Modulation of energy-dependent quenching of excitons in antennae of higher plants

doi:10.1073/pnas.0401269101

Modulation of energy-dependent quenching of excitons in antennae of higher plants

Institute of Biological Chemistry, 289 Clark Hall, Washington State University, Pullman, WA 99164-6340

Communicated by Rodney B. Croteau, Washington State University, Pullman, WA, February 25, 2004 (received for review November 13, 2003)

Abstract

Energy-dependent exciton quenching, or q_E, protects the higher plant photosynthetic apparatus from photodamage. Initiation of q_E involves protonation of violaxanthin deepoxidase and PsbS, a component of the photosystem II antenna complex, as a result of lumen acidification driven by photosynthetic electron transfer. It has become clear that the response of q_E to linear electron flow, termed “q_E sensitivity,” must be modulated in response to fluctuating environmental conditions. Previously, three mechanisms have been proposed to account for q_E modulation: (i) the sensitivity of q_E to the lumen pH is altered; (ii) elevated cyclic electron flow around photosystem I increases proton translocation into the lumen; and (iii) lowering the conductivity of the thylakoid ATP synthase to protons (g _H+) allows formation of a larger steady-state proton motive force (pmf). Kinetic analysis of the electrochromic shift of intrinsic thylakoid pigments, a linear indicator of transthylakoid electric field component, suggests that, when CO₂ alone was lowered from 350 ppm to 50 ppm CO₂, modulation of q_E sensitivity could be explained solely by changes in conductivity. Lowering both CO₂ (to 50 ppm) and O₂ (to 1%) resulted in an additional increase in q_E sensitivity that could not be explained by changes in conductivity or cyclic electron flow associated with photosystem I. Evidence is presented for a fourth mechanism, in which changes in q_E sensitivity result from variable partitioning of proton motive force into the electric field and pH gradient components. The implications of this mechanism for the storage of proton motive force and the regulation of the light reactions are discussed.

Footnotes

↵ * To whom correspondence should be addressed. E-mail: dkramer{at}wsu.edu.
Abbreviations: PS, photosystem; CEF1, cyclic electron flow associated with PS I; ECS, electrochromic shift of carotenoids; ECS_t, amplitude of light–dark ECS signal; g _H+, conductivity of CF_o-CF₁ ATP synthase to proton efflux; LC, low CO₂ (50 ppm CO₂, 21% O₂); LEA, low electron acceptor (50 ppm CO₂, 1% O₂); LEF, linear electron flow; NPQ, nonphotochemical quenching of excitation energy; pmf, proton motive force; q_E, energy-dependent component of NPQ; VDE, violaxanthin deepoxidase; Δψ and ΔpH, electric field and pH components of pmf; WWC, water–water cycle.
↵ † At steady state, the rate of proton accumulation in the lumen from electron transfer is equal to its rate of efflux.