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Integration of manganese accumulation, subcellular distribution, chemical forms, and physiological responses to understand manganese tolerance in Macleaya cordata

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Abstract

Macleaya cordata (Willd.) R. Br. are proposed for the application in phytoremediation of heavy metal-contaminated soil. In this paper, the physiological response, subcellular distribution, chemical form, ultrastructure, and manganese (Mn) absorption characteristics of M. cordata under the stress of 0, 3, 6, 9, 12, and 15 mmol/L manganese concentration were studied by sand culture experiment. The results showed that M. cordata seedlings show high tolerance to Mn stress with a concentration of less than 6 mmol/L, while higher Mn concentration showed a significant toxic effect. A low concentration of Mn (≤ 6 mmol/L) can promote the synthesis of chlorophyll and soluble protein; furthermore, superoxide dismutase and peroxidase activities responded positively. The accumulation of Mn in the inactive metabolic part (cell wall and vacuole) of M. cordata leaves might be one of the main Mn detoxification mechanism. According to the ultrastructure of M. cordata, high-concentration Mn2+ (≥ 12 mmol/L) stress can cause M. cordata cells to be distorted and deformed, black precipitates appeared in the intercellular space, mitochondria decrease, chloroplasts shrink, hungry particles increased, and starch granules decrease. The uptake ability of different tissues for Mn is leaf > root > stem, and transport coefficient decreases with the increase of Mn concentration. Clearly, M. cordata has a certain tolerance to manganese, which has the ecological application potential in Mn-polluted areas.

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Funding

Funding was supported by the National Nature Science Foundation of China (52000183), Key Laboratory of Jiangxi Province for Persistent Pollutants Control and Resources Recycle Open Fund (ES202080088), Key Project of Scientific Research Project of Hunan Provincial Department of Education (20A523), Central South University of Forestry and Technology Introduced Talent Research Startup Fund (2020YJ010), Scientific Innovation Fund for Post-graduates of Central South University of Forestry and Technology (CX20202049), and Hunan Provincial Innovation Foundation For Postgraduate (CX20200731).

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Author notes

  1. Both Langjun He and Rongkui Su contributed equally to this study and should be considered co-first authors.

Authors and Affiliations

  1. School of Environmental Science and Engineering, Central South University of Forestry and Technology, Changsha, 410004, People’s Republic of China

    Langjun He, Rongkui Su, Yonghua Chen, Peng Zeng, Lu Du, Bin Cai, Aoshan Zhang & Honghong Zhu

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  1. Langjun He
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  2. Rongkui Su
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  7. Aoshan Zhang
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  8. Honghong Zhu
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Contributions

All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Langjun He, Rongkui Su, Yonghua Chen, Peng Zeng, Lu Du, Bin Cai, Aoshan Zhang, and Honghong Zhu. The first draft of the manuscript was written by Langjun He and Rongkui Su, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Yonghua Chen.

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He, L., Su, R., Chen, Y. et al. Integration of manganese accumulation, subcellular distribution, chemical forms, and physiological responses to understand manganese tolerance in Macleaya cordata. Environ Sci Pollut Res 29, 39017–39026 (2022). https://doi.org/10.1007/s11356-022-19562-8

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