Title: A novel protein domain is important for photosystem II complex assembly and photoautotrophic growth in angiosperms

Wei Li, Jiangfan Guo, Xue Han, Xiaowen Da, Kai Wang, Hongfei Zhao, Shi-Tang Huang, Bosheng Li, Hang He, Ruirui Jiang, Shichen Zhou, Peng Yan, Tao Chen, Yi He, Jiming Xu, Yu Liu, Yunrong Wu, Huixia Shou, Zhongchang Wu, Chuanzao Mao, Xiaorong Mo

Published: December 23, 2022

DOI: https://doi.org/10.1016/j.molp.2022.12.016

Abstract

Photosystem II (PSII) is a multisubunit protein complex of the photosynthetic electron transport chain that is vital to photosynthesis. Although the structure, composition, and function of PSII are well understood, its mechanism of biogenesis remains largely elusive. THYLAKOID RHODANESE-LIKE (TROL) provides an anchor for leaf-type ferredoxin:NADP+ oxidoreductase (LFNR). Here, we identified a second type THYLAKOID RHODANESE-LIKE (TROL) protein, TROL2, encoded by seed plant genomes whose function has not previously been reported. We show that TROL2 is a photosystem II (PSII) assembly cofactor with essential roles in the establishment of photoautotrophy. TROL2 contains a 45-amino-acid domain, which we termed the CLS (chlorotic lethal seedling) domain, that is both necessary and sufficient for TROL2 function in PSII assembly and photoautotrophic growth. Based on a phylogenetic analyses, we hypothesize that TROL2 arose from ancestral TROL1 via gene duplication before the emergence of seed plants and acquired the CLS domain via evolution of the sequence encoding its N-terminal portion. We further revealed that TROL2 (or CLS) forms an assembly cofactor complex with the intrinsic thylakoid membrane protein LOW PSII ACCUMULATION2 (LPA2) and interacts with small PSII subunits to facilitate PSII complex assembly. In conclusion, we report that TROL2 (CLS) is essential for photoautotrophy in angiosperms and reveal its mechanistic role in PSII complex assembly, shedding light on both the molecular mechanism of photosynthetic complex assembly and the evolution of angiosperms.

Link:  https://www.cell.com/molecular-plant/fulltext/S1674-2052(22)00451-8