Uncovering the key miRNA-target network of tea plants in resistance to sooty mold disease

Abstract Background Sooty mold (SM) disease severely threatens tea plant health, reducing yield and quality. Driven by climate change and intensive farming practices, SM prevalence in China has surged, causing significant economic losses and forcing farmers to rely on chemical fungicides, which comp...

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Main Authors: Shuangshuang Wang, Ran Zhang, Litao Sun, Xiuxiu Xu, Jiazhi Shen, Xiaojiang Li, Chaoling Wei, Zhaotang Ding, Shengrui Liu
Format: Article
Language:English
Published: BMC 2025-04-01
Series:BMC Plant Biology
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Online Access:https://doi.org/10.1186/s12870-025-06509-7
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author Shuangshuang Wang
Ran Zhang
Litao Sun
Xiuxiu Xu
Jiazhi Shen
Xiaojiang Li
Chaoling Wei
Zhaotang Ding
Shengrui Liu
author_facet Shuangshuang Wang
Ran Zhang
Litao Sun
Xiuxiu Xu
Jiazhi Shen
Xiaojiang Li
Chaoling Wei
Zhaotang Ding
Shengrui Liu
author_sort Shuangshuang Wang
collection DOAJ
description Abstract Background Sooty mold (SM) disease severely threatens tea plant health, reducing yield and quality. Driven by climate change and intensive farming practices, SM prevalence in China has surged, causing significant economic losses and forcing farmers to rely on chemical fungicides, which compromise environmental sustainability. Despite its impact, the molecular mechanisms underlying tea plant defenses against SM remain unclear. Results Integrated transcriptomic, sRNAome, and degradome analyses revealed that differentially expressed genes (DEGs) exhibited infection-level-dependent expression patterns. Post-transcriptional regulation by miRNAs was identified through sRNAome-degradome mapping, with six miRNA-target defense pairs validated by 5′ RLM-RACE and qRT-PCR. Co-expression network analysis showed that two miRNA-target pairs, PC-5p-33681_128-auxin response factor (CsARF) and ppe-MIR535b-p3-1ss12TC-aldehyde dehydrogenase (CsALDH), play crucial roles in responding to SM infection. Furthermore, 5′ RLM-RACE and dual-luciferase assays revealed that the PC-5p-33681_128 and ppe-MIR535b-p3-1ss12TC could regulate the expression of CsARF and CsALDH by mRNA cleavage, respectively. Conclusion This study elucidates miRNA-mediated defense networks in tea plants against SM, offering actionable targets for breeding SM-resistant cultivars via genetic engineering or marker-assisted selection. Implementing these strategies could reduce yield losses, stabilize farmer incomes, and minimize environmental harm from fungicide overuse. This work advances climate-resilient practices for the global tea industry by linking molecular insights to sustainable agriculture.
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spelling doaj-art-8e73a0b5e4da4e02aaee073cb20b367f2025-08-20T02:11:41ZengBMCBMC Plant Biology1471-22292025-04-0125111310.1186/s12870-025-06509-7Uncovering the key miRNA-target network of tea plants in resistance to sooty mold diseaseShuangshuang Wang0Ran Zhang1Litao Sun2Xiuxiu Xu3Jiazhi Shen4Xiaojiang Li5Chaoling Wei6Zhaotang Ding7Shengrui Liu8Tea Research Institute, Shandong Academy of Agricultural SciencesSericultural Research Institute, Anhui Academy of Agricultural SciencesTea Research Institute, Shandong Academy of Agricultural SciencesTea Research Institute, Shandong Academy of Agricultural SciencesTea Research Institute, Shandong Academy of Agricultural SciencesTea Research Institute, Shandong Academy of Agricultural SciencesState Key Laboratory of Tea Plant Biology and Utilization, Anhui Agricultural UniversityTea Research Institute, Shandong Academy of Agricultural SciencesState Key Laboratory of Tea Plant Biology and Utilization, Anhui Agricultural UniversityAbstract Background Sooty mold (SM) disease severely threatens tea plant health, reducing yield and quality. Driven by climate change and intensive farming practices, SM prevalence in China has surged, causing significant economic losses and forcing farmers to rely on chemical fungicides, which compromise environmental sustainability. Despite its impact, the molecular mechanisms underlying tea plant defenses against SM remain unclear. Results Integrated transcriptomic, sRNAome, and degradome analyses revealed that differentially expressed genes (DEGs) exhibited infection-level-dependent expression patterns. Post-transcriptional regulation by miRNAs was identified through sRNAome-degradome mapping, with six miRNA-target defense pairs validated by 5′ RLM-RACE and qRT-PCR. Co-expression network analysis showed that two miRNA-target pairs, PC-5p-33681_128-auxin response factor (CsARF) and ppe-MIR535b-p3-1ss12TC-aldehyde dehydrogenase (CsALDH), play crucial roles in responding to SM infection. Furthermore, 5′ RLM-RACE and dual-luciferase assays revealed that the PC-5p-33681_128 and ppe-MIR535b-p3-1ss12TC could regulate the expression of CsARF and CsALDH by mRNA cleavage, respectively. Conclusion This study elucidates miRNA-mediated defense networks in tea plants against SM, offering actionable targets for breeding SM-resistant cultivars via genetic engineering or marker-assisted selection. Implementing these strategies could reduce yield losses, stabilize farmer incomes, and minimize environmental harm from fungicide overuse. This work advances climate-resilient practices for the global tea industry by linking molecular insights to sustainable agriculture.https://doi.org/10.1186/s12870-025-06509-7Tea plantsSooty mold diseaseDefense responseIntegration analysismiRNA-target circuits
spellingShingle Shuangshuang Wang
Ran Zhang
Litao Sun
Xiuxiu Xu
Jiazhi Shen
Xiaojiang Li
Chaoling Wei
Zhaotang Ding
Shengrui Liu
Uncovering the key miRNA-target network of tea plants in resistance to sooty mold disease
BMC Plant Biology
Tea plants
Sooty mold disease
Defense response
Integration analysis
miRNA-target circuits
title Uncovering the key miRNA-target network of tea plants in resistance to sooty mold disease
title_full Uncovering the key miRNA-target network of tea plants in resistance to sooty mold disease
title_fullStr Uncovering the key miRNA-target network of tea plants in resistance to sooty mold disease
title_full_unstemmed Uncovering the key miRNA-target network of tea plants in resistance to sooty mold disease
title_short Uncovering the key miRNA-target network of tea plants in resistance to sooty mold disease
title_sort uncovering the key mirna target network of tea plants in resistance to sooty mold disease
topic Tea plants
Sooty mold disease
Defense response
Integration analysis
miRNA-target circuits
url https://doi.org/10.1186/s12870-025-06509-7
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