FZL, a dynamin-like protein localized to curved grana edges, is required for efficient photosynthetic electron transfer in Arabidopsis

Yu Ogawa; Megumi Iwano; Toshiharu Shikanai; Wataru Sakamoto

doi:10.3389/fpls.2023.1279699

FZL, a dynamin-like protein localized to curved grana edges, is required for efficient photosynthetic electron transfer in Arabidopsis

Front Plant Sci. 2023 Sep 28:14:1279699. doi: 10.3389/fpls.2023.1279699. eCollection 2023.

Authors

Yu Ogawa¹, Megumi Iwano², Toshiharu Shikanai³, Wataru Sakamoto¹

Affiliations

¹ Institute of Plant Science and Resources, Okayama University, Kurashiki, Japan.
² Graduate School of Biostudies, Kyoto University, Kyoto, Japan.
³ Department of Botany, Graduate School of Science, Kyoto University, Kyoto, Japan.

Abstract

Photosynthetic electron transfer and its regulation processes take place on thylakoid membranes, and the thylakoid of vascular plants exhibits particularly intricate structure consisting of stacked grana and flat stroma lamellae. It is known that several membrane remodeling proteins contribute to maintain the thylakoid structure, and one putative example is FUZZY ONION LIKE (FZL). In this study, we re-evaluated the controversial function of FZL in thylakoid membrane remodeling and in photosynthesis. We investigated the sub-membrane localization of FZL and found that it is enriched on curved grana edges of thylakoid membranes, consistent with the previously proposed model that FZL mediates fusion of grana and stroma lamellae at the interfaces. The mature fzl thylakoid morphology characterized with the staggered and less connected grana seems to agree with this model as well. In the photosynthetic analysis, the fzl knockout mutants in Arabidopsis displayed reduced electron flow, likely resulting in higher oxidative levels of Photosystem I (PSI) and smaller proton motive force (pmf). However, nonphotochemical quenching (NPQ) of chlorophyll fluorescence was excessively enhanced considering the pmf levels in fzl, and we found that introducing kea3-1 mutation, lowering pH in thylakoid lumen, synergistically reinforced the photosynthetic disorder in the fzl mutant background. We also showed that state transitions normally occurred in fzl, and that they were not involved in the photosynthetic disorders in fzl. We discuss the possible mechanisms by which the altered thylakoid morphology in fzl leads to the photosynthetic modifications.

Keywords: Arabidopsis; FUZZY ONION LIKE (FZL); chloroplast; photosynthetic electron transfer; thylakoid; thylakoid structure.

Grants and funding

This work was supported by KAKENHI (23H04959 and 21H02508 to WS), by JST Grant (the establishment of university fellowships towards the creation of science technology innovation, Grant Number JPMJFS2128), by Research Grant for Encouragement of Students, Graduate School of Environmental and Life Science, Okayama University, and by Ohara Foundation.