Transcriptome-based analysis reveals key molecular mechanisms and functional characterization of MaCAX3 gene involved in manganese stress responses in mulberry plants
Background Manganese (Mn) deficiency and toxicity are major constraints on crop production in soil. Plants have evolved cascade strategies and specific mechanisms to tolerate these stresses. Understanding the molecular mechanisms of tolerance to Mn stress is crucial for improving the efficiency of c...
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| Published in | BMC plant biology Vol. 25; no. 1; pp. 971 - 27 |
|---|---|
| Main Authors | , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
BioMed Central
29.07.2025
BioMed Central Ltd BMC |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1471-2229 1471-2229 |
| DOI | 10.1186/s12870-025-06767-5 |
Cover
| Abstract | Background
Manganese (Mn) deficiency and toxicity are major constraints on crop production in soil. Plants have evolved cascade strategies and specific mechanisms to tolerate these stresses. Understanding the molecular mechanisms of tolerance to Mn stress is crucial for improving the efficiency of conferring Mn tolerance and phytoremediation, which is intriguing for evolutionary research on plant adaptation to abiotic stresses. In this study, the responses of mulberry to varied concentration levels of Mn (MnSO
4
), ranging from deficiency (0 mM and 0.03 mM), sufficiency (0.15 mM), and toxicity regimes (1.5 mM and 3 mM) were compared by elucidating the physiological, transcriptome profiling, and functional characterization of the
MaCAX3
gene in mulberry leaves.
Results
The results show that Mn-induced deficiency and toxicity not only trigger an increase in oxidation and antioxidant parameters, including hydrogen peroxide (H
2
O
2
), lipid peroxidase (LPO), polyphenol oxidase (PPO), and reactive oxygen species (ROS) but also concomitantly improved the activities of total antioxidant capacity (TAC) and hydroxyl radical (•OH) scavenging levels in mulberry. Results of the cell wall structural components show that cellulose, hemicellulose, and lignin contents were significantly higher, except for pectin, in the control (CK) compared to the deficiency and toxicity. Functional validation of the
MaCAX3
gene via gene silencing revealed that the heterologous expression of the
MaCAX3
gene increased the transport of Mn in yeast, thus inhibiting the toxic effect of Mn relative to the silenced
Macax3
-VIGS. Additionally, transcriptome analysis identified a total of 811 differentially expressed genes (DEGs), with 189 and 622 being up- and downregulated, respectively. These DEGs were significantly involved in Mn transport, detoxification, oxidation, antioxidant defense, and cell wall and protein processing, which conferred tolerance to Mn in mulberry plants.
Conclusion
The study sheds substantial light on key molecular mechanisms and the functional characterization and validation of crucial Mn tolerance genes in mulberry leaves. |
|---|---|
| AbstractList | BackgroundManganese (Mn) deficiency and toxicity are major constraints on crop production in soil. Plants have evolved cascade strategies and specific mechanisms to tolerate these stresses. Understanding the molecular mechanisms of tolerance to Mn stress is crucial for improving the efficiency of conferring Mn tolerance and phytoremediation, which is intriguing for evolutionary research on plant adaptation to abiotic stresses. In this study, the responses of mulberry to varied concentration levels of Mn (MnSO4), ranging from deficiency (0 mM and 0.03 mM), sufficiency (0.15 mM), and toxicity regimes (1.5 mM and 3 mM) were compared by elucidating the physiological, transcriptome profiling, and functional characterization of the MaCAX3 gene in mulberry leaves.ResultsThe results show that Mn-induced deficiency and toxicity not only trigger an increase in oxidation and antioxidant parameters, including hydrogen peroxide (H2O2), lipid peroxidase (LPO), polyphenol oxidase (PPO), and reactive oxygen species (ROS) but also concomitantly improved the activities of total antioxidant capacity (TAC) and hydroxyl radical (•OH) scavenging levels in mulberry. Results of the cell wall structural components show that cellulose, hemicellulose, and lignin contents were significantly higher, except for pectin, in the control (CK) compared to the deficiency and toxicity. Functional validation of the MaCAX3 gene via gene silencing revealed that the heterologous expression of the MaCAX3 gene increased the transport of Mn in yeast, thus inhibiting the toxic effect of Mn relative to the silenced Macax3-VIGS. Additionally, transcriptome analysis identified a total of 811 differentially expressed genes (DEGs), with 189 and 622 being up- and downregulated, respectively. These DEGs were significantly involved in Mn transport, detoxification, oxidation, antioxidant defense, and cell wall and protein processing, which conferred tolerance to Mn in mulberry plants.ConclusionThe study sheds substantial light on key molecular mechanisms and the functional characterization and validation of crucial Mn tolerance genes in mulberry leaves. Manganese (Mn) deficiency and toxicity are major constraints on crop production in soil. Plants have evolved cascade strategies and specific mechanisms to tolerate these stresses. Understanding the molecular mechanisms of tolerance to Mn stress is crucial for improving the efficiency of conferring Mn tolerance and phytoremediation, which is intriguing for evolutionary research on plant adaptation to abiotic stresses. In this study, the responses of mulberry to varied concentration levels of Mn (MnSO.sub.4), ranging from deficiency (0 mM and 0.03 mM), sufficiency (0.15 mM), and toxicity regimes (1.5 mM and 3 mM) were compared by elucidating the physiological, transcriptome profiling, and functional characterization of the MaCAX3 gene in mulberry leaves. The results show that Mn-induced deficiency and toxicity not only trigger an increase in oxidation and antioxidant parameters, including hydrogen peroxide (H.sub.2O.sub.2), lipid peroxidase (LPO), polyphenol oxidase (PPO), and reactive oxygen species (ROS) but also concomitantly improved the activities of total antioxidant capacity (TAC) and hydroxyl radical (*OH) scavenging levels in mulberry. Results of the cell wall structural components show that cellulose, hemicellulose, and lignin contents were significantly higher, except for pectin, in the control (CK) compared to the deficiency and toxicity. Functional validation of the MaCAX3 gene via gene silencing revealed that the heterologous expression of the MaCAX3 gene increased the transport of Mn in yeast, thus inhibiting the toxic effect of Mn relative to the silenced Macax3-VIGS. Additionally, transcriptome analysis identified a total of 811 differentially expressed genes (DEGs), with 189 and 622 being up- and downregulated, respectively. These DEGs were significantly involved in Mn transport, detoxification, oxidation, antioxidant defense, and cell wall and protein processing, which conferred tolerance to Mn in mulberry plants. The study sheds substantial light on key molecular mechanisms and the functional characterization and validation of crucial Mn tolerance genes in mulberry leaves. Background Manganese (Mn) deficiency and toxicity are major constraints on crop production in soil. Plants have evolved cascade strategies and specific mechanisms to tolerate these stresses. Understanding the molecular mechanisms of tolerance to Mn stress is crucial for improving the efficiency of conferring Mn tolerance and phytoremediation, which is intriguing for evolutionary research on plant adaptation to abiotic stresses. In this study, the responses of mulberry to varied concentration levels of Mn (MnSO.sub.4), ranging from deficiency (0 mM and 0.03 mM), sufficiency (0.15 mM), and toxicity regimes (1.5 mM and 3 mM) were compared by elucidating the physiological, transcriptome profiling, and functional characterization of the MaCAX3 gene in mulberry leaves. Results The results show that Mn-induced deficiency and toxicity not only trigger an increase in oxidation and antioxidant parameters, including hydrogen peroxide (H.sub.2O.sub.2), lipid peroxidase (LPO), polyphenol oxidase (PPO), and reactive oxygen species (ROS) but also concomitantly improved the activities of total antioxidant capacity (TAC) and hydroxyl radical (*OH) scavenging levels in mulberry. Results of the cell wall structural components show that cellulose, hemicellulose, and lignin contents were significantly higher, except for pectin, in the control (CK) compared to the deficiency and toxicity. Functional validation of the MaCAX3 gene via gene silencing revealed that the heterologous expression of the MaCAX3 gene increased the transport of Mn in yeast, thus inhibiting the toxic effect of Mn relative to the silenced Macax3-VIGS. Additionally, transcriptome analysis identified a total of 811 differentially expressed genes (DEGs), with 189 and 622 being up- and downregulated, respectively. These DEGs were significantly involved in Mn transport, detoxification, oxidation, antioxidant defense, and cell wall and protein processing, which conferred tolerance to Mn in mulberry plants. Conclusion The study sheds substantial light on key molecular mechanisms and the functional characterization and validation of crucial Mn tolerance genes in mulberry leaves. Keywords: Morus alba, Manganese, Transcriptome, Gene silencing, Cell wall polysaccharides, MaCAX3 gene, Reactive oxygen species Abstract Background Manganese (Mn) deficiency and toxicity are major constraints on crop production in soil. Plants have evolved cascade strategies and specific mechanisms to tolerate these stresses. Understanding the molecular mechanisms of tolerance to Mn stress is crucial for improving the efficiency of conferring Mn tolerance and phytoremediation, which is intriguing for evolutionary research on plant adaptation to abiotic stresses. In this study, the responses of mulberry to varied concentration levels of Mn (MnSO4), ranging from deficiency (0 mM and 0.03 mM), sufficiency (0.15 mM), and toxicity regimes (1.5 mM and 3 mM) were compared by elucidating the physiological, transcriptome profiling, and functional characterization of the MaCAX3 gene in mulberry leaves. Results The results show that Mn-induced deficiency and toxicity not only trigger an increase in oxidation and antioxidant parameters, including hydrogen peroxide (H2O2), lipid peroxidase (LPO), polyphenol oxidase (PPO), and reactive oxygen species (ROS) but also concomitantly improved the activities of total antioxidant capacity (TAC) and hydroxyl radical (•OH) scavenging levels in mulberry. Results of the cell wall structural components show that cellulose, hemicellulose, and lignin contents were significantly higher, except for pectin, in the control (CK) compared to the deficiency and toxicity. Functional validation of the MaCAX3 gene via gene silencing revealed that the heterologous expression of the MaCAX3 gene increased the transport of Mn in yeast, thus inhibiting the toxic effect of Mn relative to the silenced Macax3-VIGS. Additionally, transcriptome analysis identified a total of 811 differentially expressed genes (DEGs), with 189 and 622 being up- and downregulated, respectively. These DEGs were significantly involved in Mn transport, detoxification, oxidation, antioxidant defense, and cell wall and protein processing, which conferred tolerance to Mn in mulberry plants. Conclusion The study sheds substantial light on key molecular mechanisms and the functional characterization and validation of crucial Mn tolerance genes in mulberry leaves. Background Manganese (Mn) deficiency and toxicity are major constraints on crop production in soil. Plants have evolved cascade strategies and specific mechanisms to tolerate these stresses. Understanding the molecular mechanisms of tolerance to Mn stress is crucial for improving the efficiency of conferring Mn tolerance and phytoremediation, which is intriguing for evolutionary research on plant adaptation to abiotic stresses. In this study, the responses of mulberry to varied concentration levels of Mn (MnSO 4 ), ranging from deficiency (0 mM and 0.03 mM), sufficiency (0.15 mM), and toxicity regimes (1.5 mM and 3 mM) were compared by elucidating the physiological, transcriptome profiling, and functional characterization of the MaCAX3 gene in mulberry leaves. Results The results show that Mn-induced deficiency and toxicity not only trigger an increase in oxidation and antioxidant parameters, including hydrogen peroxide (H 2 O 2 ), lipid peroxidase (LPO), polyphenol oxidase (PPO), and reactive oxygen species (ROS) but also concomitantly improved the activities of total antioxidant capacity (TAC) and hydroxyl radical (•OH) scavenging levels in mulberry. Results of the cell wall structural components show that cellulose, hemicellulose, and lignin contents were significantly higher, except for pectin, in the control (CK) compared to the deficiency and toxicity. Functional validation of the MaCAX3 gene via gene silencing revealed that the heterologous expression of the MaCAX3 gene increased the transport of Mn in yeast, thus inhibiting the toxic effect of Mn relative to the silenced Macax3 -VIGS. Additionally, transcriptome analysis identified a total of 811 differentially expressed genes (DEGs), with 189 and 622 being up- and downregulated, respectively. These DEGs were significantly involved in Mn transport, detoxification, oxidation, antioxidant defense, and cell wall and protein processing, which conferred tolerance to Mn in mulberry plants. Conclusion The study sheds substantial light on key molecular mechanisms and the functional characterization and validation of crucial Mn tolerance genes in mulberry leaves. Manganese (Mn) deficiency and toxicity are major constraints on crop production in soil. Plants have evolved cascade strategies and specific mechanisms to tolerate these stresses. Understanding the molecular mechanisms of tolerance to Mn stress is crucial for improving the efficiency of conferring Mn tolerance and phytoremediation, which is intriguing for evolutionary research on plant adaptation to abiotic stresses. In this study, the responses of mulberry to varied concentration levels of Mn (MnSO4), ranging from deficiency (0 mM and 0.03 mM), sufficiency (0.15 mM), and toxicity regimes (1.5 mM and 3 mM) were compared by elucidating the physiological, transcriptome profiling, and functional characterization of the MaCAX3 gene in mulberry leaves.BACKGROUNDManganese (Mn) deficiency and toxicity are major constraints on crop production in soil. Plants have evolved cascade strategies and specific mechanisms to tolerate these stresses. Understanding the molecular mechanisms of tolerance to Mn stress is crucial for improving the efficiency of conferring Mn tolerance and phytoremediation, which is intriguing for evolutionary research on plant adaptation to abiotic stresses. In this study, the responses of mulberry to varied concentration levels of Mn (MnSO4), ranging from deficiency (0 mM and 0.03 mM), sufficiency (0.15 mM), and toxicity regimes (1.5 mM and 3 mM) were compared by elucidating the physiological, transcriptome profiling, and functional characterization of the MaCAX3 gene in mulberry leaves.The results show that Mn-induced deficiency and toxicity not only trigger an increase in oxidation and antioxidant parameters, including hydrogen peroxide (H2O2), lipid peroxidase (LPO), polyphenol oxidase (PPO), and reactive oxygen species (ROS) but also concomitantly improved the activities of total antioxidant capacity (TAC) and hydroxyl radical (•OH) scavenging levels in mulberry. Results of the cell wall structural components show that cellulose, hemicellulose, and lignin contents were significantly higher, except for pectin, in the control (CK) compared to the deficiency and toxicity. Functional validation of the MaCAX3 gene via gene silencing revealed that the heterologous expression of the MaCAX3 gene increased the transport of Mn in yeast, thus inhibiting the toxic effect of Mn relative to the silenced Macax3-VIGS. Additionally, transcriptome analysis identified a total of 811 differentially expressed genes (DEGs), with 189 and 622 being up- and downregulated, respectively. These DEGs were significantly involved in Mn transport, detoxification, oxidation, antioxidant defense, and cell wall and protein processing, which conferred tolerance to Mn in mulberry plants.RESULTSThe results show that Mn-induced deficiency and toxicity not only trigger an increase in oxidation and antioxidant parameters, including hydrogen peroxide (H2O2), lipid peroxidase (LPO), polyphenol oxidase (PPO), and reactive oxygen species (ROS) but also concomitantly improved the activities of total antioxidant capacity (TAC) and hydroxyl radical (•OH) scavenging levels in mulberry. Results of the cell wall structural components show that cellulose, hemicellulose, and lignin contents were significantly higher, except for pectin, in the control (CK) compared to the deficiency and toxicity. Functional validation of the MaCAX3 gene via gene silencing revealed that the heterologous expression of the MaCAX3 gene increased the transport of Mn in yeast, thus inhibiting the toxic effect of Mn relative to the silenced Macax3-VIGS. Additionally, transcriptome analysis identified a total of 811 differentially expressed genes (DEGs), with 189 and 622 being up- and downregulated, respectively. These DEGs were significantly involved in Mn transport, detoxification, oxidation, antioxidant defense, and cell wall and protein processing, which conferred tolerance to Mn in mulberry plants.The study sheds substantial light on key molecular mechanisms and the functional characterization and validation of crucial Mn tolerance genes in mulberry leaves.CONCLUSIONThe study sheds substantial light on key molecular mechanisms and the functional characterization and validation of crucial Mn tolerance genes in mulberry leaves. Manganese (Mn) deficiency and toxicity are major constraints on crop production in soil. Plants have evolved cascade strategies and specific mechanisms to tolerate these stresses. Understanding the molecular mechanisms of tolerance to Mn stress is crucial for improving the efficiency of conferring Mn tolerance and phytoremediation, which is intriguing for evolutionary research on plant adaptation to abiotic stresses. In this study, the responses of mulberry to varied concentration levels of Mn (MnSO ), ranging from deficiency (0 mM and 0.03 mM), sufficiency (0.15 mM), and toxicity regimes (1.5 mM and 3 mM) were compared by elucidating the physiological, transcriptome profiling, and functional characterization of the MaCAX3 gene in mulberry leaves. The results show that Mn-induced deficiency and toxicity not only trigger an increase in oxidation and antioxidant parameters, including hydrogen peroxide (H O ), lipid peroxidase (LPO), polyphenol oxidase (PPO), and reactive oxygen species (ROS) but also concomitantly improved the activities of total antioxidant capacity (TAC) and hydroxyl radical (•OH) scavenging levels in mulberry. Results of the cell wall structural components show that cellulose, hemicellulose, and lignin contents were significantly higher, except for pectin, in the control (CK) compared to the deficiency and toxicity. Functional validation of the MaCAX3 gene via gene silencing revealed that the heterologous expression of the MaCAX3 gene increased the transport of Mn in yeast, thus inhibiting the toxic effect of Mn relative to the silenced Macax3-VIGS. Additionally, transcriptome analysis identified a total of 811 differentially expressed genes (DEGs), with 189 and 622 being up- and downregulated, respectively. These DEGs were significantly involved in Mn transport, detoxification, oxidation, antioxidant defense, and cell wall and protein processing, which conferred tolerance to Mn in mulberry plants. The study sheds substantial light on key molecular mechanisms and the functional characterization and validation of crucial Mn tolerance genes in mulberry leaves. |
| ArticleNumber | 971 |
| Audience | Academic |
| Author | Qiu, Changyu Ackah, Michael Wang, Zhenjiang Amoako, Frank Kwarteng Zhao, Weiguo Lin, Qiang Zhao, Mengdi Li, Jianbin Zhu, Meina Asare, Aaron Tettey Shen, Manman |
| Author_xml | – sequence: 1 givenname: Jianbin surname: Li fullname: Li, Jianbin organization: Jiangsu Key Laboratory of Sericulture Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture and Rural Affairs, The Sericultural Research Institute, Chinese Academy of Agricultural Sciences – sequence: 2 givenname: Michael orcidid: 0000-0001-9019-8986 surname: Ackah fullname: Ackah, Michael organization: Jiangsu Key Laboratory of Sericulture Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture and Rural Affairs, The Sericultural Research Institute, Chinese Academy of Agricultural Sciences, Department of Molecular Biology and Biotechnology, School of Biological Sciences, College of Agriculture and Natural Sciences, University of Cape Coast, PMB Ghana – sequence: 3 givenname: Frank Kwarteng surname: Amoako fullname: Amoako, Frank Kwarteng organization: Institute of Plant Nutrition and Soil Science, Kiel University, Department of Molecular Biology and Biotechnology, School of Biological Sciences, College of Agriculture and Natural Sciences, University of Cape Coast, PMB Ghana – sequence: 4 givenname: Aaron Tettey surname: Asare fullname: Asare, Aaron Tettey organization: Department of Molecular Biology and Biotechnology, School of Biological Sciences, College of Agriculture and Natural Sciences, University of Cape Coast, PMB Ghana – sequence: 5 givenname: Manman surname: Shen fullname: Shen, Manman organization: Jiangsu Key Laboratory of Sericulture Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture and Rural Affairs, The Sericultural Research Institute, Chinese Academy of Agricultural Sciences – sequence: 6 givenname: Zhenjiang surname: Wang fullname: Wang, Zhenjiang organization: Sericulture & Agri-Food Research Institute, Guangdong Academy of Agricultural Sciences – sequence: 7 givenname: Qiang surname: Lin fullname: Lin, Qiang organization: Sericulture Technology Promotion Station, Guangxi Zhuang Autonomous Region – sequence: 8 givenname: Changyu surname: Qiu fullname: Qiu, Changyu organization: Sericulture Technology Promotion Station, Guangxi Zhuang Autonomous Region – sequence: 9 givenname: Meina surname: Zhu fullname: Zhu, Meina email: zhumeina1993@163.com organization: Jiangsu Key Laboratory of Sericulture Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture and Rural Affairs, The Sericultural Research Institute, Chinese Academy of Agricultural Sciences – sequence: 10 givenname: Mengdi surname: Zhao fullname: Zhao, Mengdi email: mdzhao@usts.edu.cn organization: Department of Materials Science and Engineering, Suzhou University of Science and Technology – sequence: 11 givenname: Weiguo surname: Zhao fullname: Zhao, Weiguo email: wgzsri@126.com organization: Jiangsu Key Laboratory of Sericulture Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture and Rural Affairs, The Sericultural Research Institute, Chinese Academy of Agricultural Sciences |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/40730943$$D View this record in MEDLINE/PubMed |
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| Keywords | Gene silencing Reactive oxygen species Cell wall polysaccharides gene Transcriptome Manganese MaCAX3 gene Morus alba |
| Language | English |
| License | 2025. The Author(s). Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. |
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Manganese (Mn) deficiency and toxicity are major constraints on crop production in soil. Plants have evolved cascade strategies and specific... Manganese (Mn) deficiency and toxicity are major constraints on crop production in soil. Plants have evolved cascade strategies and specific mechanisms to... Background Manganese (Mn) deficiency and toxicity are major constraints on crop production in soil. Plants have evolved cascade strategies and specific... BackgroundManganese (Mn) deficiency and toxicity are major constraints on crop production in soil. Plants have evolved cascade strategies and specific... Abstract Background Manganese (Mn) deficiency and toxicity are major constraints on crop production in soil. Plants have evolved cascade strategies and... |
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| SubjectTerms | Agricultural research Agriculture Antioxidants Antioxidants - metabolism Biomedical and Life Sciences Biosynthesis Cell wall polysaccharides Cell walls Cellulose Crop production Detoxification Enzymes Flavonoids Gene expression Gene Expression Profiling Gene Expression Regulation, Plant Gene silencing Genes Genes, Plant Genetic aspects Hardiness Hemicellulose Hydrogen peroxide Hydroxyl radicals Leaves Life Sciences Lignin Lipids MaCAX3 gene Manganese Manganese - metabolism Manganese - toxicity Metabolism Metabolites Methods Molecular modelling Morus - drug effects Morus - genetics Morus - metabolism Morus - physiology Morus alba Mulberry Oxidation Pectin Peroxidase Photosynthesis Physiological aspects Physiology Phytoremediation Plant Leaves - genetics Plant Leaves - metabolism Plant Proteins - genetics Plant Proteins - metabolism Plant Sciences Plants Polyphenol oxidase Proteins Reactive oxygen species RNA sequencing Scavenging Stress response Stress, Physiological - genetics Stresses Toxicity Transcriptome Transcriptomes Tree Biology |
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| Title | Transcriptome-based analysis reveals key molecular mechanisms and functional characterization of MaCAX3 gene involved in manganese stress responses in mulberry plants |
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