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Light-harvesting complex Lhcb9 confers a green alga-type photosystem I supercomplex to the moss Physcomitrella patens

Nature Plants volume 1, Article number: 14008 (2015) Cite this article

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Abstract

Light-harvesting complex (LHC) proteins in chloroplast thylakoid membranes not only transfer absorbed light energy to the two photosystems but also regulate the rate of energy transfer to avoid photodamage. Here we demonstrate that Lhcb9, a recently discovered LHC protein in the moss Physcomitrella patens, functions to connect LHC proteins with photosystem I (PSI), resulting in the formation of two different types of PSI supercomplexes in thylakoid membranes. We observed that the Lhcb9-containing PSI supercomplex is disassembled in response to excess light conditions. On the basis of our phylogenetic analysis, it appears that P. patens acquired Lhcb9 by horizontal gene transfer from the earlier green algal lineage, leading to the presence of both green alga-type and vascular plant-type PSI supercomplexes, which would have been crucial for conquering the dynamic environmental interface between aquatic and terrestrial conditions it faced during evolution.

Photosynthetic organisms capture solar energy to drive electron transport and generate reducing equivalents, a process that involves excitation of both PSI and PSII in chloroplast thylakoid membranes1. To maintain balanced excitation between PSI and PSII under changing light quality conditions, the light-harvesting complex of PSII (LHCII) controls the distribution of excitation energy between the two photosystems through so-called state transitions2,3. It has been suggested that phosphorylation of LHCII decreases and increases its affinity for PSII and PSI, respectively, resulting in its dissociation from PSII and association with PSI4–6. In addition, under excess light conditions that could lead to photodamage of thylakoid membrane proteins, LHCII functions to dissipate the excess excitation energy as heat, in a process termed non-photochemical quenching (qE)7,8. Although the detailed mechanism is not clearly understood, the transthylakoid pH gradient-dependent protonation of stress-related LHC9 and PSBS10 appears to induce reorganization of the PSII–LHCII supercomplex in algae11,12 and vascular plants13,14, respectively. Therefore, reorganization of the associated LHC proteins involving the two photosystems regulates excitation energy transfer among thylakoid membrane proteins to achieve optimal photosynthetic activity under a fluctuating natural light environment.

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Figure 1: Protein supercomplexes in P. patens thylakoid membranes.
Figure 2: Comparison of the protein compositions of the B3, B4 and B5 fractions obtained from WT and the ΔLhcb9 mutants.
Figure 3: Nickel affinity purification of Lhcb9.1-His.
Figure 4: Spectroscopy analysis of the functional antenna size of PSI–LHCI supercomplex.
Figure 5: Protein reorganization of PSI–LHCI supercomplex under high light conditions.
Figure 6: Evolutionary relationships of Lhcb9 among LHC proteins in photosynthetic eukaryotes.

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Acknowledgements

We are grateful to Dr Ichiro Terashima for fruitful discussion of the manuscript; Drs Mitsuyasu Hasebe and Yuji Hiwatashi for providing the P. patens WT strain and extensive technical advice on using the moss; Dr Hiroshi Abe for technical advice regarding cloning and gene construction; the Support Unit for Bio-Material Analysis, RIKEN BSI Research Resources Center, with special thanks to Kaori Otsuki, Masaya Usui and Aya Abe for MS; and Kaoru Kotoshiba and Hiroe Watanabe for technical support. This work was supported by JST PRESTO, JSPS KAKENHI Grant Number 23687008, and grants from RIKEN Center for Advanced Photonics, Extreme Photonics Research Project.

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Authors and Affiliations

  1. Live Cell Molecular Imaging Research Team, Extreme Photonics Research Group, RIKEN Center for Advanced Photonics, 2-1 Hirosawa, Wako, 351-0198, Saitama, Japan

    Masakazu Iwai & Akihiko Nakano

  2. PRESTO, Japan Science and Technology Agency (JST), Honcho, Kawaguchi, 332-0012, Saitama, Japan

    Masakazu Iwai

  3. Institute of Low Temperature Science, Hokkaido University, Sapporo, 060-0819, Hokkaido, Japan

    Makio Yokono

  4. Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Bunkyo-ku, 113-0033, Tokyo, Japan

    Masaru Kono, Ko Noguchi & Akihiko Nakano

  5. Molecular Photoscience Research Center, Kobe University, Kobe, 657-8501, Japan

    Seiji Akimoto

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  1. Masakazu Iwai
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Contributions

M.I. designed the study, constructed the transgenic plants, performed the genetic, biochemical and PAM experiments, analysed the data and wrote the paper; M.Y. and S.A. performed the time-resolved fluorescence spectroscopy experiments and analysed the data; M.Y. performed the phylogenetic analysis; M.K. and K.N. provided essential assistance for PAM experiments; and A.N. supervised the study.

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Correspondence to Masakazu Iwai.

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Iwai, M., Yokono, M., Kono, M. et al. Light-harvesting complex Lhcb9 confers a green alga-type photosystem I supercomplex to the moss Physcomitrella patens. Nature Plants 1, 14008 (2015). https://doi.org/10.1038/nplants.2014.8

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