Chinese Bulletin of Botany >

2026 , Vol. 61 >Issue 3: 416 - 427

DOI: https://doi.org/10.11983/CBB25053

The Mechanism of Manganese Accumulation Mediated by SpMTP10 Isolated from Sedum plumbizincicola

  • Siying Chen 1, 2 ,
  • Jinglin Wang 1 ,
  • Yingyi Li 1 ,
  • Xiangxin Lu 1 ,
  • Peihong Zhang 1 ,
  • Qinghong Qiu 1 ,
  • Yan Gao 1, 2 ,
  • Tianyu Gu 1, 2 ,
  • Jiashi Peng , 1, 2, *
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  • 1 School of Life and Health Sciences, Hunan University of Science and Technology , Xiangtan 411201, China
  • 2Hunan Key Laboratory of Economic Crops Genetic Improvement and Integrated Utilization/Key Laboratory of Ecological Remediation and Safe Utilization of Heavy Metal—Polluted Soils, Xiangtan 411201, China

Received date: 2025-04-02

  Accepted date: 2025-07-29

  Online published: 2025-09-03

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Abstract

INTRODUCTION: Manganese (Mn) is an essential micronutrient for plant growth and primarily acts as an enzyme cofactor and participates in the redox processes. However, excessive absorption of Mn by plants can also induce toxicity damage. Therefore, plants need to tightly regulate the uptake, homeostasis, and distribution of Mn to cope with stresses caused by its deficiency or excess. In these processes, cation diffusion facilitator (CDF) family transporters, which in plants are also known as metal tolerance proteins (MTPs), have been shown to be crucial for Mn homeostasis. Therefore, identifying MTP family genes and elucidating their underlying mechanisms for Mn accumulation would provide not only novel insights into basic scientific issues of plant Mn accumulation but also gene resources for crop improvement and Mn pollution bioremediation. RATIONALE: Sedum plumbizincicola is a recently discovered Cd/Zn hyperaccumulator that grows in mining areas. The soil in its natural habitat contains more than 10 000 mg·kg–1 Mn, suggesting that S. plumbizincicola may have efficient Mn transport and detoxification capabilities. Based on the transcriptome sequencing results of S. plumbizincicola obtained previously, a member of the MTP family gene named SpMTP10 was cloned and its role in mediating Mn accumulation was investigated in this study. RESULTS: Phylogenetic analysis with orthologs from Arabidopsis and rice revealed that SpMTP10 belongs to the Mn-CDF subfamily and is most closely related to AtMTP10, AtMTP9 and OsMTP9, with the highest sequence identity of 72% to AtMTP10. SpMTP10 is mainly expressed in the roots of S. plumbizincicola and its expression level is not affected by Mn treatment. Expression of SpMTP10 in yeast can greatly enhance the tolerance of transformants to excessive Mn stress and increase Mn accumulation in transformants. However, under conditions of excessive cadmium (Cd), zinc (Zn), copper (Cu), and iron (Fe) stress, the yeast transformants exhibited no significant changes in tolerance. Subsequent subcellular localization analysis revealed that SpMTP10 was localized to the endoplasmic reticulum (ER) membrane. Compared with wild-type plants, transgenic Arabidopsis overexpressing SpMTP10 demonstrated reduced Mn accumulation in roots but increased Mn accumulation in shoots, rendering the plants more sensitive to excessive Mn stress. CONCLUSION: In conclusion, SpMTP10 likely enhances yeast tolerance to excessive Mn toxicity by promoting Mn sequestration in the ER. In plants, Mn transport mediated by SpMTP10 into the ER may facilitate intercellular migration of Mn in the ER lumen via plasmodesmata, thereby promoting Mn movement toward vascular tissues in roots and subsequent long-distance transport to shoots.

Key words： manganese; endoplasmic reticulum; metal tolerance proteins; Sedum plumbizincicola

Cite this article

Siying Chen , Jinglin Wang , Yingyi Li , Xiangxin Lu , Peihong Zhang , Qinghong Qiu , Yan Gao , Tianyu Gu , Jiashi Peng . The Mechanism of Manganese Accumulation Mediated by SpMTP10 Isolated from Sedum plumbizincicola[J]. Chinese Bulletin of Botany, 2026 , 61(3) : 416 -427 . DOI: 10.11983/CBB25053

References

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AlejandroS, HöllerS, MeierB, PeiterE (2020). Manganese in plants: from acquisition to subcellular allocation. Front Plant Sci 11, 300.

BartonDA, ColeL, CollingsDA, LiuDYT, SmithPMC, DayDA, OverallRL (2011). Cell—to—cell transport via the lumen of the endoplasmic reticulum. Plant J 66, 806-817.

ChenSY, GuTY, QiZA, YanJ, FangZJ, LuYT, LiH, GongJM (2021). Two NPF transporters mediate iron long—distance transport and homeostasis in Arabidopsis. Plant Commun 2, 100244.

ChenZH, FujiiY, YamajiN, MasudaS, TakemotoY, KamiyaT, YusuyinY, IwasakiK, KatoSI, MaeshimaM, MaJF, UenoD (2013). Mn tolerance in rice is mediated by MTP8.1, a member of the cation diffusion facilitator family. J Exp Bot 64, 4375-4387.

DelhaizeE, GruberBD, PittmanJK, WhiteRG, LeungH, MiaoYS, JiangLW, RyanPR, RichardsonAE (2007). A role for the AtMTP11 gene of Arabidopsis in manganese transport and tolerance. Plant J 51, 198-210.

ElbleR (1992). A simple and efficient procedure for transformation of yeasts. Biotechniques 13, 18-20.

ErogluS, MeierB, VonWirén N, PeiterE (2016). The vacuolar manganese transporter MTP8 determines tolerance to iron deficiency—induced chlorosis in Arabidopsis. Plant Physiol 170, 1030-1045.

Fang X, Tian DL, Xie RX (2006). Soil physical and chemical properties of the wasteland in Xiangtan manganese mine. Acta Ecol Sin 26, 1494-1501. (in Chinese)

方晰, 田大伦, 谢荣秀 (2006). 湘潭锰矿矿渣废弃地植被修复前的土壤诊断. 生态学报 26, 1494-1501.

GeHM, ShaoQL, ChenJL, ChenJH, LiXQ, TanY, LanWZ, YangL, WangY (2022). A metal tolerance protein, MTP10, is required for the calcium and magnesium homeostasis in Arabidopsis. Plant Signal Behav 17, 2025322.

GuDF, ZhouXL, YinXH, WuMY, ChenWZ, XuED, LiuYY, GongCY, ZhangW, ChenX (2022). Metal tolerance protein family members are involved in Mn homeostasis through internal compartmentation and exocytosis in Brassica napus. Environ Exp Bot 195, 104785.

GuTY, GongYQ, ZhangGB, PengJS (2020). Development and application of the meta—ionomic assay to identify heavy metal pollution. Plant Physiol J 56, 583-589. (in Chinese)

顾天宇, 龚韵秋, 张国斌, 彭佳师 (2020). 植被宏离子组分析方法的建立及重金属污染的监测应用. 植物生理学报 56, 583-589.

GustinJL, ZanisMJ, SaltDE (2011). Structure and evolution of the plant cation diffusion facilitator family of ion transporters. BMC Evol Biol 11, 76.

Hu HL, Gu TY, Chen SY, Wang Y, Peng JS (2024). Isolation and functional verification of genes mediating mineral element stress tolerance in lotus. Sci Agric Sin 57, 980-988. (in Chinese)

胡衡亮, 顾天宇, 陈思颖, 王垚, 彭佳师 (2024). 莲中介导矿质元素胁迫耐受性基因的筛选与功能验证. 中国农业科学 57, 980-988.

HuHL, HeYT, GaoY, ChenSY, GuTY, PengJS (2025). NnMTP10 from Nelumbo nucifera acts as a transporter mediating manganese and iron efflux. Plant Mol Biol 115, 26.

JaiswalS, KumariA, KumarK, LaxmiV, KaurS, KumarA, VermaH, ShimrayP, TouthangL, TalukdarM, MishraVK, SinghBK (2024). Deciphering genetic mechanisms of Al toxicity tolerance through meta—QTL analysis in rice (Oryza sativa L.). Environ Exp Bot 228, 106030.

JuCF, ZhangZQ, DengJP, MiaoCC, WangZQ, WallradL, JavedL, FuDL, ZhangT, KudlaJ, GongZZ, WangC (2022). Ca 2+—dependent successive phosphorylation of vacuolar transporter MTP8 by CBL2/3—CIPK3/9/26 and CPK5 is critical for manganese homeostasis in Arabidopsis . Mol Plant 15, 419-437.

KrämerU (2010). Metal hyperaccumulation in plants. Annu Rev Plant Biol 61, 517-534.

LiJF, DongRS, JiaYD, HuangJ, ZouXY, AnN, SongJL, ChenZJ (2021). Characterization of metal tolerance proteins and functional analysis of GmMTP8.1 involved in manganese tolerance in soybean. Front Plant Sci 12, 683813.

LiJF, JiaYD, DongRS, HuangR, LiuPD, LiXY, WangZY, LiuGD, ChenZJ (2019). Advances in the mechanisms of plant tolerance to manganese toxicity. Int J Mol Sci 20, 5096.

LiuH, ZhaoHX, WuLH, LiuAN, ZhaoFJ, XuWZ (2017). Heavy metal ATPase 3 (HMA3) confers cadmium hypertolerance on the cadmium/zinc hyperaccumulator Sedum plumbizincicola. New Phytol 215, 687-698.

LiuP, SunL, ZhangY, TanY, ZhuY, PengC, WangJ, YanH, MaoD, LiangG, LiangG, LiX, LiangY, WangF, HeZ, TangW, HuangD, ChenC (2024). The metal tolerance protein OsMTP11 facilitates cadmium sequestration in the vacuoles of leaf vascular cells for restricting its translocation into rice grains. Mol Plant 17, 1733-1752.

LuZC, QiuWM, JinKM, YuM, HanXJ, HeXY, WuLH, WuC, ZhuoRY (2022). Identification and analysis of bZIP family genes in Sedum plumbizincicola and their potential roles in response to cadmium stress. Front Plant Sci 13, 859386.

MaG, LiJY, LiJJ, LiY, GuDF, ChenC, CuiJ, ChenX, ZhangW (2018). OsMTP11, a trans—Golgi network localized transporter, is involved in manganese tolerance in rice. Plant Sci 274, 59-69.

MillaleoR, Reyes—DiazM, IvanovAG, MoraML, AlberdiM (2010). Manganese as essential and toxic element for plants: transport, accumulation and resistance mechanisms. J Soil Sci Plant Nutr 10, 470-481.

MontaniniB, BlaudezD, JeandrozS, SandersD, ChalotM (2007). Phylogenetic and functional analysis of the cation diffusion facilitator (CDF) family: improved signature and prediction of substrate specificity. BMC Genomics 8, 107.

NelsonBK, CaiX, NebenführA (2007). A multicolored set of in vivo organelle markers for co—localization studies in Arabidopsis and other plants. Plant J 51, 1126-1136.

PedasP, StokholmMS, HegelundJN, LadegårdAH, SchjoerringJK, HustedS (2014). Golgi localized barley MTP8 proteins facilitate Mn transport. PLoS One 9, e113759.

PeiterE, MontaniniB, GobertA, PedasP, HustedS, MaathuisFJM, BlaudezD, ChalotM, SandersD (2007). A secretory pathway—localized cation diffusion facilitator confers plant manganese tolerance. Proc Natl Acad Sci USA 104, 8532-8537.

PengJS, DingG, MengS, YiHY, GongJM (2017a). Enhanced metal tolerance correlates with heterotypic variation in SpMTL, a metallothionein—like protein from the hyperaccumulator Sedum plumbizincicola. Plant Cell Environ 40, 1368-1378.

Peng JS, Ding G, Yi HY, Gong JM (2014). Cloning and functional analysis of phytochelatin synthase gene from Sedum plumbizincicola. Plant Physiol J 50, 625-633. (in Chinese)

彭佳师, 丁戈, 易红英, 龚继明 (2014). 伴矿景天植物螯合肽合酶基因的克隆及功能分析. 植物生理学报 50, 625-633.

PengJS, WangYJ, DingG, MaHL, ZhangYJ, GongJM (2017b). A pivotal role of cell wall in cadmium accumulation in the Crassulaceae hyperaccumulator Sedum plumbizincicola. Mol Plant 10, 771-774.

PengJS, WangYT, WangMQ, LuLL, WangP, LiZ, LiS, ChenSY, MengS, GuTY, XuWZ, ChaoZF, HuangYQ, JinCW, ChaoDY, ChenCY, WuLH, TengY, ZhaoFJ, GongJM (2024). Research and regulation of cadmium uptake, transport and accumulation in plants. Plant Physiol J 60, 185-210. (in Chinese)

彭佳师, 王娅婷, 王梦琦, 卢玲丽, 汪鹏, 李柱, 李赛, 陈思颖, 孟栓, 顾天宇, 徐文忠, 晁振飞, 黄煜琪, 金崇伟, 晁代印, 陈彩艳, 吴龙华, 滕应, 赵方杰, 龚继明 (2024). 植物重金属镉积累调控机制及其应用研究进展. 植物生理学报 60, 185-210.

Peng JS, Yi HY, Gong JM (2020). Isolation and characterization of cadmium tolerant gene SpMT2 in the hyperaccumulator Sedum plumbizincicola. Chin J Biotech 36, 541-548. (in Chinese)

彭佳师, 易红英, 龚继明 (2020). 超积累植物伴矿景天镉耐受基因 SpMT2 的分离及功能鉴定 . 生物工程学报 36, 541-548.

SinclairSA, SengerT, TalkeIN, CobbettCS, HaydonMJ, KrämerU (2018). Systemic upregulation of MTP2— and HMA2—mediated Zn partitioning to the shoot supplements local Zn deficiency responses. Plant Cell 30, 2463-2479.

TakemotoY, TsunemitsuY, Fujii—KashinoM, Mitani—UenoN, YamajiN, MaJF, KatoSI, IwasakiK, UenoD (2017). The tonoplast—localized transporter MTP8.2 contributes to manganese detoxification in the shoots and roots of Oryza sativa L. Plant Cell Physiol 58, 1573-1582.

TsunemitsuY, YamajiN, MaJF, KatoSI, IwasakiK, UenoD (2018). Rice reduces Mn uptake in response to Mn stress. Plant Signal Behav 13, e1422466.

UenoD, SasakiA, YamajiN, MiyajiT, FujiiY, TakemotoY, MoriyamaS, CheJ, MoriyamaY, IwasakiK, MaJF (2015). A polarly localized transporter for efficient manganese uptake in rice. Nat Plants 1, 15170.

Wang Y, Hu B, Deng XQ, Jiang JJ, Du LF, Peng JS (2022). SpPCR3 gene from Sedum plumbizincicola confers cadmium tolerance in yeast. Plant Physiol J 58, 1353-1358. (in Chinese)

王垚, 胡博, 邓小秋, 蒋佳佳, 杜兰芳, 彭佳师 (2022). 伴矿景天 SpPCR3 基因提高酵母对镉的抗性 . 植物生理学报 58, 1353-1358.

ZhangM, LiuBX (2017). Identification of a rice metal tolerance protein OsMTP11 as a manganese transporter. PLoS One 12, e0174987.

ZhangPH, ZhangSZ, ZhangZY, LiMY, LiuYJ, ZhangXJ, BaiNN, MaM, PengJS (2022). SpHIPP45 gene from Sedum plumbizincicola specifically mediates cadmium tolerance. Plant Physiol J 58, 1346-1352. (in Chinese)

张培红, 张仕泽, 张治远, 李明悦, 刘奕君, 张雪洁, 白宁宁, 马敏, 彭佳师 (2022). 伴矿景天SpHIPP45基因特异介导镉耐受性. 植物生理学报 58, 1346-1352.

ZhangXJ, ZhangZY, ZhangSZ, BaiNN, LiuM, PengJS (2023). Isolation and functional characterization of phytochelatin synthase gene BnPCS1a in Brassica napus. Plant Physiol J 59, 861-868. (in Chinese)

张雪洁, 张治远, 张仕泽, 白宁宁, 刘敏, 彭佳师 (2023). 甘蓝型油菜植物螯合肽合酶基因 BnPCS1a 的分离与功能验证 . 植物生理学报 59, 861-868.

Zhang YX, Li LF, Chai TY, Lin D, Zhang HM (2010). Mechanisms of manganese toxicity and manganese tolerance in plants. Chin Bull Bot 45, 506-520. (in Chinese with English abstract)

张玉秀, 李林峰, 柴团耀, 林单, 张红梅 (2010). 锰对植物毒害及植物耐锰机理研究进展. 植物学报 45, 506-520.

ZhaoHX, WangLS, ZhaoFJ, WuLH, LiuAN, XuWZ (2019). SpHMA1 is a chloroplast cadmium exporter protecting photochemical reactions in the Cd hyperaccumulator Sedum plumbizincicola. Plant Cell Environ 42, 1112-1124.

ZhaoYX, LiL, MaSF, HanR, HeYY, ZhuJ, LiM, ZhuangJ, WangYH, ZhaoZ, ChenX, LiuSJ, LiXH (2024). Mn—CDF family genes enhance the manganese tolerance of the tea plants (Camellia sinensis) under acidic condition. Plant Physiol Bioch 216, 109179.

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