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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...

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Autores principales: 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
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
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.
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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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