In vivo modulation of nonphotochemical exciton quenching (NPQ) by regulation of the chloroplast ATP synthase

Abstract

Nonphotochemical quenching (NPQ) of excitation energy, which protects higher plant photosynthetic machinery from photodamage, is triggered by acidification of the thylakoid lumen as a result of light-induced proton pumping, which also drives the synthesis of ATP. It is clear that the sensitivity of NPQ is modulated in response to changing physiological conditions, but the mechanism for this modulation has remained unclear. Evidence is presented that, in intact tobacco or Arabidopsis leaves, NPQ modulation in response to changing CO 2 levels occurs predominantly by alterations in the conductivity of the CF O-CF1 ATP synthase to protons (g H ؉ ). At a given proton flux, decreasing g H ؉ will increase transthylakoid proton motive force (pmf ), thus lowering lumen pH and contributing to the activation of NPQ. violaxanthin deepoxidase ͉ photoinhibition ͉ xanthophyll cycle ͉ proton motive force ͉ chemiosmotic coupling L ight-driven transthylakoid proton motive force (pmf ) serves two essential roles in higher plant photosynthesis (1). First, it is the central intermediate in the chemiosmotic circuit for light-driven ATP synthesis. Light-driven electron transfer leads to the pumping of protons from the stroma to the thylakoid lumen, establishing pmf, which drives the endergonic synthesis of ATP from ADP and orthophosphate (P i ) at the CF O -CF 1 ATP synthase (ATP synthase).Second, the ⌬pH component of pmf is the key regulatory signal for initiation of nonphotochemical quenching (NPQ) of excitation energy, which is important for photoprotection. Light absorption by the light-harvesting complexes (LHCs) in excess of that which can be processed can lead to harmful side reactions, collectively termed photoinhibition, that can occur at several levels, including the antenna complexes, the oxidizing and reducing sides of photosystem II (PS II), and the reducing side of photosystem I (PS I) (see reviews in refs. 2 and 3).In higher plants, photoinhibition is avoided in part by activation of NPQ, which can dump a large fraction of excitation energy, preventing the accumulation of reactive intermediates (see reviews in refs. 4 and 5-7). It is now generally accepted that NPQ involves two processes activated by acidification of the lumen, the interconversion of xanthophyll cycle carotenoids by violaxanthin deepoxidase (VDE), and the protonation of residues on key LHC components, in particular the psbS subunit (reviewed in ref. 7). Arabidopsis mutants deficient in NPQ are light sensitive, confirming its role in photoprotection (e.g., refs. 8 and 9-12).In the most basic working model for NPQ function (e.g., figure 2 of reference 12), where the kinetic and thermodynamic properties of each step in the process are consistent, NPQ should be a continuous function of linear electron flow (LEF). On the other hand, it has become clear that the relationship between LEF and NPQ is strongly modulated in response to rapid changes in physiological state, and we provide a direct demonstration of this below. It has been suggested that such NPQ mod...

The Roles of ATP Synthase and the Cytochrome b 6/f Complexes in Limiting Chloroplast Electron Transport and Determining Photosynthetic Capacity

“…We found that reductions in ATP synthase content increased NPQ and probably the transthylakoid DpH as previously reported (Price et al, 1995). It has also been suggested that ATP synthase senses the status of stromal metabolites either directly or indirectly (Kramer et al, 2004) and it has been suggested that its activity can be modulated by altering Pi levels (Kanazawa and Kramer, 2002;Takizawa et al, 2008). A number of Calvin cycle enzyme activities are regulated by the chloroplast ferredoxin-thioredoxin pathway (e.g.…”

“…However, there are few studies that have considered the role of chloroplast ATP synthase as a limiting factor for the thylakoid reactions. Recent studies have documented that the in vivo activity of ATP synthase is modulated, especially at low or high CO 2 concentration where CO 2 assimilation is restricted either by CO 2 concentration or end product limitation (Kanazawa and Kramer, 2002;Kramer et al, 2004;Baker et al, 2007). The conductivity of proton efflux from the lumen (gH + ) through the ATP synthase could be modulated to regulate the thylakoid proton motive force (pmf; Kramer et al, 2004), providing flexibility in the ratio of ATP production per H + .…”

BIOGENESIS FACTOR REQUIRED FOR ATP SYNTHASE 3 Facilitates Assembly of the Chloroplast ATP Synthase Complex

“…These results indicate that photosynthetic linear electron transport is inhibited between PSII and PSI in bfa3. Similar photosynthetic properties were observed in tobacco (Nicotiana tabacum) plants with low accumulation of chloroplast ATP synthase, in which linear electron transport is strongly inhibited at the cytochrome b 6 f (Cyt b 6 f ) complex via the photosynthetic control mechanism (Foyer et al, 1990;Kanazawa and Kramer, 2002;Rott et al, 2011).…”

PHOTOSYSTEM II PROTEIN33, a Protein Conserved in the Plastid Lineage, Is Associated with the Chloroplast Thylakoid Membrane and Provides Stability to Photosystem II Supercomplexes in Arabidopsis

“…5A). The effect on NPQ observed with the mutant could be related to the observed loss of the PSII-LHCII supercomplex in the psb33 mutants, but we were interested to determine whether the PSB33 mutant also displayed other phenotypes indicative of impaired NPQ, such as an altered luminal pH, increased activity of the violaxanthin cycle, and state transitions (Niyogi et al, 1998;Kanazawa and Kramer, 2002;Pesaresi et al, 2009).…”