Glutathione and phytochelatins jointly allow intracellular and extracellular detoxification of cadmium in the liverwort Marchantia polymorpha

被引:15
作者
Bellini, Erika [1 ]
Bandoni, Elena [1 ]
Giardini, Silvia [1 ]
Sorce, Carlo [1 ]
Spano, Carmelina [1 ]
Bottega, Stefania [1 ]
Fontanini, Debora [1 ]
Kola, Arian [2 ]
Valensin, Daniela [2 ]
Bertolini, Andrea [3 ]
Saba, Alessandro [3 ]
Paoli, Luca [1 ]
Andreucci, Andrea [1 ]
Li, Mingai [4 ]
Varotto, Claudio [4 ]
di Toppi, Luigi Sanita [1 ]
机构
[1] Univ Pisa, Dept Biol, Via L Ghini 13, I-56126 Pisa, Italy
[2] Univ Siena, Dept Biotechnol Chem & Pharm, Siena, Italy
[3] Univ Pisa, Dept Surg Med & Mol Pathol & Crit Care Med, Pisa, Italy
[4] Fdn Edmund Mach, Res & Innovat Ctr, Biodivers Ecol & Environm Area, Via Mach 1, I-38098 Trento, San Michele All, Italy
关键词
Cadmium; Glutathione; Marchantia polymorpha; Phytochelatins; Thiol-cadmium complex; Thiol extracellular release; AGROBACTERIUM-MEDIATED TRANSFORMATION; ARABIDOPSIS-THALIANA; BINDING PEPTIDES; ABC TRANSPORTERS; HEAVY-METALS; ESI-MS; CELL; BRYOPHYTES; TOLERANCE; MOSS;
D O I
10.1016/j.envexpbot.2023.105303
中图分类号
Q94 [植物学];
学科分类号
071001 ;
摘要
Plants have evolved a set of mechanisms that control and respond to the uptake and accumulation of both essential and non-essential metals, including chelation and sequestration of these elements by thiol ligands, such as glutathione and phytochelatins. Indeed, such thiol peptides can chelate some metals, quickly form thiol-metal complexes, and segregate them in the vacuolar compartment. Reasonably, conceptually similar mechanisms can be assumed to be responsible for the transport of metal complexes -in particular thiol-cadmium complexes-across the plasma membrane, with the consequent release of this toxic metal in the extracellular environment. Such hypothesis, focusing on prevention and detoxification mechanisms, was here verified in axenically-grown ga-metophytes of the model liverwort Marchantia polymorpha, exposed to three different cadmium concentrations over five exposure times. From the data obtained, it can be deduced that the cell wall of M. polymorpha moderately reduced the influx of cadmium into the cells, since it was rapidly saturated by this metal. At an intracellular level, cadmium induced the activity, but not the gene expression, of the phytochelatin synthase enzyme, leading to synthesis of phytochelatins. Moreover, both glutathione and phytochelatins chelated cad-mium at the cytosolic level and allowed its detoxification, possibly involving tonoplast transporters belonging to type-C ABC subfamily (Mp7g13860 and Mp4g11930). Likewise, cadmium, glutathione and phytochelatins were released extracellularly, thus highlighting a possible novel role in cadmium detoxification, in a pH-dependent manner. The overall results suggest that, in M. polymorpha, glutathione and phytochelatins can accomplish intracellular and extracellular detoxification of cadmium.
引用
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页数:12
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共 75 条
[1]  
ALLOWAY BJ., 2013, Heavy metals in soils : trace metals and metalloids in soils and their bioavailability, V3rd
[2]   Differential Metal Tolerance and Accumulation Patterns of Cd, Cu, Pb and Zn in the Liverwort Marchantia polymorpha L. [J].
Ares, Angela ;
Itouga, Misao ;
Kato, Yukari ;
Sakakibara, Hitoshi .
BULLETIN OF ENVIRONMENTAL CONTAMINATION AND TOXICOLOGY, 2018, 100 (03) :444-450
[3]   Response of Pteris vittata to different cadmium treatments [J].
Balestri, Mirko ;
Bottega, Stefania ;
Spano, Carmelina .
ACTA PHYSIOLOGIAE PLANTARUM, 2014, 36 (03) :767-775
[4]   Bioacumulation and ultrastructural effects of Cd, Cu, Pb and Zn in the moss Scorpiurum circinatum (Brid.) Fleisch & Loeske [J].
Basile, A. ;
Sorbo, S. ;
Pisani, T. ;
Paoli, L. ;
Munzi, S. ;
Loppi, S. .
ENVIRONMENTAL POLLUTION, 2012, 166 :208-211
[5]   Heavy metal deposition in the Italian "triangle of death" determined with the moss Scorpiurum circinatum [J].
Basile, A. ;
Sorbo, S. ;
Aprile, G. ;
Conte, B. ;
Cobianchi, R. Castaldo ;
Pisani, T. ;
Loppi, S. .
ENVIRONMENTAL POLLUTION, 2009, 157 (8-9) :2255-2260
[6]   Responses to Cadmium in Early-Diverging Streptophytes (Charophytes and Bryophytes): Current Views and Potential Applications [J].
Bellini, Erika ;
Betti, Camilla ;
Sanita di Toppi, Luigi .
PLANTS-BASEL, 2021, 10 (04)
[7]   Eukaryotic and Prokaryotic Phytochelatin Synthases Differ Less in Functional Terms Than Previously Thought: A Comparative Analysis of Marchantia polymorpha and Geitlerinema sp. PCC 7407 [J].
Bellini, Erika ;
Varotto, Claudio ;
Borso, Marco ;
Rugnini, Lorenza ;
Bruno, Laura ;
Sanita di Toppi, Luigi .
PLANTS-BASEL, 2020, 9 (07) :1-12
[8]   Characterization and quantification of thiol-peptides in Arabidopsis thaliana using combined dilution and high sensitivity HPLC-ESI-MS-MS [J].
Bellini, Erika ;
Borso, Marco ;
Betti, Camilla ;
Bruno, Laura ;
Andreucci, Andrea ;
Castiglione, Monica Ruffini ;
Saba, Alessandro ;
Sanita di Toppi, Luigi .
PHYTOCHEMISTRY, 2019, 164 :215-222
[9]   The renaissance and enlightenment of Marchantia as a model system [J].
Bowman, John L. ;
Arteaga-Vazquez, Mario ;
Berger, Frederic ;
Briginshaw, Liam N. ;
Carella, Philip ;
Aguilar-Cruz, Adolfo ;
Davies, Kevin M. ;
Dierschke, Tom ;
Dolan, Liam ;
Dorantes-Acosta, Ana E. ;
Fisher, Tom J. ;
Flores-Sandoval, Eduardo ;
Futagami, Kazutaka ;
Ishizaki, Kimitsune ;
Jibran, Rubina ;
Kanazawa, Takehiko ;
Kato, Hirotaka ;
Kohchi, Takayuki ;
Levins, Jonathan ;
Lin, Shih-Shun ;
Nakagami, Hirofumi ;
Nishihama, Ryuichi ;
Romani, Facundo ;
Schornack, Sebastian ;
Tanizawa, Yasuhiro ;
Tsuzuki, Masayuki ;
Ueda, Takashi ;
Watanabe, Yuichiro ;
Yamato, Katsuyuki T. ;
Zachgo, Sabine .
PLANT CELL, 2022, 34 (10) :3512-3542
[10]   Insights into Land Plant Evolution Garnered from the Marchantia polymorpha Genome [J].
Bowman, John L. ;
Kohchi, Takayuki ;
Yamato, Katsuyuki T. ;
Jenkins, Jerry ;
Shu, Shengqiang ;
Ishizaki, Kimitsune ;
Yamaoka, Shohei ;
Nishihama, Ryuichi ;
Nakamura, Yasukazu ;
Berger, Frederic ;
Adam, Catherine ;
Aki, Shiori Sugamata ;
Althoff, Felix ;
Araki, Takashi ;
Arteaga-Vazquez, Mario A. ;
Balasubrmanian, Sureshkumar ;
Barry, Kerrie ;
Bauer, Diane ;
Boehm, Christian R. ;
Briginshaw, Liam ;
Caballero-Perez, Juan ;
Catarino, Bruno ;
Chen, Feng ;
Chiyoda, Shota ;
Chovatia, Mansi ;
Davies, Kevin M. ;
Delmans, Mihails ;
Demura, Taku ;
Dierschke, Tom ;
Dolan, Liam ;
Dorantes-Acosta, Ana E. ;
Eklund, D. Magnus ;
Florent, Stevie N. ;
Flores-Sandoval, Eduardo ;
Fujiyama, Asao ;
Fukuzawa, Hideya ;
Galik, Bence ;
Grimanelli, Daniel ;
Grimwood, Jane ;
Grossniklaus, Ueli ;
Hamada, Takahiro ;
Haseloff, Jim ;
Hetherington, Alexander J. ;
Higo, Asuka ;
Hirakawa, Yuki ;
Hundley, Hope N. ;
Ikeda, Yoko ;
Inoue, Keisuke ;
Inoue, Shin-Ichiro ;
Ishida, Sakiko .
CELL, 2017, 171 (02) :287-+