Transcriptome-based analysis reveals key molecular mechanisms and functional characterization of MaCAX3 gene involved in manganese stress responses in mulberry plants

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 effici...

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Main Authors: Jianbin Li, Michael Ackah, Frank Kwarteng Amoako, Aaron Tettey Asare, Manman Shen, Zhenjiang Wang, Qiang Lin, Changyu Qiu, Meina Zhu, Mengdi Zhao, Weiguo Zhao
Format: Article
Language:English
Published: BMC 2025-07-01
Series:BMC Plant Biology
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Online Access:https://doi.org/10.1186/s12870-025-06767-5
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author Jianbin Li
Michael Ackah
Frank Kwarteng Amoako
Aaron Tettey Asare
Manman Shen
Zhenjiang Wang
Qiang Lin
Changyu Qiu
Meina Zhu
Mengdi Zhao
Weiguo Zhao
author_facet Jianbin Li
Michael Ackah
Frank Kwarteng Amoako
Aaron Tettey Asare
Manman Shen
Zhenjiang Wang
Qiang Lin
Changyu Qiu
Meina Zhu
Mengdi Zhao
Weiguo Zhao
author_sort Jianbin Li
collection DOAJ
description 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.
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spelling doaj-art-595eb6497e3644d796b52e669c623ebf2025-08-20T04:01:53ZengBMCBMC Plant Biology1471-22292025-07-0125112710.1186/s12870-025-06767-5Transcriptome-based analysis reveals key molecular mechanisms and functional characterization of MaCAX3 gene involved in manganese stress responses in mulberry plantsJianbin Li0Michael Ackah1Frank Kwarteng Amoako2Aaron Tettey Asare3Manman Shen4Zhenjiang Wang5Qiang Lin6Changyu Qiu7Meina Zhu8Mengdi Zhao9Weiguo Zhao10Jiangsu Key Laboratory of Sericulture Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and TechnologyJiangsu Key Laboratory of Sericulture Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and TechnologyInstitute of Plant Nutrition and Soil Science, Kiel UniversityDepartment of Molecular Biology and Biotechnology, School of Biological Sciences, College of Agriculture and Natural Sciences, University of Cape Coast, PMB GhanaJiangsu Key Laboratory of Sericulture Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and TechnologySericulture & Agri-Food Research Institute, Guangdong Academy of Agricultural SciencesSericulture Technology Promotion Station, Guangxi Zhuang Autonomous RegionSericulture Technology Promotion Station, Guangxi Zhuang Autonomous RegionJiangsu Key Laboratory of Sericulture Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and TechnologyDepartment of Materials Science and Engineering, Suzhou University of Science and TechnologyJiangsu Key Laboratory of Sericulture Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and TechnologyAbstract 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.https://doi.org/10.1186/s12870-025-06767-5Morus albaManganeseTranscriptomeGene silencingCell wall polysaccharidesMaCAX3 gene
spellingShingle Jianbin Li
Michael Ackah
Frank Kwarteng Amoako
Aaron Tettey Asare
Manman Shen
Zhenjiang Wang
Qiang Lin
Changyu Qiu
Meina Zhu
Mengdi Zhao
Weiguo Zhao
Transcriptome-based analysis reveals key molecular mechanisms and functional characterization of MaCAX3 gene involved in manganese stress responses in mulberry plants
BMC Plant Biology
Morus alba
Manganese
Transcriptome
Gene silencing
Cell wall polysaccharides
MaCAX3 gene
title Transcriptome-based analysis reveals key molecular mechanisms and functional characterization of MaCAX3 gene involved in manganese stress responses in mulberry plants
title_full Transcriptome-based analysis reveals key molecular mechanisms and functional characterization of MaCAX3 gene involved in manganese stress responses in mulberry plants
title_fullStr Transcriptome-based analysis reveals key molecular mechanisms and functional characterization of MaCAX3 gene involved in manganese stress responses in mulberry plants
title_full_unstemmed Transcriptome-based analysis reveals key molecular mechanisms and functional characterization of MaCAX3 gene involved in manganese stress responses in mulberry plants
title_short Transcriptome-based analysis reveals key molecular mechanisms and functional characterization of MaCAX3 gene involved in manganese stress responses in mulberry plants
title_sort transcriptome based analysis reveals key molecular mechanisms and functional characterization of macax3 gene involved in manganese stress responses in mulberry plants
topic Morus alba
Manganese
Transcriptome
Gene silencing
Cell wall polysaccharides
MaCAX3 gene
url https://doi.org/10.1186/s12870-025-06767-5
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