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Both the concentration and redox state of glutathione and ascorbate influence the sensitivity of arabidopsis to cadmium
Background and Aims Cadmium (Cd) is a non-essential trace element that elicits oxidative stress. Plants respond to Cd toxicity via increasing their Cd-chelating and antioxidative capacities. They predominantly chelate Cd via glutathione (GSH) and phytochelatins (PCs), while antioxidative defence is...
Autores principales: | , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Oxford University Press
2015
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4577996/ https://www.ncbi.nlm.nih.gov/pubmed/26070641 http://dx.doi.org/10.1093/aob/mcv075 |
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author | Jozefczak, Marijke Bohler, Sacha Schat, Henk Horemans, Nele Guisez, Yves Remans, Tony Vangronsveld, Jaco Cuypers, Ann |
author_facet | Jozefczak, Marijke Bohler, Sacha Schat, Henk Horemans, Nele Guisez, Yves Remans, Tony Vangronsveld, Jaco Cuypers, Ann |
author_sort | Jozefczak, Marijke |
collection | PubMed |
description | Background and Aims Cadmium (Cd) is a non-essential trace element that elicits oxidative stress. Plants respond to Cd toxicity via increasing their Cd-chelating and antioxidative capacities. They predominantly chelate Cd via glutathione (GSH) and phytochelatins (PCs), while antioxidative defence is mainly based on the use and recycling of both GSH and ascorbate (AsA), complemented by superoxide dismutase (SOD) and catalase (CAT). In addition, both metabolites act as a substrate for the regeneration of other essential antioxidants, which neutralize and regulate reactive oxygen species (ROS). Together, these functions influence the concentration and cellular redox state of GSH and AsA. In this study, these two parameters were examined in plants of Arabidopsis thaliana exposed to sub-lethal Cd concentrations. Methods Wild-type plants and mutant arabidopsis plants containing 30–45 % of wild-type levels of GSH (cad2-1) or 40–50 % of AsA (vtc1-1), together with the double-mutant (cad2-1 vtc1-1) were cultivated in a hydroponic system and exposed to sub-lethal Cd concentrations. Cadmium detoxification was investigated at different levels including gene expression and metabolite concentrations. Key Results In comparison with wild-type plants, elevated basal thiol levels and enhanced PC synthesis upon exposure to Cd efficiently compensated AsA deficiency in vtc1-1 plants and contributed to decreased sensitivity towards Cd. Glutathione-deficient (cad2-1 and cad2-1 vtc1-1) mutants, however, showed a more oxidized GSH redox state, resulting in initial oxidative stress and a higher sensitivity to Cd. In order to cope with the Cd stress to which they were exposed, GSH-deficient mutants activated multiple alternative pathways. Conclusions Our observations indicate that GSH and AsA deficiency differentially alter plant GSH homeostasis, resulting in opposite Cd sensitivities relative to wild-type plants. Upon Cd exposure, GSH-deficient mutants were hampered in chelation. They experienced phenotypic disturbances and even more oxidative stress, and therefore activated multiple alternative pathways such as SOD, CAT and ascorbate peroxidase, indicating a higher Cd sensitivity. Ascorbate deficiency, however, was associated with enhanced PC synthesis in comparison with wild-type plants after Cd exposure, which contributed to decreased sensitivity towards Cd. |
format | Online Article Text |
id | pubmed-4577996 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2015 |
publisher | Oxford University Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-45779962015-09-24 Both the concentration and redox state of glutathione and ascorbate influence the sensitivity of arabidopsis to cadmium Jozefczak, Marijke Bohler, Sacha Schat, Henk Horemans, Nele Guisez, Yves Remans, Tony Vangronsveld, Jaco Cuypers, Ann Ann Bot Articles Background and Aims Cadmium (Cd) is a non-essential trace element that elicits oxidative stress. Plants respond to Cd toxicity via increasing their Cd-chelating and antioxidative capacities. They predominantly chelate Cd via glutathione (GSH) and phytochelatins (PCs), while antioxidative defence is mainly based on the use and recycling of both GSH and ascorbate (AsA), complemented by superoxide dismutase (SOD) and catalase (CAT). In addition, both metabolites act as a substrate for the regeneration of other essential antioxidants, which neutralize and regulate reactive oxygen species (ROS). Together, these functions influence the concentration and cellular redox state of GSH and AsA. In this study, these two parameters were examined in plants of Arabidopsis thaliana exposed to sub-lethal Cd concentrations. Methods Wild-type plants and mutant arabidopsis plants containing 30–45 % of wild-type levels of GSH (cad2-1) or 40–50 % of AsA (vtc1-1), together with the double-mutant (cad2-1 vtc1-1) were cultivated in a hydroponic system and exposed to sub-lethal Cd concentrations. Cadmium detoxification was investigated at different levels including gene expression and metabolite concentrations. Key Results In comparison with wild-type plants, elevated basal thiol levels and enhanced PC synthesis upon exposure to Cd efficiently compensated AsA deficiency in vtc1-1 plants and contributed to decreased sensitivity towards Cd. Glutathione-deficient (cad2-1 and cad2-1 vtc1-1) mutants, however, showed a more oxidized GSH redox state, resulting in initial oxidative stress and a higher sensitivity to Cd. In order to cope with the Cd stress to which they were exposed, GSH-deficient mutants activated multiple alternative pathways. Conclusions Our observations indicate that GSH and AsA deficiency differentially alter plant GSH homeostasis, resulting in opposite Cd sensitivities relative to wild-type plants. Upon Cd exposure, GSH-deficient mutants were hampered in chelation. They experienced phenotypic disturbances and even more oxidative stress, and therefore activated multiple alternative pathways such as SOD, CAT and ascorbate peroxidase, indicating a higher Cd sensitivity. Ascorbate deficiency, however, was associated with enhanced PC synthesis in comparison with wild-type plants after Cd exposure, which contributed to decreased sensitivity towards Cd. Oxford University Press 2015-09 2015-06-12 /pmc/articles/PMC4577996/ /pubmed/26070641 http://dx.doi.org/10.1093/aob/mcv075 Text en © The Author 2015. Published by Oxford University Press on behalf of the Annals of Botany Company. http://creativecommons.org/licenses/by/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. |
spellingShingle | Articles Jozefczak, Marijke Bohler, Sacha Schat, Henk Horemans, Nele Guisez, Yves Remans, Tony Vangronsveld, Jaco Cuypers, Ann Both the concentration and redox state of glutathione and ascorbate influence the sensitivity of arabidopsis to cadmium |
title | Both the concentration and redox state of glutathione and ascorbate influence the sensitivity of arabidopsis to cadmium |
title_full | Both the concentration and redox state of glutathione and ascorbate influence the sensitivity of arabidopsis to cadmium |
title_fullStr | Both the concentration and redox state of glutathione and ascorbate influence the sensitivity of arabidopsis to cadmium |
title_full_unstemmed | Both the concentration and redox state of glutathione and ascorbate influence the sensitivity of arabidopsis to cadmium |
title_short | Both the concentration and redox state of glutathione and ascorbate influence the sensitivity of arabidopsis to cadmium |
title_sort | both the concentration and redox state of glutathione and ascorbate influence the sensitivity of arabidopsis to cadmium |
topic | Articles |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4577996/ https://www.ncbi.nlm.nih.gov/pubmed/26070641 http://dx.doi.org/10.1093/aob/mcv075 |
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