Combined metabolomic and transcriptomic analysis to reveal the response of rice to Mn toxicity stress
Excessive manganese (Mn) concentrations affect plant gene expression, alter metabolite content, and impede plant growth. Rice plants are particularly susceptible to Mn toxicity stress in acidic soil; however, the underlying molecular mechanisms are so far unclear. This study used transcriptomic and...
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Elsevier
2025-01-01
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| Series: | Ecotoxicology and Environmental Safety |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S0147651324015306 |
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| author | Feng Li Yushuang Yao Jiapeng Ma Zhengwei Wu Dianfeng Zheng Yingbin Xue Ying Liu |
| author_facet | Feng Li Yushuang Yao Jiapeng Ma Zhengwei Wu Dianfeng Zheng Yingbin Xue Ying Liu |
| author_sort | Feng Li |
| collection | DOAJ |
| description | Excessive manganese (Mn) concentrations affect plant gene expression, alter metabolite content, and impede plant growth. Rice plants are particularly susceptible to Mn toxicity stress in acidic soil; however, the underlying molecular mechanisms are so far unclear. This study used transcriptomic and metabolomic sequencing to examine roots and leaves of rice plants subjected to Mn toxicity stress. The findings showed that high Mn stress increased the content of malondialdehyde, proline, and soluble sugar in rice roots by 262.28 %, 803.37 %, and 167.25 %, respectively. In rice roots, the enzymatic activities of peroxidase (POD), superoxide dismutase (SOD), catalase (CAT), and ascorbate peroxidase (APX) elevated by 119.69 %, 408.44 %, 151.97 %, and 27.19 %, respectively. In rice leaves, the proline content increased by 632.45 %, whereas the enzymatic activities of POD, SOD, CAT, and APX were elevated by 167.17 %, 14.08 %, 103.60 %, and 146.74 %, respectively. Mn toxicity stress decreased soluble protein content in rice roots, and in the leaves, it reduced the soluble protein, soluble sugar, and chlorophyll contents. In addition, Mn toxicity led to reduced biomass accumulation, plant height, stem diameter, and root growth. The contents of salicylic acid (increased by 118.40 % in roots and 66.38 % in leaves) and jasmonic acid (decreased by 50.18 % in roots and increased by 143.97 % in leaves) were also affected. Transcriptome analysis identified differentially expressed genes associated with transcription factors, antioxidant enzymes, and metal transporters. Metabolomics revealed 176 and 214 different metabolites in the roots and leaves, respectively, that under Mn toxicity stress affected major metabolic pathways associated with fatty and amino acids. The phenylalanine metabolism pathway was significantly enriched in both the roots and leaves. Combined transcriptomic and metabolomic analyses revealed three key pathways: lysine degradation and phenylpropanoid biosynthesis in roots and alpha-linolenic acid metabolism in leaves. Metabolic substances and genes associated with metabolic enzymes were identified. These results enhance our understanding of the molecular processes underlying the responses of rice to Mn toxicity stress and provide a basis for breeding Mn-tolerant rice varieties. |
| format | Article |
| id | doaj-art-077d48bc7c4a4f79b41c97d1525b232b |
| institution | Kabale University |
| issn | 0147-6513 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Elsevier |
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| series | Ecotoxicology and Environmental Safety |
| spelling | doaj-art-077d48bc7c4a4f79b41c97d1525b232b2025-01-23T05:25:37ZengElsevierEcotoxicology and Environmental Safety0147-65132025-01-01289117454Combined metabolomic and transcriptomic analysis to reveal the response of rice to Mn toxicity stressFeng Li0Yushuang Yao1Jiapeng Ma2Zhengwei Wu3Dianfeng Zheng4Yingbin Xue5Ying Liu6Department of Agronomy, College of Coastal Agricultural Sciences, Guangdong Ocean University, Zhanjiang 524088, ChinaDepartment of Agronomy, College of Coastal Agricultural Sciences, Guangdong Ocean University, Zhanjiang 524088, ChinaDepartment of Agronomy, College of Coastal Agricultural Sciences, Guangdong Ocean University, Zhanjiang 524088, ChinaDepartment of Agronomy, College of Coastal Agricultural Sciences, Guangdong Ocean University, Zhanjiang 524088, ChinaDepartment of Agronomy, College of Coastal Agricultural Sciences, Guangdong Ocean University, Zhanjiang 524088, ChinaDepartment of Agronomy, College of Coastal Agricultural Sciences, Guangdong Ocean University, Zhanjiang 524088, ChinaCorresponding author.; Department of Agronomy, College of Coastal Agricultural Sciences, Guangdong Ocean University, Zhanjiang 524088, ChinaExcessive manganese (Mn) concentrations affect plant gene expression, alter metabolite content, and impede plant growth. Rice plants are particularly susceptible to Mn toxicity stress in acidic soil; however, the underlying molecular mechanisms are so far unclear. This study used transcriptomic and metabolomic sequencing to examine roots and leaves of rice plants subjected to Mn toxicity stress. The findings showed that high Mn stress increased the content of malondialdehyde, proline, and soluble sugar in rice roots by 262.28 %, 803.37 %, and 167.25 %, respectively. In rice roots, the enzymatic activities of peroxidase (POD), superoxide dismutase (SOD), catalase (CAT), and ascorbate peroxidase (APX) elevated by 119.69 %, 408.44 %, 151.97 %, and 27.19 %, respectively. In rice leaves, the proline content increased by 632.45 %, whereas the enzymatic activities of POD, SOD, CAT, and APX were elevated by 167.17 %, 14.08 %, 103.60 %, and 146.74 %, respectively. Mn toxicity stress decreased soluble protein content in rice roots, and in the leaves, it reduced the soluble protein, soluble sugar, and chlorophyll contents. In addition, Mn toxicity led to reduced biomass accumulation, plant height, stem diameter, and root growth. The contents of salicylic acid (increased by 118.40 % in roots and 66.38 % in leaves) and jasmonic acid (decreased by 50.18 % in roots and increased by 143.97 % in leaves) were also affected. Transcriptome analysis identified differentially expressed genes associated with transcription factors, antioxidant enzymes, and metal transporters. Metabolomics revealed 176 and 214 different metabolites in the roots and leaves, respectively, that under Mn toxicity stress affected major metabolic pathways associated with fatty and amino acids. The phenylalanine metabolism pathway was significantly enriched in both the roots and leaves. Combined transcriptomic and metabolomic analyses revealed three key pathways: lysine degradation and phenylpropanoid biosynthesis in roots and alpha-linolenic acid metabolism in leaves. Metabolic substances and genes associated with metabolic enzymes were identified. These results enhance our understanding of the molecular processes underlying the responses of rice to Mn toxicity stress and provide a basis for breeding Mn-tolerant rice varieties.http://www.sciencedirect.com/science/article/pii/S0147651324015306Oryza sativaMn toxicity stressMetabolomeTranscriptomeKey pathways |
| spellingShingle | Feng Li Yushuang Yao Jiapeng Ma Zhengwei Wu Dianfeng Zheng Yingbin Xue Ying Liu Combined metabolomic and transcriptomic analysis to reveal the response of rice to Mn toxicity stress Ecotoxicology and Environmental Safety Oryza sativa Mn toxicity stress Metabolome Transcriptome Key pathways |
| title | Combined metabolomic and transcriptomic analysis to reveal the response of rice to Mn toxicity stress |
| title_full | Combined metabolomic and transcriptomic analysis to reveal the response of rice to Mn toxicity stress |
| title_fullStr | Combined metabolomic and transcriptomic analysis to reveal the response of rice to Mn toxicity stress |
| title_full_unstemmed | Combined metabolomic and transcriptomic analysis to reveal the response of rice to Mn toxicity stress |
| title_short | Combined metabolomic and transcriptomic analysis to reveal the response of rice to Mn toxicity stress |
| title_sort | combined metabolomic and transcriptomic analysis to reveal the response of rice to mn toxicity stress |
| topic | Oryza sativa Mn toxicity stress Metabolome Transcriptome Key pathways |
| url | http://www.sciencedirect.com/science/article/pii/S0147651324015306 |
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