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

• Published in: eLife Vol. 12
• Main Authors: 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
• Format: Journal Article
• Language: English
• Published: Cambridge eLife Sciences Publications Ltd 21.11.2023; eLife Sciences Publication
• Subjects: Amino acids; Arabidopsis thaliana; Chlorophyll; Chloroplasts; Degradation; Electron transfer; Genetic transformation; Life Sciences; Light; Membranes; Molecular dynamics; N-Terminus; Oxidation; Peptides; photo-oxidative damage; Photosynthesis; Photosystem II; Post-translation; post-translational modification; protein degradation; Proteins; Quality control; Reactive oxygen species; Tryptophan; tryptophan oxidation
• ISSN: 2050-084X; 2050-084X
• DOI: 10.7554/eLife.88822

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.