{"title":"Navel orange postharvest resistance towards Penicillium digitatum − role of histone demethylase CsJMJ12","authors":"Jing Zeng, Ting Li, Mengting Liu, Jiechun Peng, Xiaoyan Duan, Zhiwei Li, Guoxiang Jiang, Jianbo Xiao, Yueming Jiang, Xuewu Duan","doi":"10.1016/j.jare.2025.10.012","DOIUrl":null,"url":null,"abstract":"<h3>Introduction</h3>Histone methylation is essential for plant growth and development, and adaptation to biotic and abiotic stresses. However, its role in postharvest disease resistance in fruits remains poorly understood. The study aimed to investigate the involvement of histone demethylase CsJMJ12 in enhancing postharvest resistance to <em>Penicillium digitatum</em> in Navel orange (<em>Citrus sinensis</em>).<h3>Methods</h3>Jumonji (JmjC) domain-containing proteins (JMJs) potentially involved in resistance to <em>P. digitatum</em> in Navel orange were identified using bioinformatics analysis, artificial inoculation and RT-qPCR<em>.</em> The role of JMJ12 in disease resistance and its underlying mechanism were further investigated through a series of assays, including subcellular location, Western blotting, immunofluorescence staining, transient overexpression, RNA-seq, widely targeted metabolomics, chromatin Immunoprecipitation (ChIP)-qPCR.<h3>Results</h3>A total of 17 JMJs were identified from the citrus genome. In Navel orange infected with <em>P. digitatum</em>, the expression of <em>CsJMJ12</em> was significantly upregulated. CsJMJ12 is localized to the nuclei and functions as a site-specific H3K27me3 histone demethylase. Overexpressing <em>CsJMJ12</em> transiently in fruit resulted in increased resistance to <em>P. digitatum</em>, accompanied by reduced global H3K27me3 levels. Transcriptome sequencing revealed that CsJMJ12 regulates multiple defense pathways, including phenylpropanoid biosynthesis, lignin biosynthesis, cell wall organization, pathogenesis-related protein, and hormone signaling. Metabolomics showed that CsJMJ12 regulates the accumulation of disease-resistant metabolites such as dihydrocoumarin, caffeoylputrescine, prenylnaringenin, quinic acid and syringic acid in phenylpropanoid biosynthesis pathways. Furthermore, CsJMJ12 promoted the expression of key defense-associated genes, including <em>POD, COMT1, LAC7L, SAME, SAMT, CHI, GT2</em> and <em>CSL5</em>, by demethylating H3K27me3 at their chromatin loci, thereby enhancing fruit resistance to <em>P. digitatum</em>.<h3>Conclusions</h3>This study identifies CsJMJ12 as a potential epigenetic regulator of <em>P. digitatum</em> resistance in Navel orange. Our findings provide valuable insights into the molecular mechanism of pathogen defense in sweet orange (<em>Citrus sinensis</em>). Further studies are needed to explore its broader application in agricultural practices and postharvest disease management.","PeriodicalId":14952,"journal":{"name":"Journal of Advanced Research","volume":"114 1","pages":""},"PeriodicalIF":13.0000,"publicationDate":"2025-10-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of Advanced Research","FirstCategoryId":"103","ListUrlMain":"https://doi.org/10.1016/j.jare.2025.10.012","RegionNum":1,"RegionCategory":"综合性期刊","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"MULTIDISCIPLINARY SCIENCES","Score":null,"Total":0}
引用次数: 0
Abstract
Introduction
Histone methylation is essential for plant growth and development, and adaptation to biotic and abiotic stresses. However, its role in postharvest disease resistance in fruits remains poorly understood. The study aimed to investigate the involvement of histone demethylase CsJMJ12 in enhancing postharvest resistance to Penicillium digitatum in Navel orange (Citrus sinensis).
Methods
Jumonji (JmjC) domain-containing proteins (JMJs) potentially involved in resistance to P. digitatum in Navel orange were identified using bioinformatics analysis, artificial inoculation and RT-qPCR. The role of JMJ12 in disease resistance and its underlying mechanism were further investigated through a series of assays, including subcellular location, Western blotting, immunofluorescence staining, transient overexpression, RNA-seq, widely targeted metabolomics, chromatin Immunoprecipitation (ChIP)-qPCR.
Results
A total of 17 JMJs were identified from the citrus genome. In Navel orange infected with P. digitatum, the expression of CsJMJ12 was significantly upregulated. CsJMJ12 is localized to the nuclei and functions as a site-specific H3K27me3 histone demethylase. Overexpressing CsJMJ12 transiently in fruit resulted in increased resistance to P. digitatum, accompanied by reduced global H3K27me3 levels. Transcriptome sequencing revealed that CsJMJ12 regulates multiple defense pathways, including phenylpropanoid biosynthesis, lignin biosynthesis, cell wall organization, pathogenesis-related protein, and hormone signaling. Metabolomics showed that CsJMJ12 regulates the accumulation of disease-resistant metabolites such as dihydrocoumarin, caffeoylputrescine, prenylnaringenin, quinic acid and syringic acid in phenylpropanoid biosynthesis pathways. Furthermore, CsJMJ12 promoted the expression of key defense-associated genes, including POD, COMT1, LAC7L, SAME, SAMT, CHI, GT2 and CSL5, by demethylating H3K27me3 at their chromatin loci, thereby enhancing fruit resistance to P. digitatum.
Conclusions
This study identifies CsJMJ12 as a potential epigenetic regulator of P. digitatum resistance in Navel orange. Our findings provide valuable insights into the molecular mechanism of pathogen defense in sweet orange (Citrus sinensis). Further studies are needed to explore its broader application in agricultural practices and postharvest disease management.
期刊介绍:
Journal of Advanced Research (J. Adv. Res.) is an applied/natural sciences, peer-reviewed journal that focuses on interdisciplinary research. The journal aims to contribute to applied research and knowledge worldwide through the publication of original and high-quality research articles in the fields of Medicine, Pharmaceutical Sciences, Dentistry, Physical Therapy, Veterinary Medicine, and Basic and Biological Sciences.
The following abstracting and indexing services cover the Journal of Advanced Research: PubMed/Medline, Essential Science Indicators, Web of Science, Scopus, PubMed Central, PubMed, Science Citation Index Expanded, Directory of Open Access Journals (DOAJ), and INSPEC.