A leap in quantum efficiency through light harvesting in photoreceptor UVR8

• Published in: Nature communications Vol. 11; no. 1; p. 4316
• Main Authors: Li, Xiankun, Ren, Haisheng, Kundu, Mainak, Liu, Zheyun, Zhong, Frank W., Wang, Lijuan, Gao, Jiali, Zhong, Dongping
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 28.08.2020; Nature Publishing Group; Nature Portfolio
• Subjects: 140/125; 631/57/2272/1590; 639/638/440/948; 639/638/440/949; Amino acids; Arabidopsis - metabolism; Arabidopsis - physiology; Arabidopsis - radiation effects; Arabidopsis Proteins - chemistry; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Chromosomal Proteins, Non-Histone - chemistry; Chromosomal Proteins, Non-Histone - genetics; Chromosomal Proteins, Non-Histone - metabolism; Computer applications; Dimers; Efficiency; Energy Transfer; Environmental regulations; Excitation; Fluorescence; Fluorescence spectroscopy; Funnels; Gene expression; Humanities and Social Sciences; Kinetics; Light; Models, Molecular; multidisciplinary; Mutation; Perception; Photoreceptors; Photoreceptors, Plant - chemistry; Photoreceptors, Plant - metabolism; Protein Conformation; Protein Multimerization; Quantum efficiency; Residues; Science; Science (multidisciplinary); Tryptophan; Tryptophan - metabolism; Ultraviolet Rays
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-020-17838-6

Plants utilize a UV-B (280 to 315 nm) photoreceptor UVR8 (UV RESISTANCE LOCUS 8) to sense environmental UV levels and regulate gene expression to avoid harmful UV effects. Uniquely, UVR8 uses intrinsic tryptophan for UV-B perception with a homodimer structure containing 26 structural tryptophan residues. However, besides 8 tryptophans at the dimer interface to form two critical pyramid perception centers, the other 18 tryptophans’ functional role is unknown. Here, using ultrafast fluorescence spectroscopy, computational methods and extensive mutations, we find that all 18 tryptophans form light-harvesting networks and funnel their excitation energy to the pyramid centers to enhance light-perception efficiency. We determine the timescales of all elementary tryptophan-to-tryptophan energy-transfer steps in picoseconds to nanoseconds, in excellent agreement with quantum computational calculations, and finally reveal a significant leap in light-perception quantum efficiency from 35% to 73%. This photoreceptor is the first system discovered so far, to be best of our knowledge, using natural amino-acid tryptophans to form networks for both light harvesting and light perception. Photoreceptor UVR8 in plants senses environmental UV levels through 26 structural tryptophan residues, but the role of 18 of them was unknown. The authors show, by experiments and computations, how these form a light-harvesting network that funnels the excitation to the pyramid centers enhancing the light-perception efficiency.