript level, which were predominantly enriched in pathways associated with “phenylpropane biosynthesis”, “plant hormone signal transduction”, “plant−pathogen interaction” and “starch and sucrose metabolism” pathways. Additionally, we identified 120 differentially expressed proteins (DEPs) at the protein level. These proteins were mainly enriched in pathways such as “phenylpropanoid biosynthesis”, “photosynthesis”, “biosynthesis of various plant secondary metabolites”, and “biosynthesis of secondary metabolites” pathways. The comprehensive transcriptome and proteome analyses revealed a regulatory network for root shortening in Arabidopsis seedlings under 16F16 treatment, mainly involving phenylpropane biosynthesis and plant hormone signal transduction pathways. This study enhances our understanding of the significant role of PDIs in Arabidopsis root growth and provides insights into the regulatory mechanisms of root shortening following 16F16 treatment.https://www.mdpi.com/1422-0067/25/7/3596protein disulfide isomerasetranscriptomeproteomerootArabidopsis16F16
spellingShingle Yanan Liu
Peng Song
Meilin Yan
Jinmei Luo
Yingjuan Wang
Fenggui Fan
Integrated Transcriptome and Proteome Analysis Reveals the Regulatory Mechanism of Root Growth by Protein Disulfide Isomerase in Arabidopsis
International Journal of Molecular Sciences
protein disulfide isomerase
transcriptome
proteome
root
Arabidopsis
16F16
title Integrated Transcriptome and Proteome Analysis Reveals the Regulatory Mechanism of Root Growth by Protein Disulfide Isomerase in Arabidopsis
title_full Integrated Transcriptome and Proteome Analysis Reveals the Regulatory Mechanism of Root Growth by Protein Disulfide Isomerase in Arabidopsis
title_fullStr Integrated Transcriptome and Proteome Analysis Reveals the Regulatory Mechanism of Root Growth by Protein Disulfide Isomerase in Arabidopsis
title_full_unstemmed Integrated Transcriptome and Proteome Analysis Reveals the Regulatory Mechanism of Root Growth by Protein Disulfide Isomerase in Arabidopsis
title_short Integrated Transcriptome and Proteome Analysis Reveals the Regulatory Mechanism of Root Growth by Protein Disulfide Isomerase in Arabidopsis
title_sort integrated transcriptome and proteome analysis reveals the regulatory mechanism of root growth by protein disulfide isomerase in arabidopsis
topic protein disulfide isomerase
transcriptome
proteome
root
Arabidopsis
16F16
url https://www.mdpi.com/1422-0067/25/7/3596
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AT pengsong integratedtranscriptomeandproteomeanalysisrevealstheregulatorymechanismofrootgrowthbyproteindisulfideisomeraseinarabidopsis
AT meilinyan integratedtranscriptomeandproteomeanalysisrevealstheregulatorymechanismofrootgrowthbyproteindisulfideisomeraseinarabidopsis
AT jinmeiluo integratedtranscriptomeandproteomeanalysisrevealstheregulatorymechanismofrootgrowthbyproteindisulfideisomeraseinarabidopsis
AT yingjuanwang integratedtranscriptomeandproteomeanalysisrevealstheregulatorymechanismofrootgrowthbyproteindisulfideisomeraseinarabidopsis
AT fengguifan integratedtranscriptomeandproteomeanalysisrevealstheregulatorymechanismofrootgrowthbyproteindisulfideisomeraseinarabidopsis