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

Glutathione degradation activity of γ-glutamyl peptidase 1 manifests its dual roles in primary and secondary sulfur metabolism in Arabidopsis.
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DOI:
10.1111/tpj.15912
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发表时间:
2022-09
期刊:
影响因子:
7.2
通讯作者:
Ohkama-Ohtsu, Naoko
Ohkama-Ohtsu, Naoko
中科院分区:
生物学1区
文献类型:
--
作者:
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

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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. Glutathione (GSH) is a major repository for organic sulfur in plants. In this study, we identified novel GSH degradation enzymes, γ‐glutamyl peptidases (GGPs), which may supply a substantial amount of cysteine in the cell. Moreover, GGPs also function in glucosinolate and camalexin synthesis, so GGPs can be regarded as enzymes that play important roles in both GSH degradation and glucosinolate and camalexin synthesis, that is, primary and secondary sulfur metabolism.
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