Antenna arrangement and energy-transfer pathways of PSI\u2013LHCI from the moss Physcomitrella patens

Qiujing Yan,Xiong Pi,Lingpeng Cheng,Wenda Wang,Tingyun Kuang,Jie Wang,Xiaochun Qin,Sen-Fang Sui,Yi-Kun He,Jian-Ren Shen,Guangye Han,Liang Zhao

doi:10.1038/s41421-021-00242-9

Abstract

Plants harvest light energy utilized for photosynthesis by light-harvesting complex I and II (LHCI and LHCII) surrounding photosystem I and II (PSI and PSII), respectively. During the evolution of green plants, moss is at an evolutionarily intermediate position from aquatic photosynthetic organisms to land plants, being the first photosynthetic organisms that landed. Here, we report the structure of the PSI–LHCI supercomplex from the moss Physcomitrella patens (Pp) at 3.23 Å resolution solved by cryo-electron microscopy. Our structure revealed that four Lhca subunits are associated with the PSI core in an order of Lhca1–Lhca5–Lhca2–Lhca3. This number is much decreased from 8 to 10, the number of subunits in most green algal PSI–LHCI, but the same as those of land plants. Although Pp PSI–LHCI has a similar structure as PSI–LHCI of land plants, it has Lhca5, instead of Lhca4, in the second position of Lhca, and several differences were found in the arrangement of chlorophylls among green algal, moss, and land plant PSI–LHCI. One chlorophyll, PsaF–Chl 305, which is found in the moss PSI–LHCI, is located at the gap region between the two middle Lhca subunits and the PSI core, and therefore may make the excitation energy transfer from LHCI to the core more efficient than that of land plants. On the other hand, energy-transfer paths at the two side Lhca subunits are relatively conserved. These results provide a structural basis for unravelling the mechanisms of light-energy harvesting and transfer in the moss PSI–LHCI, as well as important clues on the changes of PSI–LHCI after landing.

Highlights

Photosynthesis harvests and converts light energy from the sun into chemical energy that sustains almost all life activities on the earth
Purification and characterization of P. patens photosystem I (PSI)–LHCI Photosynthetic pigment-protein complexes were isolated from P. patens by anion-exchange chromatography and sucrose density gradient ultracentrifugation, and a dark green band in the lower part of the gradient was identified as PSI–LHCI by SDS-PAGE
It is notable that the fluorescence emission peak of Physcomitrella patens (Pp) PSI–LHCI is redshifted as compared with the peak of PSI–LHCI (709 nm) from a green algae B. corticulans, and is blue-shifted as compared with the peak of PSI–LHCI (735 nm) from a land plant P. sativum (Supplementary Fig. S1e)

Summary

Introduction

Photosynthesis harvests and converts light energy from the sun into chemical energy that sustains almost all life activities on the earth. PSI cores from eukaryotic algae and higher plants exist as a monomer, which is associated with various membrane-spanning light-harvesting. The structures of PSI–LHCI supercomplexes have been solved from various eukaryotic organisms such as red algae[6], diatoms[7,8], green algae[9,10,11], and land plants[12,13,14] These studies showed that the PSI core is relatively conserved during more than 2.5 billion years of evolution, whereas there is a large diversity in the pigment and protein compositions of LHCI from different organisms[15]. The distinct structural differences between aquatic green algae and land plants may be a result of adaptation to different light environments that different organisms experience[15]

Methods

Results

Conclusion