Limitations to photosynthesis by proton motive force-induced photosystem II photodamage

Abstract

The thylakoid proton motive force (<i>pmf</i>) generated during photosynthesis is the essential driving force for ATP production; it is also a central regulator of light capture and electron transfer. We investigated the effects of elevated <i>pmf</i> on photosynthesis in a library of <i>Arabidopsis thaliana</i> mutants with altered rates of thylakoid lumen proton efflux, leading to a range of steady-state <i>pmf</i> extents. We observed the expected <i>pmf-</i>dependent alterations in photosynthetic regulation, but also strong effects on the rate of photosystem II (PSII) photodamage. Detailed analyses indicate this effect is related to an elevated electric field (Δ<i>ψ</i>) component of the <i>pmf</i>, rather than lumen acidification, which <i>in vivo</i> increased PSII charge recombination rates, producing singlet oxygen and subsequent photodamage. The effects are seen even in wild type plants, especially under fluctuating illumination, suggesting that Δ<i>ψ</i>-induced photodamage represents a previously unrecognized limiting factor for plant productivity under dynamic environmental conditions seen in the field.