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The thiol-reductase activity of YUCCA6 enhances nickel heavy metal stress tolerance in Arabidopsis
Anthropogenic activities cause the leaching of heavy metals into groundwater and their accumulation in soil. Excess levels of heavy metals cause toxicity in plants, inducing the production of reactive oxygen species (ROS) and possible death caused by the resulting oxidative stress. Heavy metal stres...
Autores principales: | , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Frontiers Media S.A.
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9551240/ https://www.ncbi.nlm.nih.gov/pubmed/36237515 http://dx.doi.org/10.3389/fpls.2022.1007542 |
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author | Cha, Joon-Yung Jeong, Song Yi Ahn, Gyeongik Shin, Gyeong-Im Ji, Myung Geun Lee, Sang Cheol Khakurel, Dhruba Macoy, Donah Mary Lee, Yong Bok Kim, Min Gab Lee, Sang Yeol Yun, Dae-Jin Kim, Woe-Yeon |
author_facet | Cha, Joon-Yung Jeong, Song Yi Ahn, Gyeongik Shin, Gyeong-Im Ji, Myung Geun Lee, Sang Cheol Khakurel, Dhruba Macoy, Donah Mary Lee, Yong Bok Kim, Min Gab Lee, Sang Yeol Yun, Dae-Jin Kim, Woe-Yeon |
author_sort | Cha, Joon-Yung |
collection | PubMed |
description | Anthropogenic activities cause the leaching of heavy metals into groundwater and their accumulation in soil. Excess levels of heavy metals cause toxicity in plants, inducing the production of reactive oxygen species (ROS) and possible death caused by the resulting oxidative stress. Heavy metal stresses repress auxin biosynthesis and transport, inhibiting plant growth. Here, we investigated whether nickel (Ni) heavy metal toxicity is reduced by exogenous auxin application and whether Ni stress tolerance in Arabidopsis thaliana is mediated by the bifunctional enzyme YUCCA6 (YUC6), which functions as an auxin biosynthetic enzyme and a thiol-reductase (TR). We found that an application of up to 1 µM exogenous indole-3-acetic acid (IAA) reduces Ni stress toxicity. yuc6-1D, a dominant mutant of YUC6 with high auxin levels, was more tolerant of Ni stress than wild-type (WT) plants, despite absorbing significantly more Ni. Treatments of WT plants with YUCASIN, a specific inhibitor of YUC-mediated auxin biosynthesis, increased Ni toxicity; however yuc6-1D was not affected by YUCASIN and remained tolerant of Ni stress. This suggests that rather than the elevated IAA levels in yuc6-1D, the TR activity of YUC6 might be critical for Ni stress tolerance. The loss of TR activity in YUC6 caused by the point-mutation of Cys85 abolished the YUC6-mediated Ni stress tolerance. We also found that the Ni stress–induced ROS accumulation was inhibited in yuc6-1D plants, which consequently also showed reduced oxidative damage. An enzymatic assay and transcriptional analysis revealed that the peroxidase activity and transcription of PEROXIREDOXIN Q were enhanced by Ni stress to a greater level in yuc6-1D than in the WT. These findings imply that despite the need to maintain endogenous IAA levels for basal Ni stress tolerance, the TR activity of YUC6, not the elevated IAA levels, plays the predominant role inNi stress tolerance by lowering Ni-induced oxidative stress. |
format | Online Article Text |
id | pubmed-9551240 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-95512402022-10-12 The thiol-reductase activity of YUCCA6 enhances nickel heavy metal stress tolerance in Arabidopsis Cha, Joon-Yung Jeong, Song Yi Ahn, Gyeongik Shin, Gyeong-Im Ji, Myung Geun Lee, Sang Cheol Khakurel, Dhruba Macoy, Donah Mary Lee, Yong Bok Kim, Min Gab Lee, Sang Yeol Yun, Dae-Jin Kim, Woe-Yeon Front Plant Sci Plant Science Anthropogenic activities cause the leaching of heavy metals into groundwater and their accumulation in soil. Excess levels of heavy metals cause toxicity in plants, inducing the production of reactive oxygen species (ROS) and possible death caused by the resulting oxidative stress. Heavy metal stresses repress auxin biosynthesis and transport, inhibiting plant growth. Here, we investigated whether nickel (Ni) heavy metal toxicity is reduced by exogenous auxin application and whether Ni stress tolerance in Arabidopsis thaliana is mediated by the bifunctional enzyme YUCCA6 (YUC6), which functions as an auxin biosynthetic enzyme and a thiol-reductase (TR). We found that an application of up to 1 µM exogenous indole-3-acetic acid (IAA) reduces Ni stress toxicity. yuc6-1D, a dominant mutant of YUC6 with high auxin levels, was more tolerant of Ni stress than wild-type (WT) plants, despite absorbing significantly more Ni. Treatments of WT plants with YUCASIN, a specific inhibitor of YUC-mediated auxin biosynthesis, increased Ni toxicity; however yuc6-1D was not affected by YUCASIN and remained tolerant of Ni stress. This suggests that rather than the elevated IAA levels in yuc6-1D, the TR activity of YUC6 might be critical for Ni stress tolerance. The loss of TR activity in YUC6 caused by the point-mutation of Cys85 abolished the YUC6-mediated Ni stress tolerance. We also found that the Ni stress–induced ROS accumulation was inhibited in yuc6-1D plants, which consequently also showed reduced oxidative damage. An enzymatic assay and transcriptional analysis revealed that the peroxidase activity and transcription of PEROXIREDOXIN Q were enhanced by Ni stress to a greater level in yuc6-1D than in the WT. These findings imply that despite the need to maintain endogenous IAA levels for basal Ni stress tolerance, the TR activity of YUC6, not the elevated IAA levels, plays the predominant role inNi stress tolerance by lowering Ni-induced oxidative stress. Frontiers Media S.A. 2022-09-27 /pmc/articles/PMC9551240/ /pubmed/36237515 http://dx.doi.org/10.3389/fpls.2022.1007542 Text en Copyright © 2022 Cha, Jeong, Ahn, Shin, Ji, Lee, Khakurel, Macoy, Lee, Kim, Lee, Yun and Kim https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
spellingShingle | Plant Science Cha, Joon-Yung Jeong, Song Yi Ahn, Gyeongik Shin, Gyeong-Im Ji, Myung Geun Lee, Sang Cheol Khakurel, Dhruba Macoy, Donah Mary Lee, Yong Bok Kim, Min Gab Lee, Sang Yeol Yun, Dae-Jin Kim, Woe-Yeon The thiol-reductase activity of YUCCA6 enhances nickel heavy metal stress tolerance in Arabidopsis |
title | The thiol-reductase activity of YUCCA6 enhances nickel heavy metal stress tolerance in Arabidopsis |
title_full | The thiol-reductase activity of YUCCA6 enhances nickel heavy metal stress tolerance in Arabidopsis |
title_fullStr | The thiol-reductase activity of YUCCA6 enhances nickel heavy metal stress tolerance in Arabidopsis |
title_full_unstemmed | The thiol-reductase activity of YUCCA6 enhances nickel heavy metal stress tolerance in Arabidopsis |
title_short | The thiol-reductase activity of YUCCA6 enhances nickel heavy metal stress tolerance in Arabidopsis |
title_sort | thiol-reductase activity of yucca6 enhances nickel heavy metal stress tolerance in arabidopsis |
topic | Plant Science |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9551240/ https://www.ncbi.nlm.nih.gov/pubmed/36237515 http://dx.doi.org/10.3389/fpls.2022.1007542 |
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