Cargando…
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...
Autores principales: | , , , , , , , , , , , , |
---|---|
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 |
_version_ | 1785148827459649536 |
---|---|
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. |
format | Online Article Text |
id | pubmed-10665015 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | eLife Sciences Publications, Ltd |
record_format | MEDLINE/PubMed |
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 |
work_keys_str_mv | AT katoyusuke characterizationoftryptophanoxidationaffectingd1degradationbyftshinthephotosystemiiqualitycontrolofchloroplasts AT kurodahiroshi characterizationoftryptophanoxidationaffectingd1degradationbyftshinthephotosystemiiqualitycontrolofchloroplasts AT ozawashinichiro characterizationoftryptophanoxidationaffectingd1degradationbyftshinthephotosystemiiqualitycontrolofchloroplasts AT saitokeisuke characterizationoftryptophanoxidationaffectingd1degradationbyftshinthephotosystemiiqualitycontrolofchloroplasts AT dogravivek characterizationoftryptophanoxidationaffectingd1degradationbyftshinthephotosystemiiqualitycontrolofchloroplasts AT scholzmartin characterizationoftryptophanoxidationaffectingd1degradationbyftshinthephotosystemiiqualitycontrolofchloroplasts AT zhangguoxian characterizationoftryptophanoxidationaffectingd1degradationbyftshinthephotosystemiiqualitycontrolofchloroplasts AT devitrycatherine characterizationoftryptophanoxidationaffectingd1degradationbyftshinthephotosystemiiqualitycontrolofchloroplasts AT ishikitahiroshi characterizationoftryptophanoxidationaffectingd1degradationbyftshinthephotosystemiiqualitycontrolofchloroplasts AT kimchanhong characterizationoftryptophanoxidationaffectingd1degradationbyftshinthephotosystemiiqualitycontrolofchloroplasts AT hipplermichael characterizationoftryptophanoxidationaffectingd1degradationbyftshinthephotosystemiiqualitycontrolofchloroplasts AT takahashiyuichiro characterizationoftryptophanoxidationaffectingd1degradationbyftshinthephotosystemiiqualitycontrolofchloroplasts AT sakamotowataru characterizationoftryptophanoxidationaffectingd1degradationbyftshinthephotosystemiiqualitycontrolofchloroplasts |