LHC-like Proteins: The Guardians of Photosynthesis

Abstract

The emergence of chlorophyll-containing light-harvesting complexes (LHCs) was a crucial milestone in the evolution of photosynthetic eukaryotic organisms. Light-harvesting chlorophyll-binding proteins form complexes in proximity to the reaction centres of photosystems I and II and serve as an antenna, funnelling the harvested light energy towards the reaction centres, facilitating photochemical quenching, thereby optimizing photosynthesis. It is now generally accepted that the LHC proteins evolved from LHC-like proteins, a diverse family of proteins containing up to four transmembrane helices. Interestingly, LHC-like proteins do not participate in light harvesting to elevate photosynthesis activity under low light. Instead, they protect the photosystems by dissipating excess energy and taking part in non-photochemical quenching processes. Although there is evidence that LHC-like proteins are crucial factors of photoprotection, the roles of only a few of them, mainly the stress-related psbS and lhcSR, are well described. Here, we summarize the knowledge gained regarding the evolution and function of the various LHC-like proteins, with emphasis on those strongly related to photoprotection. We further suggest LHC-like proteins as candidates for improving photosynthesis in significant food crops and discuss future directions in their research.

Keywords: light-harvesting; non-photochemical quenching; photoinhibition; photoprotection; photosynthesis.

Figure 1

Photosynthesis during HL and suggested photoprotective roles of LHC-like proteins. Light is harvested in the LHC and directed to PSII RC, where it excites a specialized chlorophyll-pair (P680) and initiates charge separation and linear electron flow (LEF). Electrons are transferred from PSII-RC via QA to QB that then join the plastoquinone (PQ) pool. From PQ, the electrons move to cytochrome b6f, PSI, and ferredoxin NADPH reductase (FNR) (not shown). FNR reduces NADP+ to NADPH, which is further utilized for carbon-fixation reaction via the Calvin–Benson–Bassham cycle. During HL, PSI and PSII are saturated with energy. The continuous photosynthesis facilitates a proton gradient between the lumen of the thylakoid and the stroma of the chloroplast due to the splitting of water and import of protons via the PQ pool and cytochrome b6f. This lumen acidification leads to protonation of protonable residues in psbS (mostly plants and mosses) and lhcSR (algae and mosses). In response, the pigment-less psbS interacts and activates NPQ in the LHCII subunit CP29. lhcSR binds lutein and chlorophyll and can act as a sinkhole for excess energy in the LHC. Thus, it can receive and scavenge excess energy from LHCII. When the light energy exceeds the amount that could be used for photochemistry, excited chlorophylls in the LHCs and RCs may dissipate the excess energy as heat via interactions with other chlorophylls or carotenoids. During HL, the xanthophyll cycle is activated: violaxanthin is de-epoxidated by VDE to zeaxanthin (via antheraxanthin), which in turn acts to relax excited chlorophylls and prevent ROS formation. Remaining excess energy excites chlorophyll to a triplet state where it reacts with O₂ to form ROS. The ROS then interacts with and damages the photosynthetic reaction centres and LHC subunits, leading to photoinhibition. It is suggested that SEPs/Lils and ELIPs serve as a temporary reservoir for the chlorophylls of the damaged proteins during their turnover (see also Figure 2).

Figure 2

Suggested roles of HLIP/OHP, ELIPs and SEP/Lil in the PSII repair cycle. During HL, generated ROS damages mainly the PSII reaction centre protein D1, followed by D2, and then the LHCII subunits. Chlorophylls from the damaged reaction centres and LHC are transferred to OHP1 or ELIP and SEP/Lil, respectively, while the damaged proteins are degraded. During this time, the energy of excited chlorophylls is quenched via carotenoids. Once newly synthesized subunits are incorporated and PSII reassembled, chlorophylls are transferred back to the reaction centre to harvest light for photosynthesis. It is important to note that ELIPs, SEPs and OHPs are most certainly involved in regulation of other mechanisms, including chlorophyll and carotenoid biosynthesis.

Figure 3

LHCII and LHC-like proteins share vast structural similarities. (a) The known structure of LHCII (taken from pdb id: 6KAF) is shown in green. The structure models of LHC-like proteins as predicted by Swiss model. (b) OHP1 and psbS predicted models superimposed on the known LHCII structure. Note the overlapping of the two conserved TM helices in OHP, LHCI and psbS. All models (including OHP and SEP) were predicted with Arabidopsis thaliana sequences of the relevant proteins except lhcSR. The lhcSR model was predicted with C. reinhardtii sequence. The predicted structures are coloured by hydrophobicity: red indicates hydrophobic regions and blue indicates hydrophilic regions.

Figure 4

Suggested evolution of LHC and LHC-like proteins. HLIP was first introduced to eukaryotes via primary endosymbiosis and acquired a signal peptide when its gene transferred to the nuclear genome. OHP1-like protein gave rise to a pool of different SEPs. OHP2 is likely a consequence of a gene-deletion event of SEP while a small portion remains and acts as a membrane anchor. Different SEPs evolved into LHCs, ELIPs and psbS.

Figure 5

Proposed quenching mechanisms for psbS, lhcSR, and C. ohadii CBR. HL conditions promote thylakoid lumen acidification. psbS (mainly in plants) is protonated at conserved Glu residues (indicated by pink arrows) and undergoes conformational shift before interacting with and activating energy quenching in the LHCII subunit CP29 (top). lhcSR is protonated at conserved Glu and Asp residues and also undergoes conformational shift and interacts with LHCII subunits. Excess energy can be transferred to lhcSR, where it is quenched via carotenoids (middle). The mechanism of CBR is unknown, yet evidence points to a conserved Glu residue with the same location of one of the proton-sensing Glutamates of psbS, suggesting a possibility in which CBR acts as a substitute for psbS and lhcSR in the highly light-tolerant C. ohadii (Levin et al., 2022) [27]. Figure adapted and modified from Pinnola., 2019 [23] LHCII and PSII core structures were taken from pdb id: 6KAF.