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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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-09-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2022.1007542/full |
| _version_ | 1798001330485198848 |
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| author | Joon-Yung Cha Joon-Yung Cha Song Yi Jeong Gyeongik Ahn Gyeong-Im Shin Myung Geun Ji Myung Geun Ji Sang Cheol Lee Dhruba Khakurel Donah Mary Macoy Yong Bok Lee Min Gab Kim Sang Yeol Lee Dae-Jin Yun Woe-Yeon Kim Woe-Yeon Kim |
| author_facet | Joon-Yung Cha Joon-Yung Cha Song Yi Jeong Gyeongik Ahn Gyeong-Im Shin Myung Geun Ji Myung Geun Ji Sang Cheol Lee Dhruba Khakurel Donah Mary Macoy Yong Bok Lee Min Gab Kim Sang Yeol Lee Dae-Jin Yun Woe-Yeon Kim Woe-Yeon Kim |
| author_sort | Joon-Yung Cha |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-04-11T11:35:35Z |
| format | Article |
| id | doaj.art-424cd8d9b1c443b68a42e0f526d913d4 |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-04-11T11:35:35Z |
| publishDate | 2022-09-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-424cd8d9b1c443b68a42e0f526d913d42022-12-22T04:26:00ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-09-011310.3389/fpls.2022.10075421007542The thiol-reductase activity of YUCCA6 enhances nickel heavy metal stress tolerance in ArabidopsisJoon-Yung Cha0Joon-Yung Cha1Song Yi Jeong2Gyeongik Ahn3Gyeong-Im Shin4Myung Geun Ji5Myung Geun Ji6Sang Cheol Lee7Dhruba Khakurel8Donah Mary Macoy9Yong Bok Lee10Min Gab Kim11Sang Yeol Lee12Dae-Jin Yun13Woe-Yeon Kim14Woe-Yeon Kim15Research Institute of Life Sciences, Institute of Agriculture and Life Science, Gyeongsang National University, Jinju, South KoreaDivision of Applied Life Science (BK21four), Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University, Jinju, South KoreaDivision of Applied Life Science (BK21four), Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University, Jinju, South KoreaResearch Institute of Life Sciences, Institute of Agriculture and Life Science, Gyeongsang National University, Jinju, South KoreaDivision of Applied Life Science (BK21four), Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University, Jinju, South KoreaResearch Institute of Life Sciences, Institute of Agriculture and Life Science, Gyeongsang National University, Jinju, South KoreaDivision of Applied Life Science (BK21four), Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University, Jinju, South KoreaDivision of Applied Life Science (BK21four), Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University, Jinju, South KoreaDepartment of Biology, Graduate School of Gyeongsang National University, Jinju, South KoreaCollege of Pharmacy and Research Institute of Pharmaceutical Science, Gyeongsang National University, Jinju, South KoreaDivision of Applied Life Science (BK21four), Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University, Jinju, South KoreaCollege of Pharmacy and Research Institute of Pharmaceutical Science, Gyeongsang National University, Jinju, South KoreaDivision of Applied Life Science (BK21four), Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University, Jinju, South KoreaDepartment of Biomedical Science and Engineering, Konkuk University, Seoul, South KoreaResearch Institute of Life Sciences, Institute of Agriculture and Life Science, Gyeongsang National University, Jinju, South KoreaDivision of Applied Life Science (BK21four), Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University, Jinju, South KoreaAnthropogenic 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.https://www.frontiersin.org/articles/10.3389/fpls.2022.1007542/fullauxinheavy metal tolerancenickel stressreactive oxygen speciesthiol-reductase |
| spellingShingle | Joon-Yung Cha Joon-Yung Cha Song Yi Jeong Gyeongik Ahn Gyeong-Im Shin Myung Geun Ji Myung Geun Ji Sang Cheol Lee Dhruba Khakurel Donah Mary Macoy Yong Bok Lee Min Gab Kim Sang Yeol Lee Dae-Jin Yun Woe-Yeon Kim Woe-Yeon Kim The thiol-reductase activity of YUCCA6 enhances nickel heavy metal stress tolerance in Arabidopsis Frontiers in Plant Science auxin heavy metal tolerance nickel stress reactive oxygen species thiol-reductase |
| 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 | auxin heavy metal tolerance nickel stress reactive oxygen species thiol-reductase |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2022.1007542/full |
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