Dynamics and mechanism of light harvesting in UV photoreceptor UVR8

Xiankun Li, Zheyun Liu, Haisheng Ren, Mainak Kundu, Lijuan Wang, Jiali Gao, Dongping Zhong

Research output: Contribution to journalArticlepeer-review

Abstract

Photosynthetic pigments form light-harvesting networks to enable nearly perfect quantum efficiency in photosynthesis via excitation energy transfer. However, similar light-harvesting mechanisms have not been reported in light sensing processes in other classes of photoreceptors during light-mediated signaling. Here, based on our earlier report, we mapped out a striking energy-transfer network composed of 26 structural tryptophan residues in the plant UV-B photoreceptor UVR8. The spectra of the tryptophan chromophores are tuned by the protein environments, funneling all excitation energy to a cluster of four tryptophan residues, a pyramid center, where the excitation-induced monomerization is initiated for cell signaling. With extensive site-directed mutagenesis, various time-resolved fluorescence techniques, and combined QM/MM simulations, we determined the energy-transfer rates for all donor-acceptor pairs, revealing the time scales from tens of picoseconds to nanoseconds. The overall light harvesting quantum efficiency by the pyramid center is significantly increased to 73%, compared to a direct excitation probability of 35%. UVR8 is the only photoreceptor discovered so far using a natural amino-acid tryptophan without utilizing extrinsic chromophores to form a network to carry out both light harvesting and light perception for biological functions.

Original languageEnglish (US)
Pages (from-to)12553-12569
Number of pages17
JournalChemical Science
Volume11
Issue number46
DOIs
StatePublished - Dec 14 2020

Bibliographical note

Funding Information:
We thank Prof. Yigong Shi (Tsinghua University) for generously providing the UVR8 plasmid, Prof. Maria-Elisabeth Michel-Beyerle (Nanyang Technological University) for stimulating discussions. This work was supported in part by the National Institute of Health (Grant GM118332 to DZ for experiments and GM46736 to JG for computation) and the National Natural Science Foundation of China (for support of collaboration effort of a visit of XL and DZ to Shanghai Jiao Tong University and Grant No. 21533003 to JG for support of HR to complete computational work).

Publisher Copyright:
© The Royal Society of Chemistry.

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