Structure of the red-shifted Fittonia albivenis photosystem I

Abstract

Photosystem I (PSI) from Fittonia albivenis, an Acanthaceae ornamental plant, is notable among green plants for its red-shifted emission spectrum. Here, we solved the structure of a PSI-light harvesting complex I (LHCI) supercomplex from F. albivenis at 2.46-Å resolution using cryo-electron microscopy. The supercomplex contains a core complex of 14 subunits and an LHCI belt with four antenna subunits (Lhca1-4) similar to previously reported angiosperm PSI-LHCI structures; however, Lhca3 differs in three regions surrounding a dimer of low-energy chlorophylls (Chls) termed red Chls, which absorb far-red beyond visible light. The unique amino acid sequences within these regions are exclusively shared by plants with strongly red-shifted fluorescence emission, suggesting candidate structural elements for regulating the energy state of red Chls. These results provide a structural basis for unraveling the mechanisms of light harvest and transfer in PSI-LHCI of under canopy plants and for designing Lhc to harness longer-wavelength light in the far-red spectral range.

Fig. 1. Spectral characteristics of several shade plants, Acanthaceae plants, and Arabidopsis thaliana.

a Low-temperature (77-K) fluorescence emission spectra of Arabidopsis thaliana (At), three understory traditional Chinese medicine plants (P. ginseng, P. notoginseng and D. nobile) and two houseplants (E. aureum and F. albivenis [Fa]). b Wavelength of maximum fluorescence emission (λ_max) of the plant species from (a) Error bars (standard deviation) were calculated from three different experimental units (n = 3 independent experiments), and data were presented as mean values ± SD. c The absorption spectra of leaves from At, Ea and Fa. The absorption spectra were normalized to the maximum in the red region, which was set to 1. The differential absorption spectrum between Fa and At is shown as a dashed line. d, e 77-K fluorescence emission spectra of chloroplast (d) and thylakoid membranes (e) from Arabidopsis and Fa. f Absorption spectra at room temperature of At thylakoids and Fa thylakoids. The differential absorption spectrum between Fa thylakoids and At thylakoids (multiplied by 5) is shown as a dashed line, with peaks at 456.5 nm, 488.5 nm, 650 nm, and 693.5 nm and the shoulder at 718 nm indicated by arrows. g 77-K fluorescence emission spectra of the ten Acanthaceae plants Fa, S. cusia, J. brandegeeana, P. curviflorus, B. cristata, R. tuberosa, C. infundibuliformis, H. phyllostachya, A. squarrosa and A. paniculata. h Wavelength of maximum fluorescence emission for plants shown in g Error bars (standard deviation) were calculated from three different experimental units (n = 3 independent experiments), and data were presented as mean values ± SD. The fluorescence emission spectra were collected following excitation at 440 nm and normalized with respect to their wavelength at maximal emission in the far-red region (750 nm), which was set to 1. The data are based on three independent experiments, each producing similar results.

Fig. 2. Overall architecture of the F. albivenis PSI–LHCI supercomplex.

a, b View along the membrane normal from the stromal side (a) and along the membrane plan from the LHCI side (b). Protein subunits are shown as ribbon models and colored differently. c Pigment arrangement in the Fa PSI–LHCI supercomplex. Chls are shown as stick models in the same color as their interacting protein subunits in a, and carotenoids are shown as stick models in light blue. d Distribution of lipids in Fa PSI–LHCI. Five phosphatidyl glycerol molecules (PG, green), three monogalatosyl diglyceride molecules (MGDG, blue) and one digalactosyl diacylglycerol molecule (DGDG, magenta) are depicted as stick models. e, f Overlay of the Fa PSI–LHCI structure (PDB code 8WGH, red) with that of maize PSI–LHCI (Zm PSI–LHCI, PDB code 5ZJI, light blue), At PSI–LHCI (PDB code 8J7B, smudge) and pea PSI–LHCI (Ps PSI–LHCI, PDB code 4XK8, gray; 5L8R, tv_blue; 7DKZ, yellow) based on PsaA viewed along the membrane normal from the stromal side, with the protein structure and the chlorophyll arrangement shown in (e) and f, respectively. In c and f, the phytol chains of all Chls have been deleted for clarity.

Fig. 3. Structures of F. albivenis Lhcas and Lhcas from other land plants.

a Structure of Lhca1, Lhca2, Lhca3 and Lhca4 from F. albivenis. Each Lhca is shown as ribbon model with the same color code as in Fig. 2a. Color codes: gray, Chls a; blue, Chls b; orange, carotenoids. b, c Overlay of each of the four Fa Lhca apoprotein structures (PDB code 8WGH, red) (b) and pigment arrangement (c) and the corresponding structures from maize PSI–LHCI (PDB code 5ZJI, light blue) and pea PSI–LHCI (PDB code 4XK8, gray; 5L8R, tv_blue; 7DKZ, yellow). d Superposition of the LHCI belt based on Lhca3 between the six land plants PSI–LHCI structures. Shifts between helix C_{Fa Lhca1} and helix C_{maize/pea/At Lhca1} are enlarged. The structure of PSI–LHCI from Arabidopsis thaliana is also included (PDB code 8J7B, smudge).

Fig. 4. Pigments and coordination of the red Chl a303 and red Chl a309 in F. albivenis Lhcas.

Dashed boxes represent the enlarged views showing amino acids as ligands for the central Mg of Chl a303 and Chl a309. Color codes: purple, Red Chls a; orange, other Chls a; blue, Chl b; yellow, carotenoids.

Fig. 5. Structural comparison of the local environment around Chl a303 and Chl a309 in F. albivenis Lhca3 and their counterpart in pea Lhca3 and maize Lhca3.

a Structure of Fa Lhca3 showing the extent of surface hydrophobicity. The degree of hydrophobicity is shown from white (no hydrophobicity) to red (high hydrophobicity). The black dashed boxes indicate three regions (I, II and III) surrounding Chl a303 and Chl a309, with different amino acid residues between Fa Lhca3, pea (Pisum sativum, Ps) Lhca3 and maize (Zea mays, Zm) Lhca3. b Enlarged views of boxed areas I–III) in Fa Lhca3 and the structure of the corresponding area in Ps Lhca3 and Zm Lhca3. c Sequence alignment of regions I–III from Fa Lhca3, Ps Lhca3 and Zm Lhca3. Color codes: Chl a303 and Chls a309, green; other Chl molecules, purple. PDB codes: Fa PSI–LHCI, 8WGH; Ps Lhca3, 4XK8; Zm Lhca3, 5ZJI.