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{"title":"Coprinellus disseminates ArsM confers multi-layer arsenic resistance in transgenic tobacco by coordinating detoxification, photosynthetic protection, and stress signaling","authors":"Yalin Yang, Fuxin Yang, Lijun Qin","doi":"10.1016/j.envexpbot.2025.106236","DOIUrl":null,"url":null,"abstract":"<div><div>Plant arsenic pollution, entering the food chain via soil-plant systems, constitutes a global environmental health threat. The macrofungus <em>Coprinellus disseminatus</em> (Pers.:Fr.) J.E. Lange, endemic to arsenic-contaminated areas of Bijie, China, exhibits exceptional arsenic resistance confirmed through physiological analysis under arsenic exposure. Integrated transcriptomics identified key resistance genes (<em>CdACR3</em>, <em>CdsHSP</em>, <em>CdSEP</em>, <em>CdArsM</em>), with qRT-PCR revealing time-dependent upregulation of <em>CdArsM</em> and <em>CdACR3</em> during prolonged arsenic stress. Given reported roles of ArsM orthologs in plant tolerance, we engineered codon-optimized <em>CdArsM</em>-expressing <em>Nicotiana tabacum</em> transgenics. Under arsenic stress, transgenic lines showed enhancing chloroplast/mitochondrial integrity, significantly reducing ROS accumulation (O₂˙⁻, H₂O₂), lower oxidative damage (reduced MDA) and elevating antioxidant enzyme activity. Transcriptomics revealed pronounced enrichment of upregulated DEGs in arsenic-stressed transgenics (12 h) versus wild-type across: photosynthesis, phenylpropanoid metabolism, light-circadian signaling, energy-carbon partitioning, stress transduction, and redox homeostasis. qRT-PCR further validated progressive upregulation of key regulators: phosphate transporter (<em>Pht1;1</em>), metal transporter (<em>MTP1</em>), transcription factor (<em>NAC029</em>), and glutathione peroxidase (<em>GSH2</em>). These results demonstrate <em>CdArsM</em>-mediated arsenic resistance involves coordinated activation of complementary physiological pathways.</div></div>","PeriodicalId":11758,"journal":{"name":"Environmental and Experimental Botany","volume":"238 ","pages":"Article 106236"},"PeriodicalIF":4.7000,"publicationDate":"2025-09-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Environmental and Experimental Botany","FirstCategoryId":"99","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S0098847225001534","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"ENVIRONMENTAL SCIENCES","Score":null,"Total":0}
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Abstract
Plant arsenic pollution, entering the food chain via soil-plant systems, constitutes a global environmental health threat. The macrofungus Coprinellus disseminatus (Pers.:Fr.) J.E. Lange, endemic to arsenic-contaminated areas of Bijie, China, exhibits exceptional arsenic resistance confirmed through physiological analysis under arsenic exposure. Integrated transcriptomics identified key resistance genes (CdACR3 , CdsHSP , CdSEP , CdArsM ), with qRT-PCR revealing time-dependent upregulation of CdArsM and CdACR3 during prolonged arsenic stress. Given reported roles of ArsM orthologs in plant tolerance, we engineered codon-optimized CdArsM -expressing Nicotiana tabacum transgenics. Under arsenic stress, transgenic lines showed enhancing chloroplast/mitochondrial integrity, significantly reducing ROS accumulation (O₂˙⁻, H₂O₂), lower oxidative damage (reduced MDA) and elevating antioxidant enzyme activity. Transcriptomics revealed pronounced enrichment of upregulated DEGs in arsenic-stressed transgenics (12 h) versus wild-type across: photosynthesis, phenylpropanoid metabolism, light-circadian signaling, energy-carbon partitioning, stress transduction, and redox homeostasis. qRT-PCR further validated progressive upregulation of key regulators: phosphate transporter (Pht1;1 ), metal transporter (MTP1 ), transcription factor (NAC029 ), and glutathione peroxidase (GSH2 ). These results demonstrate CdArsM -mediated arsenic resistance involves coordinated activation of complementary physiological pathways.
在转基因烟草中,共胞菌通过协调解毒、光合保护和胁迫信号传递,使其具有多层抗砷性
植物砷污染通过土壤-植物系统进入食物链,对全球环境健康构成威胁。大型真菌广布铜菌(Coprinellus propagatus)中国毕节砷污染地区特有的je.l ange在砷暴露下表现出特殊的抗砷性,通过生理分析证实。整合转录组学鉴定出关键抗性基因(CdACR3、CdsHSP、CdSEP、cdacsm), qRT-PCR揭示了在长时间砷胁迫下cdacsm和CdACR3的时间依赖性上调。鉴于已有报道的ArsM同源物在植物耐受性中的作用,我们设计了密码子优化的表达cdarsm的烟草转基因。在砷胁迫下,转基因品系表现出增强叶绿体/线粒体完整性,显著减少ROS积累(O₂˙⁻,H₂O₂),降低氧化损伤(减少MDA)和提高抗氧化酶活性。转录组学显示,与野生型相比,砷胁迫转基因(12 h)在光合作用、苯丙代谢、光-昼夜节律信号、能量-碳分配、应激转导和氧化还原稳态中明显富集上调的DEGs。qRT-PCR进一步验证了关键调控因子的进行性上调:磷酸盐转运蛋白(Pht1;1)、金属转运蛋白(MTP1)、转录因子(NAC029)和谷胱甘肽过氧化物酶(GSH2)。这些结果表明cdsm介导的砷抗性涉及互补生理途径的协调激活。
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