Proteome and phosphoproteome analysis of 2,4-epibrassinolide-mediated cold stress response in cucumber seedlings

The 2, 4-epibrassinolide (EBR) significantly increased plants cold tolerance. However, mechanisms of EBR in regulating cold tolerance in phosphoproteome and proteome levels have not been reported. The mechanism of EBR regulating cold response in cucumber was studied by multiple omics analysis. In th...

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Main Authors: Mengdi Zhou, Yansu Li, Yan Yan, Lihong Gao, Chaoxing He, Jun Wang, Quan Yuan, Li Miao, Shuzhen Li, Qinghua Di, Xianchang Yu, Mintao Sun
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-02-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2023.1104036/full
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author Mengdi Zhou
Mengdi Zhou
Yansu Li
Yan Yan
Lihong Gao
Chaoxing He
Jun Wang
Quan Yuan
Li Miao
Shuzhen Li
Qinghua Di
Xianchang Yu
Mintao Sun
author_facet Mengdi Zhou
Mengdi Zhou
Yansu Li
Yan Yan
Lihong Gao
Chaoxing He
Jun Wang
Quan Yuan
Li Miao
Shuzhen Li
Qinghua Di
Xianchang Yu
Mintao Sun
author_sort Mengdi Zhou
collection DOAJ
description The 2, 4-epibrassinolide (EBR) significantly increased plants cold tolerance. However, mechanisms of EBR in regulating cold tolerance in phosphoproteome and proteome levels have not been reported. The mechanism of EBR regulating cold response in cucumber was studied by multiple omics analysis. In this study, phosphoproteome analysis showed that cucumber responded to cold stress through multi-site serine phosphorylation, while EBR further upregulated single-site phosphorylation for most of cold-responsive phosphoproteins. Association analysis of the proteome and phosphoproteome revealed that EBR reprogrammed proteins in response to cold stress by negatively regulating protein phosphorylation and protein content, and phosphorylation negatively regulated protein content in cucumber. Further functional enrichment analysis of proteome and phosphoproteome showed that cucumber mainly upregulated phosphoproteins related to spliceosome, nucleotide binding and photosynthetic pathways in response to cold stress. However, different from the EBR regulation in omics level, hypergeometric analysis showed that EBR further upregulated 16 cold-up-responsive phosphoproteins participated photosynthetic and nucleotide binding pathways in response to cold stress, suggested their important function in cold tolerance. Analysis of cold-responsive transcription factors (TFs) by correlation between proteome and phosphoproteome showed that cucumber regulated eight class TFs may through protein phosphorylation under cold stress. Further combined with cold-related transcriptome found that cucumber phosphorylated eight class TFs, and mainly through targeting major hormone signal genes by bZIP TFs in response to cold stress, while EBR further increased these bZIP TFs (CsABI5.2 and CsABI5.5) phosphorylation level. In conclusion, the EBR mediated schematic of molecule response mechanisms in cucumber under cold stress was proposed.
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spelling doaj.art-d133dda3ed9c4727bf0b8613d17150ac2023-02-21T06:20:50ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-02-011410.3389/fpls.2023.11040361104036Proteome and phosphoproteome analysis of 2,4-epibrassinolide-mediated cold stress response in cucumber seedlingsMengdi Zhou0Mengdi Zhou1Yansu Li2Yan Yan3Lihong Gao4Chaoxing He5Jun Wang6Quan Yuan7Li Miao8Shuzhen Li9Qinghua Di10Xianchang Yu11Mintao Sun12State Key Laboratory of Vegetable Biobreeding, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing, ChinaBeijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Tablecrops, China Agricultural University, Beijing, ChinaState Key Laboratory of Vegetable Biobreeding, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing, ChinaState Key Laboratory of Vegetable Biobreeding, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing, ChinaBeijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Tablecrops, China Agricultural University, Beijing, ChinaState Key Laboratory of Vegetable Biobreeding, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing, ChinaState Key Laboratory of Vegetable Biobreeding, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing, ChinaCollege of Horticulture, Sichuan Agricultural University, Chengdu, ChinaCollege of Horticulture, Zhejiang A & F University, Hangzhou, ChinaCollege of Life Science, Gannan Normal University, Ganzhou, ChinaState Key Laboratory of Vegetable Biobreeding, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing, ChinaState Key Laboratory of Vegetable Biobreeding, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing, ChinaState Key Laboratory of Vegetable Biobreeding, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing, ChinaThe 2, 4-epibrassinolide (EBR) significantly increased plants cold tolerance. However, mechanisms of EBR in regulating cold tolerance in phosphoproteome and proteome levels have not been reported. The mechanism of EBR regulating cold response in cucumber was studied by multiple omics analysis. In this study, phosphoproteome analysis showed that cucumber responded to cold stress through multi-site serine phosphorylation, while EBR further upregulated single-site phosphorylation for most of cold-responsive phosphoproteins. Association analysis of the proteome and phosphoproteome revealed that EBR reprogrammed proteins in response to cold stress by negatively regulating protein phosphorylation and protein content, and phosphorylation negatively regulated protein content in cucumber. Further functional enrichment analysis of proteome and phosphoproteome showed that cucumber mainly upregulated phosphoproteins related to spliceosome, nucleotide binding and photosynthetic pathways in response to cold stress. However, different from the EBR regulation in omics level, hypergeometric analysis showed that EBR further upregulated 16 cold-up-responsive phosphoproteins participated photosynthetic and nucleotide binding pathways in response to cold stress, suggested their important function in cold tolerance. Analysis of cold-responsive transcription factors (TFs) by correlation between proteome and phosphoproteome showed that cucumber regulated eight class TFs may through protein phosphorylation under cold stress. Further combined with cold-related transcriptome found that cucumber phosphorylated eight class TFs, and mainly through targeting major hormone signal genes by bZIP TFs in response to cold stress, while EBR further increased these bZIP TFs (CsABI5.2 and CsABI5.5) phosphorylation level. In conclusion, the EBR mediated schematic of molecule response mechanisms in cucumber under cold stress was proposed.https://www.frontiersin.org/articles/10.3389/fpls.2023.1104036/fullbrassinosteroid (BR)cold stresscucumber seedlingphosphoproteomeproteome
spellingShingle Mengdi Zhou
Mengdi Zhou
Yansu Li
Yan Yan
Lihong Gao
Chaoxing He
Jun Wang
Quan Yuan
Li Miao
Shuzhen Li
Qinghua Di
Xianchang Yu
Mintao Sun
Proteome and phosphoproteome analysis of 2,4-epibrassinolide-mediated cold stress response in cucumber seedlings
Frontiers in Plant Science
brassinosteroid (BR)
cold stress
cucumber seedling
phosphoproteome
proteome
title Proteome and phosphoproteome analysis of 2,4-epibrassinolide-mediated cold stress response in cucumber seedlings
title_full Proteome and phosphoproteome analysis of 2,4-epibrassinolide-mediated cold stress response in cucumber seedlings
title_fullStr Proteome and phosphoproteome analysis of 2,4-epibrassinolide-mediated cold stress response in cucumber seedlings
title_full_unstemmed Proteome and phosphoproteome analysis of 2,4-epibrassinolide-mediated cold stress response in cucumber seedlings
title_short Proteome and phosphoproteome analysis of 2,4-epibrassinolide-mediated cold stress response in cucumber seedlings
title_sort proteome and phosphoproteome analysis of 2 4 epibrassinolide mediated cold stress response in cucumber seedlings
topic brassinosteroid (BR)
cold stress
cucumber seedling
phosphoproteome
proteome
url https://www.frontiersin.org/articles/10.3389/fpls.2023.1104036/full
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