Project title: Photosynthetic Light Harvesting: Computational approaches to studying the relationship between light-harvesting, photochemistry, photo-damage, and repair
The project will look into the photoprotective switch in plants. The NPQ mechanism protects photosystem II (PSII) from photodamge by down-regulating the efficiency of light-harvesting in response to high light. It has recently been shown that NPQ is one of the factors defining plant growth and, ultimately, crop yield1. However, there is still considerable confusion over the molecular detail of the system and how this fits into the network of processes such as photosynthetic charge separation, photodamge, the PSII repair cycle.
This is a multiscale problem. The central mechanism of NPQ is the switching of the major PSII antenna complex, LHCII, between efficient (light-harvesting) and protective (dissipative) states2. The mechanics of this mechanism are still not clear although Duffy and co-workers have provided a theoretical model of the protective state, showing that dissipation occurs due to the capture of chlorophyll excitation energy by the LHCII carotenoids, followed by rapid dissipation of this energy as heat3, 4. However, the mechanism by which this pathway is activated/deactivated is essentially unknown.
The switch depends on several external factors: the transmembrane pH-gradient (developed by a high rate of water-splitting in high light)5, the hydrophobic, non-pigment binding protein PsbS6, and the xanthophyll cycle7. Additionally, aggregation of LHCII in the membrane is necessary for inducing NPQ8.
The appearance of LHCII proteins in the dissipative state, plus a rearrangement/aggregation of the PSII antenna, leads to a complete change of function of PSII, in which excess absorbed energy is now harmlessly dissipated as heat rather than being left to accumulate and damage the reaction centre.
We know that NPQ is important for defending the plant against high light (and therefore maintaining a healthy rate of photosynthesis and, ultimately, growth) but how this functions against a background of photosynthesis, damage and repair is unclear9. A recent discovery was made that gives a new picture of the NPQ mechanism: economic photoprotection. The fast-fluorescence induction measurements of Belgio and co-workers showed that the NPQ ‘traps’ (LHCII proteins that have switched to the protective state) are actually quite slow, only trapping energy once the reaction centres have become saturated but otherwise not interfering with the harvesting of energy. This is encapsulated by the phrase, ‘NPQ on protects reaction centres that need protecting’.
We therefore want a multiscale theoretical description of NPQ:
(1) How do carotenoid-chlorophyll interactions bring about the quenched state and, more importantly, how are these interactions controlled by the proteins?
(2) How does the protein switch between these two states? What are the key external factors?
(3) How does NPQ fit into the larger-scale operation of PSII photosynthesis? Is preventing damage more important than repairing it? To what extent is PSII yield determined by NPQ.
1 Kromdijk J, Głowacka K, Leonelli L, Gabilly ST, Iwai M, Niyogi KK, Long SP (2017) Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science 354, 857-861.
2 Duffy CD, Ruban AV (2015) Dissipative pathways in the photosystem-II antenna in plants. J Photochem Photobiol B 152, 215-226.
3 Chmeliov J, Bricker WP, Lo C, Duffy CDP (2015) An ‘all pigment’ model of excitation quenching in LHCII. Phys. Chem. Chem. Phys. 17, 15857-15867.
4 Fox KF, Balevičius Jr. V, Chmeliov J, Valkunas L, Ruban AV, Duffy CDP (2017) The carotenoid pathway: what is important for excitation quenching in plant antenna complexes?. Phys. Chem. Chem. Phys. 19, 22957-22968.
5 G. H. Krause, U. Behrend, ΔpH-dependent chlorophyll fluorescence quenching indicating a mechanism of protection against photoinhibition of chloroplasts. FEBS Lett. 200 (1986) 298-302.
6 A. Kiss , A. V. Ruban, P. Horton, The PsbS protein controls the organisation of the photosystem II antenna in higher plant thylakoid membranes. J. Biol. Chem. 283 (2008) 3972-3978.
7 G. Noctor, D. Rees, A. Young, P. Horton, The relationship between zeaxanthin, energy-dependent quenching of chlorophyll fluorescence, and trans-thylakoid pH gradient in isolated chloroplasts. Biochim. Biophys. Acta 1057 (1991) 320-330.
8 A. V. Ruban, D. Rees, A. A. Pascal, P. Horton, Mechanism of ΔpH-dependent dissipation of absorbed excitation energy by photosynthetic membranes II: the relationships between LHCII aggregation in vitro and qE in isolated thylakoids. Biochim. Biophys. Acta 1102 (1992) 39-44.