The xanthophyll cycle affects reversible interactions between PsbS and light-harvesting complex II to control non-photochemical quenching

Abstract

To maintain high photosynthetic rates, plants must adapt to their light environment on a timescale of seconds to minutes. Therefore, the light-harvesting antenna system of photosystem II in thylakoid membranes, light-harvesting complex II (LHCII), has a feedback mechanism, which determines the proportion of absorbed energy dissipated as heat: non-photochemical chlorophyll fluorescence quenching (NPQ). This is crucial to prevent photo-oxidative damage to photosystem II (PSII) and is controlled by the transmembrane pH differences (ΔpH). High ΔpH activates NPQ by protonation of the protein PsbS and the enzymatic de-epoxidation of LHCII-bound violaxanthin to zeaxanthin. But the precise role of PsbS and its interactions with different LHCII complexes remain uncertain. We have investigated PsbS-LHCII interactions in native thylakoid membranes using magnetic-bead-linked antibody pull-downs. The interaction of PsbS with the antenna system is affected by both ΔpH and the level of zeaxanthin. In the presence of ΔpH alone, PsbS is found to be mainly associated with the trimeric LHCII protein polypeptides, Lhcb1, Lhcb2 and Lhcb3. However, a combination of ΔpH and zeaxanthin increases the proportion of PsbS bound to the minor LHCII antenna complex proteins Lhcb4, Lhcb5 and Lhcb6. This pattern of interaction is not influenced by the presence of PSII reactions centres. Similar to LHCII particles in the photosynthetic membrane, PsbS protein forms clusters in the NPQ state. NPQ recovery in the dark requires uncoupling of PsbS. We suggest that PsbS acts as a 'seeding' centre for the LHCII antenna rearrangement that is involved in NPQ.

Photosystem II 22kDa protein level ‐ a prerequisite for excess light‐inducible memory, cross‐tolerance to UV‐C and regulation of electrical signalling

“…The role of the PsbS protein and NPQ mechanism has been recently studied. At the molecular level, it is responsible for proper antennae remodelling during strongly variable light conditions (Correa‐Galvis, Poschmann, Melzer, Stühler, & Jahns, ), and possibly acts through interaction with LHCII antenna proteins, in a ΔpH‐ and zeaxanthin‐dependent manner (Sacharz, Giovagnetti, Ungerer, Mastroianni, & Ruban, ); however, the exact molecular mechanism for this remains unknown. Null mutants in the PsbS gene ( npq4‐1 ) have been obtained and characterized (Li et al, ; Niyogi et al, ).…”

Dynamic non‐photochemical quenching in plants: from molecular mechanism to productivity

“…While the xanthophyll cycle plays a role of a light memory for antenna pushing it into more protective aggregated state, unpigmented protein PsbS is a seeding centre of this aggregation and, most importantly, a factor that could rapidly disaggregate LHCII (Ruban, ). The latter is achieved by reversible, proton‐induced monomerization of the normally dimeric in the dark protein (Bergantino et al , ; Teardo et al , ; Correa‐Galvis et al , ; Sacharz et al , ). Monomers of PsbS gain higher affinity of binding to LHCII, sending it a structural message that triggers conformational change into the photoprotective mode and subsequent aggregation (Johnson et al , ).…”

“…Monomers of PsbS gain higher affinity of binding to LHCII, sending it a structural message that triggers conformational change into the photoprotective mode and subsequent aggregation (Johnson et al , ). Interestingly, the presence of zeaxanthin was discovered to enhance PsbS binding to LHCII (Sacharz et al , ). In addition, plants overexpressing PsbS were found to have increased population of mobile LHCII that was destined for aggregation and qE (Goral et al , ).…”

The Impacts of Fluctuating Light on Crop Performance

“…qE is initiated when protons accumulate in the lumen, thereby reducing the lumen pH. PsbS, a protein associated with PSII, senses the low pH and signals a conformation change in the LHCII protein (Li et al, 2000;Sacharz et al, 2017). This conformational change occurs in concert with the xanthophyll cycle, through which violaxanthin is converted to zeaxanthin by violaxanthin deepoxidase in high light (Demmig-Adams, 1990).…”