Chloroplast ATP Synthase Modulation of the Thylakoid Proton Motive Force: Implications for Photosystem I and Photosystem II Photoprotection

Abstract

In wild type plants, decreasing CO2 lowers the activity of the chloroplast ATP synthase, slowing proton efflux from the thylakoid lumen resulting in buildup of thylakoid proton motive force (pmf). The resulting acidification of the lumen regulates both light harvesting, via the qE mechanism, and photosynthetic electron transfer through the cytochrome b6f complex. Here, we show that the cfq mutant of Arabidopsis, harboring single point mutation in its γ-subunit of the chloroplast ATP synthase, increases the specific activity of the ATP synthase and disables its down-regulation under low CO2. The increased thylakoid proton conductivity (gH+) in cfq results in decreased pmf and lumen acidification, preventing full activation of qE and more rapid electron transfer through the b6f complex, particularly under low CO2 and fluctuating light. These conditions favor the accumulation of electrons on the acceptor side of PSI, and result in severe loss of PSI activity. Comparing the current results with previous work on the pgr5 mutant suggests a general mechanism where increased PSI photodamage in both mutants is caused by loss of pmf, rather than inhibition of CEF per se. Overall, our results support a critical role for ATP synthase regulation in maintaining photosynthetic control of electron transfer to prevent photodamage.

Regulation of cyclic electron flow by chloroplast NADPH‐dependent thioredoxin system

“…Nevertheless, as discussed below, the effect is not necessarily related to the putative role of PGR5 in CEF. Our results, more likely, support the hypothesis (Kanazawa et al., ; Tikkanen, Rantala, & Aro, ) that PGR5 is involved in controlling the proton conductivity of the thylakoid membrane, which, consequently, affects the generation of pmf .…”

“…The NTRC overexpression may also affect the function of PGR5 in a way that is independent of its involvement in CEF. Redox regulation of PGR5 may occur to control its association with the ATP synthase during dark-to-light and low-to-high light transitions, and thereby allow inhibition of the ATP synthase in an unknown mechanism, as suggested earlier (Kanazawa et al, 2017;Tikkanen et al, 2015). Such a mechanism would result in acidification of the lumen and induction of NPQ, allowing dissipation of excess excitation energy from the electron transfer chain until CBC is activated.…”

“…The antimycin A‐sensitive CEF pathway depends on the proteins PROTON GRADIENT REGULATION 5 (PGR5) (Munekage et al., ) and PGR5‐LIKE 1 (PGRL1) (DalCorso et al., ), and has been suggested to constitute the hypothetical ferredoxin‐plastoquinone reductase (FQR) (Hertle et al., ). However, controversy still exists over the molecular identity of FQR and the physiological function of PGR5 (Kanazawa et al., ; Leister & Shikanai, ; Tikkanen & Aro, ). The PGR‐ and NDH‐dependent pathways differ in their energetic properties; two protons per electron are translocated to the lumen (by the Q‐cycle) in the FQR‐pathway, whereas the NDH complex functions as a proton pump and additionally transfers two protons per electron to the lumen (Strand, Fisher, & Kramer, ; Strand, Livingston, et al., ).…”

Flavodiiron Protein Substitutes for Cyclic Electron Flow without Competing CO2 Assimilation in Rice

“…Damage to PSI is frequently irreversible and can be fatal. Under excessive light, luminal acidification down-regulates the rate of electron transport through the Cyt b 6 f complex (photosynthetic control), protecting PSI from fluctuating light (Kanazawa et al, 2017). Under fluctuating light, photosynthetic organisms also prevent damage to PSI by means of electron sinks downstream of PSI.…”

Overexpression of the Rieske FeS protein of the Cytochromeb6fcomplex increases C4photosynthesis

“…Total protonmotive force (pmf) was estimated from the amplitude of the rapid decay of the electrochromic shift signal and slow relaxation of the signal showed the contribution of proton gradient (ΔpH) and the electrochemical gradient (ΔΨ) across the thylakoid membrane56,57 . Pmf levels and the magnitudes of Δ thylakoid membrane through the ATP synthase was calculated as an inverse of the time constant obtained by fitting the first-order electrochromic shift relaxation58 .…”