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Glutathione degradation activity of γ‐glutamyl peptidase 1 manifests its dual roles in primary and secondary sulfur metabolism in Arabidopsis

Glutathione (GSH) functions as a major sulfur repository and hence occupies an important position in primary sulfur metabolism. GSH degradation results in sulfur reallocation and is believed to be carried out mainly by γ‐glutamyl cyclotransferases (GGCT2;1, GGCT2;2, and GGCT2;3), which, however, do...

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Autores principales: Ito, Takehiro, Kitaiwa, Taisuke, Nishizono, Kosuke, Umahashi, Minori, Miyaji, Shunsuke, Agake, Shin‐ichiro, Kuwahara, Kana, Yokoyama, Tadashi, Fushinobu, Shinya, Maruyama‐Nakashita, Akiko, Sugiyama, Ryosuke, Sato, Muneo, Inaba, Jun, Hirai, Masami Yokota, Ohkama‐Ohtsu, Naoko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9804317/
https://www.ncbi.nlm.nih.gov/pubmed/35932489
http://dx.doi.org/10.1111/tpj.15912
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author Ito, Takehiro
Kitaiwa, Taisuke
Nishizono, Kosuke
Umahashi, Minori
Miyaji, Shunsuke
Agake, Shin‐ichiro
Kuwahara, Kana
Yokoyama, Tadashi
Fushinobu, Shinya
Maruyama‐Nakashita, Akiko
Sugiyama, Ryosuke
Sato, Muneo
Inaba, Jun
Hirai, Masami Yokota
Ohkama‐Ohtsu, Naoko
author_facet Ito, Takehiro
Kitaiwa, Taisuke
Nishizono, Kosuke
Umahashi, Minori
Miyaji, Shunsuke
Agake, Shin‐ichiro
Kuwahara, Kana
Yokoyama, Tadashi
Fushinobu, Shinya
Maruyama‐Nakashita, Akiko
Sugiyama, Ryosuke
Sato, Muneo
Inaba, Jun
Hirai, Masami Yokota
Ohkama‐Ohtsu, Naoko
author_sort Ito, Takehiro
collection PubMed
description Glutathione (GSH) functions as a major sulfur repository and hence occupies an important position in primary sulfur metabolism. GSH degradation results in sulfur reallocation and is believed to be carried out mainly by γ‐glutamyl cyclotransferases (GGCT2;1, GGCT2;2, and GGCT2;3), which, however, do not fully explain the rapid GSH turnover. Here, we discovered that γ‐glutamyl peptidase 1 (GGP1) contributes to GSH degradation through a yeast complementation assay. Recombinant proteins of GGP1, as well as GGP3, showed high degradation activity of GSH, but not of oxidized glutathione (GSSG), in vitro. Notably, the GGP1 transcripts were highly abundant in rosette leaves, in agreement with the ggp1 mutants constantly accumulating more GSH regardless of nutritional conditions. Given the lower energy requirements of the GGP‐ than the GGCT‐mediated pathway, the GGP‐mediated pathway could be a more efficient route for GSH degradation than the GGCT‐mediated pathway. Therefore, we propose a model wherein cytosolic GSH is degraded chiefly by GGP1 and likely also by GGP3. Another noteworthy fact is that GGPs are known to process GSH conjugates in glucosinolate and camalexin synthesis; indeed, we confirmed that the ggp1 mutant contained higher levels of O‐acetyl‐l‐Ser, a signaling molecule for sulfur starvation, and lower levels of glucosinolates and their degradation products. The predicted structure of GGP1 further provided a rationale for this hypothesis. In conclusion, we suggest that GGP1 and possibly GGP3 play vital roles in both primary and secondary sulfur metabolism.
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spelling pubmed-98043172023-01-03 Glutathione degradation activity of γ‐glutamyl peptidase 1 manifests its dual roles in primary and secondary sulfur metabolism in Arabidopsis Ito, Takehiro Kitaiwa, Taisuke Nishizono, Kosuke Umahashi, Minori Miyaji, Shunsuke Agake, Shin‐ichiro Kuwahara, Kana Yokoyama, Tadashi Fushinobu, Shinya Maruyama‐Nakashita, Akiko Sugiyama, Ryosuke Sato, Muneo Inaba, Jun Hirai, Masami Yokota Ohkama‐Ohtsu, Naoko Plant J Original Articles Glutathione (GSH) functions as a major sulfur repository and hence occupies an important position in primary sulfur metabolism. GSH degradation results in sulfur reallocation and is believed to be carried out mainly by γ‐glutamyl cyclotransferases (GGCT2;1, GGCT2;2, and GGCT2;3), which, however, do not fully explain the rapid GSH turnover. Here, we discovered that γ‐glutamyl peptidase 1 (GGP1) contributes to GSH degradation through a yeast complementation assay. Recombinant proteins of GGP1, as well as GGP3, showed high degradation activity of GSH, but not of oxidized glutathione (GSSG), in vitro. Notably, the GGP1 transcripts were highly abundant in rosette leaves, in agreement with the ggp1 mutants constantly accumulating more GSH regardless of nutritional conditions. Given the lower energy requirements of the GGP‐ than the GGCT‐mediated pathway, the GGP‐mediated pathway could be a more efficient route for GSH degradation than the GGCT‐mediated pathway. Therefore, we propose a model wherein cytosolic GSH is degraded chiefly by GGP1 and likely also by GGP3. Another noteworthy fact is that GGPs are known to process GSH conjugates in glucosinolate and camalexin synthesis; indeed, we confirmed that the ggp1 mutant contained higher levels of O‐acetyl‐l‐Ser, a signaling molecule for sulfur starvation, and lower levels of glucosinolates and their degradation products. The predicted structure of GGP1 further provided a rationale for this hypothesis. In conclusion, we suggest that GGP1 and possibly GGP3 play vital roles in both primary and secondary sulfur metabolism. John Wiley and Sons Inc. 2022-08-06 2022-09 /pmc/articles/PMC9804317/ /pubmed/35932489 http://dx.doi.org/10.1111/tpj.15912 Text en © 2022 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ (https://creativecommons.org/licenses/by-nc-nd/4.0/) License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.
spellingShingle Original Articles
Ito, Takehiro
Kitaiwa, Taisuke
Nishizono, Kosuke
Umahashi, Minori
Miyaji, Shunsuke
Agake, Shin‐ichiro
Kuwahara, Kana
Yokoyama, Tadashi
Fushinobu, Shinya
Maruyama‐Nakashita, Akiko
Sugiyama, Ryosuke
Sato, Muneo
Inaba, Jun
Hirai, Masami Yokota
Ohkama‐Ohtsu, Naoko
Glutathione degradation activity of γ‐glutamyl peptidase 1 manifests its dual roles in primary and secondary sulfur metabolism in Arabidopsis
title Glutathione degradation activity of γ‐glutamyl peptidase 1 manifests its dual roles in primary and secondary sulfur metabolism in Arabidopsis
title_full Glutathione degradation activity of γ‐glutamyl peptidase 1 manifests its dual roles in primary and secondary sulfur metabolism in Arabidopsis
title_fullStr Glutathione degradation activity of γ‐glutamyl peptidase 1 manifests its dual roles in primary and secondary sulfur metabolism in Arabidopsis
title_full_unstemmed Glutathione degradation activity of γ‐glutamyl peptidase 1 manifests its dual roles in primary and secondary sulfur metabolism in Arabidopsis
title_short Glutathione degradation activity of γ‐glutamyl peptidase 1 manifests its dual roles in primary and secondary sulfur metabolism in Arabidopsis
title_sort glutathione degradation activity of γ‐glutamyl peptidase 1 manifests its dual roles in primary and secondary sulfur metabolism in arabidopsis
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9804317/
https://www.ncbi.nlm.nih.gov/pubmed/35932489
http://dx.doi.org/10.1111/tpj.15912
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