研究论文

伴矿景天SpMTP10介导锰积累的机制

  • 陈思颖 ,
  • 王晶琳 ,
  • 张培红 ,
  • 邱庆红 ,
  • 高艳 ,
  • 顾天宇 ,
  • 彭佳师
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  • 1湖南科技大学生命科学与健康学院, 湘潭411201; 2经济作物遗传改良与综合利用湖南省重点实验室/重金属污染土壤生态修复与安全利用湖南省高校重点实验室, 湘潭 411201

收稿日期: 2025-04-02

  修回日期: 2025-06-10

  网络出版日期: 2025-09-03

基金资助

湖南省自然科学基金(No.2024JJ6213), 湖南省教育厅科学研究项目(No.23A0372, No.24A0352), 大学生创新创业训练计划项目(No.S202410534051)

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

  • CHEN Sai-Ying ,
  • YU Jing-Lin ,
  • ZHANG Pei-Hong ,
  • QIU Qiang-Hong ,
  • GAO Yan ,
  • GU Tian-Yu ,
  • PENG Jia-Shi
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  • 1School 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

  Revised date: 2025-06-10

  Online published: 2025-09-03

摘要

锰(Mn)是植物必需矿质元素, 其缺乏或过量都会影响植物的生长发育。鉴定植物中介导Mn积累的关键基因并揭示其作用机制, 对于相关作物遗传改良以及Mn污染生物修复都具有重要意义。本研究从超积累植物伴矿景天(Sedum plumbizincicola)中克隆了一个阳离子扩散促进子(CDF, cation diffusion facilitator)家族成员基因SpMTP10 (metal tolerance protein 10)。其在酵母中表达后能够极大地增强转化子对过量Mn胁迫的耐受性, 同时转化子中Mn的积累增加, 但是对镉(Cd)、锌(Cd)、铜(Cu)、铁(Fe)等其他金属元素过量胁迫的耐受性以及积累的作用不明显。亚细胞定位分析表明其定位于内质网膜。在拟南芥中异源表达SpMTP10使植物根部Mn积累减少, 地上部Mn积累增多, 且对过量Mn胁迫更加敏感。综上所述, SpMTP10可能通过促进Mn向内质网的区隔增加酵母对过量Mn毒害的耐受性; 而在植物中表达后, SpMTP10介导的Mn向内质网的转运则可能增加了内质网腔中的Mn通过胞间连丝进行在细胞间的迁移, 从而在促进根部的Mn向维管组织的装载并往地上部转运的过程中发挥作用。

本文引用格式

陈思颖 , 王晶琳 , 张培红 , 邱庆红 , 高艳 , 顾天宇 , 彭佳师 . 伴矿景天SpMTP10介导锰积累的机制[J]. 植物学报, 0 : 1 -0 . DOI: 10.11983/CBB25053

Abstract

INTRODUCTION: Manganese (Mn) is an essential micronutrient for plant growth and primarily act as enzyme cofactors and participate in the redox processes. However, excessive absorption of Mn by plant can also induce toxicity damages. 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, the cation diffusion facilitator (CDF) family transporters, which in plants are also known as metal tolerance proteins (MTP), had been shown to be crucial for Mn homeostasis. Therefore, identifying MTP family genes and elucidating their underlying mechanisms for Mn accumulation would not only provide the novel insights about basic scientific issues of plant Mn accumulation, but also gene resources for crops 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 of 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 the 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.

参考文献

[1]Alejandro S, H?ller S, Meier B, Peiter E((2020)).Manganese in Plants: From Acquisition to Subcellular Allocation..Front Plant Sci, 11:-. [2]Barton DA, Cole L, Collings DA, Liu DYT, Smith PMC, Day DA, Overall RL(2011).Cell‐to‐cell transport via the lumen of the endoplasmic reticulum.Plant J, 66:806-817. [3]Chen SY, Gu TY, Qi ZA, Yan J, Fang ZJ, Lu YT, Li H, Gong JM (2021).Two NPF transporters mediate iron long-distance transport and homeostasis in Arabidopsis. Plant Com 2:100244.., :-. [4]Chen Z, Fujii Y, Yamaji N, Masuda S, Takemoto Y, Kamiya T, Yusuyin Y, Iwasaki K, Kato S-i, Maeshima M, Ma JF, Ueno D(2013).Mn tolerance in rice is mediated by MTP8.a member of the cation diffusion facilitator family. J EXP BOT, 64:4375-4387. [5]Delhaize E, Gruber BD, Pittman JK, White RG, Leung H, Miao Y, Jiang L, Ryan PR, Richardson AE(2007).A role for the AtMTP11 gene of Arabidopsis in manganese transport and tolerance.Plant J, 51:198-210. [6]Elble R(1992).A simple and efficient procedure for transformation of yeasts.Biotechniques, 13(1):18-20. [7]Eroglu S, Meier B, Von WN, Peiter E(2016).The vacuolar manganese transporter MTP8 determines tolerance to Fe deficiency-induced chlorosis in Arabidopsis.Plant Physiol, 170:1030-1045. [8]Fang X, Tian DX, Xie RX(2006).Soil physical and chemical properties of the wasteland in Xiangtan manganese mine.Acta Ecol Sin, 26:1494-1501. [9]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. [10]Ge H, Shao Q, Chen J, Chen J, Li X, Tan Y, Lan W, Yang L, Wang Y (2022).A metal tolerance protein, MTP10, is required for the calcium and magnesium homeostasis in Arabidopsis. Plant Signal Behav 17.., :-. [11]Gu D, Zhou X, Yin X, Wu M, Chen W, Xu E, Liu Y, Gong C, Zhang W, Chen X (2022).Metal tolerance protein family members are involved in Mn homeostasis through internal compartmentation and exocytosis in Brassica napus. Environ. Exp. Bot 195: 104785., :-. [12]Gu TY, Gong YQ, Zhang GB, Peng JS(2020).Development and application of the meta-ionomic assay to identify heavy metal pollution.Plant Physiol J, 56(3):584-590. [13]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(3):584-590. [14]Gustin JL, Zanis MJ, Salt DE (2011).Structure and evolution of the plant cation diffusion facilitator family of ion transporters. BMC Evol Biol 11.., :-. [15]Hu HL, He YT, Gao Y, Chen SY, Gu TY, Peng JS (2025).NnMTP10 from Nelumbo nucifera acts as a transporter mediating manganese and iron efflux. Plant Mol Biol 115., :-. [16]Hu HL, Gu TY, Chen SY, Wang Y, Peng JS(2024).Isolation and functional verification of genes mediating mineral element stress tolerance in Lotus.Scientia Agricultura Sinica, 57(5):980-988. [17]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(5):980-988. [18]Jaiswal S, Kumari A, Kumar K, Laxmi V, Kaur S, Kumar A, Verma H, Shimray P, Touthang L, Talukdar M, Mishra VK, Singh BK (2024).Deciphering genetic mechanisms of Al toxicity tolerance through meta-QTL analysis in rice (Oryza sativa L.). Environ Exp Bot 228.., :-. [19]Ju CF, Zhang ZQ, Deng JP, Miao CC, Wang ZQ, Wallrad L, Javed L, Fu DL, Zhang T, Kudla J, Gong ZZ, Wang C(2021).Ca2+-dependent successive phosphorylation of vacuolar transporter MTP8 by CBL23-CIPK3926 and CPK5 contributes to manganese homeostasis in Arabidopsis.Mol Plant, 15(3):419-437. [20]Li J, Dong R, Jia Y, Huang J, Zou X, An N, Song J, Chen Z (2021).Characterization of Metal Tolerance Proteins and Functional Analysis of GmMTP8.1 Involved in Manganese Tolerance in Soybean. Front Plant Sci 12.., :-. [21]Li J, Jia Y, Dong R, Huang R, Liu P, Li X, Wang Z, Liu G, Chen Z (2019).Advances in the Mechanisms of Plant Tolerance to Manganese Toxicity. Int J Mol Sci 20.., :-. [22]Ma G, Li JY, Li JJ, Li Y, Gu DF, Chen C, Cui J, Chen X, Zhang W(2018).OsMTP11,a trans-Golgi network localized transporter,is involved in manganese tolerance in rice.Plant Sci, 274:59-69. [23]Millaleo R, Reyes-Díaz M, Ivanov AG, Mora ML, Alberdi M(2010).Manganese as essential and toxic element for plants: transport,accumulation and resistance mechanism.J Soil Sci Plant Nutr, 10:470-481. [24]Montanini B, Blaudez D, Jeandroz S, Sanders D, Chalot M (2007).Phylogenetic and functional analysis of the cation diffusion facilitator (CDF) family: improved signature and prediction of substrate specificity. BMC Genomics 8 (1): 107.., :-. [25]Nelson BK, Cai X, Nebenführ A(2007).A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants.Plant J, 51:1126-1136. [26]Pedas P, Schiller Stokholm M, Hegelund JN, Ladeg?rd AH, Schjoerring JK, Husted S (2014).Golgi localized Barley MTP8 proteins facilitate Mn transport. PLoS ONE 9.., :-. [27]Peiter E, Montanini B, Gobert A, Pedas P, Husted S, Maathuis FJM, Blaudez D, Chalot M, Sanders D(2007).A secretory pathway-localized cation diffusion facilitator confers plant manganese tolerance.Proc Natl Acad Sci, 104:8532-8537. [28]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. [29]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. [30]Peng JS, Ding G, Meng S, Yi HY, Gong JM(2017).Enhanced metal tolerance correlates with heterotypic variation in SpMTL,a metallothionein-like protein from the hyperaccumulator Sedum plumbizincicola.Plant Cell Environ, 40:1368-1378. [31]Peng JS, Wang YJ, Ding G, Ma HL, Zhang YJ, Gong JM(2017).A pivotal role of cell wall in cadmium accumulation in the Crassulaceae hyperaccumulator Sedum plumbizincicola.Mol Plant, 10:771-774. [32]Peng JS, Wang YT, Wang MQ, Liu LL, Wang P, Li Z, Li S, Chen SY, Meng S, Gu TY,Xu WZ, Chao ZF, Huang YQ, Jin CW, Chao DY, Chen CY, Wu LH, Teng Y, Zhao FJ, Gong JM (2024).Research and regulation of cadmium uptake, transport and accumulation in plants, Plant Physiol J 60 (2):185-210., :-. [33]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(2):185-210. [34]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. [35]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., :-. [36]Sinclair SA, Senger T, Talke IN, Cobbett CS, Haydon MJ, Kr?mer U(2018).Systemic Upregulation of MTP2- and HMA2-Mediated Zn Partitioning to the Shoot Supplements Local Zn Deficiency Responses.Plant Cell, 30:2463-2479. [37]Takemoto Y, Tsunemitsu Y, Fujii-Kashino M, Mitani-Ueno N, Yamaji N, Ma JF, Kato S-i, Iwasaki K, Ueno D(2017).The tonoplast-localized transporter MTP8.contributes to manganese detoxification in the shoots and roots of Oryza sativa L. Plant Cell Physiol, 58:1573-1582. [38]Tsunemitsu Y, Yamaji N, Ma JF, Kato S-i, Iwasaki K, Ueno D (2018).Rice reduces Mn uptake in response to Mn stress. Plant Signal Behav 13.., :-. [39]Ueno D, Sasaki A, Yamaji N, Miyaji T, Fujii Y, Takemoto Y, Moriyama S, Che J, Moriyama Y, Iwasaki K, Ma JF (2015).A polarly localized transporter for efficient manganese uptake in rice. Nature Plants 1.., :-. [40]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, (7):1353-1358. [41]王垚,胡博,邓小秋,蒋佳佳,杜兰芳,彭佳师(2022).伴矿景天 基因提高酵母对镉的抗性.植物生理学报, (7):1353-1358. [42]Zhang M, Liu BX (2017).Identification of a rice metal tolerance protein OsMTP11 as a manganese transporter. PLoS ONE 12(4): e0174987.., :-. [43]Zhang PH, Zhang SZ, Zhang ZY, Li MY, Liu YJ, Zhang XJ, Bai NN, Ma M, Peng JS(2022).SpHIPP45 gene from Sedum plumbizincicola specifically mediates cadmium tolerance.Plant Physiol J, (7):1346-1352. [44]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).伴矿景天基因特异介导镉耐受性.植物生理学报, (7):1346-1352. [45]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. [46]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. [47]Zhang XJ, Zhang ZY, Zhang SZ, Bai NN, Liu M, Peng JS(2023).Isolation and functional characterization of phytochelatin synthase gene BnPCS1a in Brassica napus.Plant Physiol J, (5):861-868. [48]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的分离与功能验证.植物生理学报, (5):861-868. [49]Zhao Y, Li L, Ma S, Han R, He Y, Zhu J, Li M, Zhuang J, Wang Y, Zhao Z, Chen X, Liu SJ,Li XH (2024).Mn-CDF family genes enhance the manganese tolerance of the tea plants (Camellia sinensis) under acidic condition. Plant Physiol Bioch 216.., :-.
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