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Characterization of tryptophan oxidation affecting D1 degradation by FtsH in the photosystem II quality control of chloroplasts

Photosynthesis is one of the most important reactions for sustaining our environment. Photosystem II (PSII) is the initial site of photosynthetic electron transfer by water oxidation. Light in excess, however, causes the simultaneous production of reactive oxygen species (ROS), leading to photo-oxid...

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Autores principales: Kato, Yusuke, Kuroda, Hiroshi, Ozawa, Shin-Ichiro, Saito, Keisuke, Dogra, Vivek, Scholz, Martin, Zhang, Guoxian, de Vitry, Catherine, Ishikita, Hiroshi, Kim, Chanhong, Hippler, Michael, Takahashi, Yuichiro, Sakamoto, Wataru
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10665015/
https://www.ncbi.nlm.nih.gov/pubmed/37986577
http://dx.doi.org/10.7554/eLife.88822
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author Kato, Yusuke
Kuroda, Hiroshi
Ozawa, Shin-Ichiro
Saito, Keisuke
Dogra, Vivek
Scholz, Martin
Zhang, Guoxian
de Vitry, Catherine
Ishikita, Hiroshi
Kim, Chanhong
Hippler, Michael
Takahashi, Yuichiro
Sakamoto, Wataru
author_facet Kato, Yusuke
Kuroda, Hiroshi
Ozawa, Shin-Ichiro
Saito, Keisuke
Dogra, Vivek
Scholz, Martin
Zhang, Guoxian
de Vitry, Catherine
Ishikita, Hiroshi
Kim, Chanhong
Hippler, Michael
Takahashi, Yuichiro
Sakamoto, Wataru
author_sort Kato, Yusuke
collection PubMed
description Photosynthesis is one of the most important reactions for sustaining our environment. Photosystem II (PSII) is the initial site of photosynthetic electron transfer by water oxidation. Light in excess, however, causes the simultaneous production of reactive oxygen species (ROS), leading to photo-oxidative damage in PSII. To maintain photosynthetic activity, the PSII reaction center protein D1, which is the primary target of unavoidable photo-oxidative damage, is efficiently degraded by FtsH protease. In PSII subunits, photo-oxidative modifications of several amino acids such as Trp have been indeed documented, whereas the linkage between such modifications and D1 degradation remains elusive. Here, we show that an oxidative post-translational modification of Trp residue at the N-terminal tail of D1 is correlated with D1 degradation by FtsH during high-light stress. We revealed that Arabidopsis mutant lacking FtsH2 had increased levels of oxidative Trp residues in D1, among which an N-terminal Trp-14 was distinctively localized in the stromal side. Further characterization of Trp-14 using chloroplast transformation in Chlamydomonas indicated that substitution of D1 Trp-14 to Phe, mimicking Trp oxidation enhanced FtsH-mediated D1 degradation under high light, although the substitution did not affect protein stability and PSII activity. Molecular dynamics simulation of PSII implies that both Trp-14 oxidation and Phe substitution cause fluctuation of D1 N-terminal tail. Furthermore, Trp-14 to Phe modification appeared to have an additive effect in the interaction between FtsH and PSII core in vivo. Together, our results suggest that the Trp oxidation at its N-terminus of D1 may be one of the key oxidations in the PSII repair, leading to processive degradation by FtsH.
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spelling pubmed-106650152023-11-21 Characterization of tryptophan oxidation affecting D1 degradation by FtsH in the photosystem II quality control of chloroplasts Kato, Yusuke Kuroda, Hiroshi Ozawa, Shin-Ichiro Saito, Keisuke Dogra, Vivek Scholz, Martin Zhang, Guoxian de Vitry, Catherine Ishikita, Hiroshi Kim, Chanhong Hippler, Michael Takahashi, Yuichiro Sakamoto, Wataru eLife Plant Biology Photosynthesis is one of the most important reactions for sustaining our environment. Photosystem II (PSII) is the initial site of photosynthetic electron transfer by water oxidation. Light in excess, however, causes the simultaneous production of reactive oxygen species (ROS), leading to photo-oxidative damage in PSII. To maintain photosynthetic activity, the PSII reaction center protein D1, which is the primary target of unavoidable photo-oxidative damage, is efficiently degraded by FtsH protease. In PSII subunits, photo-oxidative modifications of several amino acids such as Trp have been indeed documented, whereas the linkage between such modifications and D1 degradation remains elusive. Here, we show that an oxidative post-translational modification of Trp residue at the N-terminal tail of D1 is correlated with D1 degradation by FtsH during high-light stress. We revealed that Arabidopsis mutant lacking FtsH2 had increased levels of oxidative Trp residues in D1, among which an N-terminal Trp-14 was distinctively localized in the stromal side. Further characterization of Trp-14 using chloroplast transformation in Chlamydomonas indicated that substitution of D1 Trp-14 to Phe, mimicking Trp oxidation enhanced FtsH-mediated D1 degradation under high light, although the substitution did not affect protein stability and PSII activity. Molecular dynamics simulation of PSII implies that both Trp-14 oxidation and Phe substitution cause fluctuation of D1 N-terminal tail. Furthermore, Trp-14 to Phe modification appeared to have an additive effect in the interaction between FtsH and PSII core in vivo. Together, our results suggest that the Trp oxidation at its N-terminus of D1 may be one of the key oxidations in the PSII repair, leading to processive degradation by FtsH. eLife Sciences Publications, Ltd 2023-11-21 /pmc/articles/PMC10665015/ /pubmed/37986577 http://dx.doi.org/10.7554/eLife.88822 Text en © 2023, Kato, Kuroda, Ozawa et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Plant Biology
Kato, Yusuke
Kuroda, Hiroshi
Ozawa, Shin-Ichiro
Saito, Keisuke
Dogra, Vivek
Scholz, Martin
Zhang, Guoxian
de Vitry, Catherine
Ishikita, Hiroshi
Kim, Chanhong
Hippler, Michael
Takahashi, Yuichiro
Sakamoto, Wataru
Characterization of tryptophan oxidation affecting D1 degradation by FtsH in the photosystem II quality control of chloroplasts
title Characterization of tryptophan oxidation affecting D1 degradation by FtsH in the photosystem II quality control of chloroplasts
title_full Characterization of tryptophan oxidation affecting D1 degradation by FtsH in the photosystem II quality control of chloroplasts
title_fullStr Characterization of tryptophan oxidation affecting D1 degradation by FtsH in the photosystem II quality control of chloroplasts
title_full_unstemmed Characterization of tryptophan oxidation affecting D1 degradation by FtsH in the photosystem II quality control of chloroplasts
title_short Characterization of tryptophan oxidation affecting D1 degradation by FtsH in the photosystem II quality control of chloroplasts
title_sort characterization of tryptophan oxidation affecting d1 degradation by ftsh in the photosystem ii quality control of chloroplasts
topic Plant Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10665015/
https://www.ncbi.nlm.nih.gov/pubmed/37986577
http://dx.doi.org/10.7554/eLife.88822
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