Isolation and characterization of a large photosystem I–light‐harvesting complex II supercomplex with an additional Lhca1–a4 dimer in Arabidopsis

Abstract

The biological conversion of light energy into chemical energy is performed by a flexible photosynthetic machinery located in the thylakoid membranes. Photosystems I and II (PSI and PSII) are the two complexes able to harvest light. PSI is the last complex of the electron transport chain and is composed of multiple subunits: the proteins building the catalytic core complex that are well conserved between oxygenic photosynthetic organisms, and, in green organisms, the membrane light-harvesting complexes (Lhc) necessary to increase light absorption. In plants, four Lhca proteins (Lhca1-4) make up the antenna system of PSI, which can be further extended to optimize photosynthesis by reversible binding of LHCII, the main antenna complex of photosystem II. Here, we used biochemistry and electron microscopy in Arabidopsis to reveal a previously unknown supercomplex of PSI with LHCII that contains an additional Lhca1-a4 dimer bound on the PsaB-PsaI-PsaH side of the complex. This finding contradicts recent structural studies suggesting that the presence of an Lhca dimer at this position is an exclusive feature of algal PSI. We discuss the features of the additional Lhca dimer in the large plant PSI-LHCII supercomplex and the differences with the algal PSI. Our work provides further insights into the intricate structural plasticity of photosystems.

Developmental acclimation of the thylakoid proteome to light intensity in Arabidopsis

“…Unlike PSII, where changes in antenna size have been consistently observed, the LHCI antenna size of PSI has been reported to be unaffected by changes in light intensity in some studies (Ballottari et al ., 2007; Albanese et al ., 2018), but altered in another (Bailey et al ., 2001). Indeed, a recent study showed that PSI in Arabidopsis can bind additional copies of LHCA1 and 4 (Crepin et al ., 2020), suggesting the antenna size can undergo acclimation. Consistent with this suggestion, we observed a 10–20% increase in LHCA1 and 3 in LL compared to ML but no significant change in HL (Figure 2c).…”

Beyond ‘seeing is believing’: the antenna size of the photosystems in vivo

“…are not observed in the structures but are present in the membranes, but their exact position is unknown. The Lhca1 and Lhca4 observed by Crepin et al (2020) in some of the PSI particles are represented in lighter shades of green. The arrows indicate the locations of PSII and PSI in the grana and stroma lamellae, respectively.…”

“…The Lhca1 and Lhca4 observed by Crepin et al . (2020) in some of the PSI particles are represented in lighter shades of green. The arrows indicate the locations of PSII and PSI in the grana and stroma lamellae, respectively.…”

“…All other Lhcas are not able to substitute for each other, and the absence of one of the subunits was shown to leave a ‘hole’ in the structure, indicating that the docking sites are specific for each complex (Wientjes et al ., 2009). However, recently a PSI particle containing one additional Lhca1–4 dimer was reported (Crepin et al ., 2020). This dimer is located on the side of the core, opposite to LHCII, a position that in C. reinhardtii is partially occupied by Lhca2 and Lhca9 (Suga et al ., 2019) and that was supposed to be accessible only in green algae.…”

Composition, phosphorylation and dynamic organization of photosynthetic protein complexes in plant thylakoid membrane

“…Interestingly, an additional Lhca1/Lhca4 dimer bound to PsaH side was recently found in Arabidopsis. 78 (For a recent review on the supercomplex diversity, see ref. 79 and 80.)…”