Abstract
In plant grana thylakoid membranes Photosystem II (PSII) associates with a variable number of antenna proteins (LHCII) to form different types of supercomplexes (PSII-LHCII), whose organization is dynamically adjusted in response to light cues, with the C2S2 more abundant in high-light and the C2S2M2 in low-light. Paired PSII-LHCII supercomplexes interacting at their stromal surface from adjacent thylakoid membranes were previously suggested to mediate grana stacking. Here, we present the cryo-electron microscopy maps of paired C2S2 and C2S2M2 supercomplexes isolated from pea plants grown in high-light and low-light, respectively. These maps show a different rotational offset between the two supercomplexes in the pair, responsible for modifying their reciprocal interaction and energetic connectivity. This evidence reveals a different way by which paired PSII-LHCII supercomplexes can mediate grana stacking at diverse irradiances. Electrostatic stromal interactions between LHCII trimers almost completely overlapping in the paired C2S2 can be the main determinant by which PSII-LHCII supercomplexes mediate grana stacking in plants grown in high-light, whereas the mutual interaction of stromal N-terminal loops of two facing Lhcb4 subunits in the paired C2S2M2 can fulfil this task in plants grown in low-light. The high-light induced accumulation of the Lhcb4.3 protein in PSII-LHCII supercomplexes has been previously reported. Our cryo-electron microscopy map at 3.8 Å resolution of the C2S2 supercomplex isolated from plants grown in high-light suggests the presence of the Lhcb4.3 protein revealing peculiar structural features of this high-light-specific antenna important for photoprotection.
Highlights
Plants experience a highly fluctuating light environment, with irradiances varying seasonally, diurnally and spatially, at the level either of the plant canopy or the leaf
Electrostatic stromal interactions between light-harvesting complex II (LHCII) trimers almost completely overlapping in the paired C2S2 can be the main determinant by which Photosystem II (PSII)-LHCII supercomplexes mediate grana stacking in plants grown in high-light, whereas the mutual interaction of stromal N-terminal loops of two facing Lhcb4 subunits in the paired C2S2M2 can fulfil this task in plants grown in low-light
To investigate the effect of light intensity on the arrangement of paired PSII-LHCIIsc of different type and their stromal interaction within grana stacks, we purified paired PSII-LHCIIsc from pea plants grown in high-light (i.e., 750 μmol photons m−2 s−1, H) and low-light (i.e., 30 μmol photons m−2 s−1, L), where the C2S2 and the C2S2M2 are, respectively, the most abundant supercomplexes
Summary
Plants experience a highly fluctuating light environment, with irradiances varying seasonally, diurnally and spatially, at the level either of the plant canopy or the leaf. The amount and composition of the PSII-LHCIIsc in the thylakoid membranes are dynamically adjusted in response to changes in light intensity, with the C2S2 more abundant in high-light, whereas the C2S2M and C2S2M2 more represented at moderate and low-light, respectively [10,11,12] In this regard, a reduction of Lhcb, Lhcb and M-LHCII trimers bound to the PSII cores, in concomitance with an increase of Lhcb4.3 ( renamed Lhcb8 [13,14]), a specific high-light induced isoform of Lhcb4 [11,15,16,17], are the major players in the modulation of the PSII-LHCIIsc antenna size in plants long-term acclimated to increased light levels [10,11]. With regards to the light, these semi-crystalline arrays account for up to about 10–20% of the PSII-LHCIIsc particles in the grana of plants grown in low-light and show a markedly lower frequency under prolonged acclimation to increasing light intensities [10,19]
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