PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition

Abstract

Feedback de-excitation (qE) regulates light harvesting in plants to prevent inhibition of photosynthesis when light absorption exceeds photosynthetic capacity. Although the mechanism of qE is not completely understood, it is known to require a low thylakoid lumen pH, de-epoxidized xanthophylls, and the photosystem II protein PsbS. During a short-term 4-h exposure to excess light, three PsbS-and qE-deficient Arabidopsis thaliana mutants that differed in xanthophyll composition were more photoinhibited than the wild type. The extent of photoinhibition was the same in all of the mutants, suggesting that qE capacity rather than xanthophyll composition is critical for photoprotection in short-term high light, in contrast to longer-term high light conditions (days) when additional antioxidant roles of specific xanthophylls are evident. Plants with a 2-fold increase in qE capacity were generated by overexpression of PsbS, demonstrating that the level of PsbS limits the qE capacity in wild-type Arabidopsis. These results are consistent with the idea that variations in PsbS expression are responsible for species-specific and environmentally induced differences in qE capacity observed in nature. Furthermore, plants with higher qE capacity were more resistant to photoinhibition than the wild type. Increased qE was associated with decreased photosystem II excitation pressure and changes in the fractional areas of chlorophyll a fluorescence lifetime distributions, but not the lifetime centers, suggesting that qE protects from photoinhibition by preventing overreduction of photosystem II electron acceptors. Engineering of qE capacity by PsbS overexpression could potentially yield crop plants that are more resistant to environmental stress. P lants experience fluctuations in light intensity in nature, with quantitative changes occurring over several orders of magnitude and on time scales ranging from seconds to seasons. Because of these fluctuations, imbalances between light harvesting and utilization of absorbed light energy in photosynthesis occur frequently for most plants. Absorption of light in excess of a plant's capacity for CO 2 fixation has the potential to increase production of reactive intermediates and reactive oxygen species that can cause an inhibition of photosynthesis. To prevent this photoinhibition, plants and algae have evolved several regulatory mechanisms and antioxidant systems (1).In excess light, photosynthetic light harvesting is regulated by feedback de-excitation of singlet excited chlorophyll molecules in photosystem (PS) II. Feedback de-excitation, which can be measured as the qE component of nonphotochemical quenching of chlorophyll fluorescence (NPQ), is a nearly ubiquitous phenomenon in plants and eukaryotic algae that results in harmless thermal dissipation of excess absorbed light energy (reviewed in refs. 2 and 3). Induction and relaxation of qE occur rapidly (time scale of seconds to minutes), and qE has been considered to represent a protective mechanism that prevents PS II photoinhibition...

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

“…This suggests that qM is not related to PSII photoinhibition, as the amplitude of a photoinhibitory component is expected to increase with irradiance; indeed, the component here defined as qI increases from 0.67 at 800 mmol photons m 22 s 21 to 1.01 at 1200 mmol photons m 22 s 21 in npq4 ( figure 1 and table 1). At all light regimes tested, the npq4 leaves showed higher qI than WT leaves, consistent with the photoprotective role of qE in short-term exposure to EL [44].…”

Chlamydomonas reinhardtii PsbS Protein Is Functional and Accumulates Rapidly and Transiently under High Light

“…S3A). This is similar to the situation in Arabidopsis, where PsbS abundance is also correlated to NPQ levels (Li et al, 2002a(Li et al, , 2002b). …”

Regulation of the photosynthetic apparatus under fluctuating growth light

“…Feedback de-excitation qE (energy-dependent quenching) is very rapid, occurring in the timescale of seconds, while the slower component, called qI (photoinhibitory quenching), functions in the minutes to dozens of minutes timescale. It is well documented that qE is dependent on the presence of the PsbS protein [63], which functions as a sensor of lumenal pH through the lumen-exposed protonatable residues [28,63,67]. Despite the requirement of PsbS for rapid induction of qE, a slow induction of qE can be achieved without PsbS [68].…”