Light-induced Dissociation of an Antenna Hetero-oligomer Is Needed for Non-photochemical Quenching Induction

Abstract

PsbS plays a major role in activating the photoprotection mechanism known as "non-photochemical quenching," which dissipates chlorophyll excited states exceeding the capacity for photosynthetic electron transport. PsbS activity is known to be triggered by low lumenal pH. However, the molecular mechanism by which this subunit regulates light harvesting efficiency is still unknown. Here we show that PsbS controls the association/dissociation of a five-subunit membrane complex, composed of two monomeric Lhcb proteins (CP29 and CP24) and the trimeric LHCII-M. Dissociation of this supercomplex is indispensable for the onset of non-photochemical fluorescence quenching in high light, strongly suggesting that protein subunits catalyzing the reaction of heat dissipation are buried into the complex and thus not available for interaction with PsbS. Consistently, we showed that knock-out mutants on two subunits participating to the B4C complex were strongly affected in heat dissipation. Direct observation by electron microscopy and image analysis showed that B4C dissociation leads to the redistribution of PSII within grana membranes. We interpreted these results to mean that the dissociation of B4C makes quenching sites, possibly CP29 and CP24, available for the switch to an energy-quenching conformation. These changes are reversible and do not require protein synthesis/degradation, thus allowing for changes in PSII antenna size and adaptation to rapidly changing environmental conditions. Photosynthetic reaction centers exploit solar energy to drive electrons from water to NADP ϩ

Snapshot Transient Absorption Spectroscopy of Carotenoid Radical Cations in High-Light-Acclimating Thylakoid Membranes

“…We suggest that this is due to trimeric LHCII migration away from the photosystem II (PSII) supercomplex, which is proposed to occur within 5 min of high light exposure. 15,16 If, as suggested previously, 11,12,17 CT quenching occurs in the monomeric LHCII, this reduces the amount of excitation energy funneled to the CT quenching site. It is noteworthy that the Zea •+ TA signal slowly decreased in dark periods despite the near-constant Zea concentration, indicative of asymmetric induction-relaxation of the CT quenching mechanism.…”

On the origin of a slowly reversible fluorescence decay component in the Arabidopsis npq4 mutant

“…The first type of mechanism relies on the notion that LHC proteins exist in two conformations with different fluorescence lifetimes [18], whose interconversion is controlled by changes in protein-protein interactions in the membrane, which are promoted by activation of PsbS [19,20]. The recent report that npq4 plants lacking PsbS are competent in quenching, although longer exposure to EL is required than in WT plants [21], supports the first hypothesis.…”

“…Previous work led to different proposals for mechanisms leading to fluorescence recovery components with intermediate half-life between qE and qI. First, it was attributed to state 1-state 2 transitions [43]; second to PSII photoinhibition [51]; third to a slowly developing component of qE dependent on Zea [52]; fourth to light-induced dissociation of the complex Lhcb4-Lhcb6-LHCII-M [19]. Here, we show that qM did not correlate with Zea accumulation nor was it related to qI.…”

From ecophysiology to phenomics: some implications of photoprotection and shade–sun acclimation in situ for dynamics of thylakoids in vitro

“…There are few better reminders of this challenge, or of the rich resource available in diverse plants, than the images of thylakoids and videos of chloroplast dynamics assembled by Gunning [12]. Advances in mechanistic understanding of thylakoid dynamics achieved through studies using targeted mutants of Arabidopsis [13,14] are but an ice cube on the tip of the iceberg that is the diversity of thylakoid structure, dynamics and function in the plant kingdom.…”