Photorespiration Alleviates Photoinhibition of Photosystem I under Fluctuating Light in Tomato

Fluctuating light (FL) is a typical natural light stress that can cause photodamage to photosystem I (PSI). However, the effect of growth light on FL-induced PSI photoinhibition remains controversial. Plants grown under high light enhance photorespiration to sustain photosynthesis, but the contribution of photorespiration to PSI photoprotection under FL is largely unknown. In this study, we examined the photosynthetic performance under FL in tomato (Lycopersicon esculentum) plants grown under high light (HL-plants) and moderate light (ML-plants). After an abrupt increase in illumination, the over-reduction of PSI was lowered in HL-plants, resulting in a lower FL-induced PSI photoinhibition. HL-plants displayed higher capacities for CO2 fixation and photorespiration than ML-plants. Within the first 60 s after transition from low to high light, PSII electron transport was much higher in HL-plants, but the gross CO2 assimilation rate showed no significant difference between them. Therefore, upon a sudden increase in illumination, the difference in PSII electron transport between HL- and ML-plants was not attributed to the Calvin–Benson cycle but was caused by the change in photorespiration. These results indicated that the higher photorespiration in HL-plants enhanced the PSI electron sink downstream under FL, which mitigated the over-reduction of PSI and thus alleviated PSI photoinhibition under FL. Taking together, we here for the first time propose that photorespiration acts as a safety valve for PSI photoprotection under FL.

Regulation of Leaf Angle Protects Photosystem I under Fluctuating Light in Tobacco Young Leaves

Fluctuating light is a typical light condition in nature and can cause selective photodamage to photosystem I (PSI). The sensitivity of PSI to fluctuating light is influenced by the amplitude of low/high light intensity. Tobacco mature leaves are tended to be horizontal to maximize the light absorption and photosynthesis, but young leaves are usually vertical to diminish the light absorption. Therefore, we tested the hypothesis that such regulation of the leaf angle in young leaves might protect PSI against photoinhibition under fluctuating light. We found that, upon a sudden increase in illumination, PSI was over-reduced in extreme young leaves but was oxidized in mature leaves. After fluctuating light treatment, such PSI over-reduction aggravated PSI photoinhibition in young leaves. Furthermore, the leaf angle was tightly correlated to the extent of PSI photoinhibition induced by fluctuating light. Therefore, vertical young leaves are more susceptible to PSI photoinhibition than horizontal mature leaves when exposed to the same fluctuating light. In young leaves, the vertical leaf angle decreased the light absorption and thus lowered the amplitude of low/high light intensity. Therefore, the regulation of the leaf angle was found for the first time as an important strategy used by young leaves to protect PSI against photoinhibition under fluctuating light. To our knowledge, we show here new insight into the photoprotection for PSI under fluctuating light in nature.

Interplay between LHCSR proteins and state transitions governs the NPQ response in intact cells of Chlamydomonas during light fluctuations.

Photosynthetic organisms use sunlight as the primary energy source to fix CO2. However, in the environment, light energy fluctuates rapidly and often exceeds saturating levels for periods ranging from seconds to hours, which can lead to detrimental effects for cells. Safe dissipation of excess light energy occurs primarily by non-photochemical quenching (NPQ) processes. In the model green microalga Chlamydomonas reinhardtii, photoprotective NPQ is mostly mediated by pH-sensing light-harvesting complex stress-related (LHCSR) proteins and the redistribution of light-harvesting antenna proteins between the photosystems (state transition). Although each component underlying NPQ has been documented, their relative contributions to the dynamic functioning of NPQ under fluctuating light conditions remains unknown. Here, by monitoring NPQ throughout multiple high light-dark cycles with fluctuation periods ranging from 1 to 10 minutes, we show that the dynamics of NPQ depend on the frequency of light fluctuations. Mutants impaired in the accumulation of LHCSRs (npq4, lhcsr1, and npq4lhcsr1) showed significantly less quenching during illumination, demonstrating that LHCSR proteins are responsible for the majority of NPQ during repetitive exposure to high light fluctuations. Activation of NPQ was also observed during the dark phases of light fluctuations, and this was exacerbated in mutants lacking LHCSRs. By analyzing 77K chlorophyll fluorescence spectra and chlorophyll fluorescence lifetimes and yields in a mutant impaired in state transition, we show that this phenomenon arises from state transition. Finally, we quantified the contributions of LHCSRs and state transition to the overall NPQ amplitude and dynamics for all light periods tested and compared those with cell growth under various periods of fluctuating light. These results highlight the dynamic functioning of photoprotection under light fluctuations and open a new way to systematically characterize the photosynthetic response to an ever-changing light environment.

A novel PSII photosynthetic control is activated in anoxic cultures of green algae

Photosynthetic green algae face an ever-changing environment of fluctuating light as well as unstable oxygen levels, which via the production of free radicals constantly challenges the integrity of the photosynthetic complexes. To face such challenges, a complex photosynthetic control network monitors and tightly control the membrane redox potential. Here, we show that not only that the photosynthetic control set the rate limiting step of photosynthetic linear electron flow, but also, upon its ultimate dissipation, it triggers intrinsic alternations in the activity of the photosynthetic complexes. These changes have a grave and prolonged effect on the activity of photosystem II, leading to a massive 3-fold decrease in its electron output. We came into this conclusion via studying a variety of green algae species and applying advance mass-spectrometry and diverse spectroscopic techniques. Our results shed new light on the mechanism of photosynthetic regulation and provide new target for improving photosynthesis.

Diurnal Response of Photosystem I to Fluctuating Light Is Affected by Stomatal Conductance

Upon a sudden transition from low to high light, electrons transported from photosystem II (PSII) to PSI should be rapidly consumed by downstream sinks to avoid the over-reduction of PSI. However, the over-reduction of PSI under fluctuating light might be accelerated if primary metabolism is restricted by low stomatal conductance. To test this hypothesis, we measured the effect of diurnal changes in stomatal conductance on photosynthetic regulation under fluctuating light in tomato (Solanum lycopersicum) and common mulberry (Morus alba). Under conditions of high stomatal conductance, we observed PSI over-reduction within the first 10 s after transition from low to high light. Lower stomatal conductance limited the activity of the Calvin–Benson–Bassham cycle and aggravated PSI over-reduction within 10 s after the light transition. We also observed PSI over-reduction after transition from low to high light for 30 s at the low stomatal conductance typical of the late afternoon, indicating that low stomatal conductance extends the period of PSI over-reduction under fluctuating light. Therefore, diurnal changes in stomatal conductance significantly affect the PSI redox state under fluctuating light. Moreover, our analysis revealed an unexpected inhibition of cyclic electron flow by the severe over-reduction of PSI seen at low stomatal conductance. In conclusion, stomatal conductance can have a large effect on thylakoid reactions under fluctuating light.

Drought stress delays photosynthetic induction and accelerates photoinhibition of photosystem I under fluctuating light

Fluctuating light (FL) and drought stress usually occur concomitantly. However, whether drought stress affects photosynthetic performance under FL remains unknown. Here, we measured gas exchange, chlorophyll fluorescence, and P700 redox state under FL in drought-stressed tomato (Solanum lycopersicum) seedlings. Drought stress significantly affected stomatal opening and mesophyll conductance after transition from low to high light and thus delayed photosynthetic induction under FL. Therefore, drought stress exacerbated the loss of carbon gain under FL. Furthermore, restriction of CO2 fixation under drought stress aggravated the over-reduction of photosystem I (PSI) upon transition from low to high light. The resulting stronger FL-induced PSI photoinhibition significantly supressed linear electron flow and PSI photoprotection. These results indicated that drought stress not only affected gas exchange under FL but also accelerated FL-induced photoinhibition of PSI. Furthermore, drought stress enhanced relative cyclic electron flow in FL, which partially compensated for restricted CO2 fixation and thus favored PSI photoprotection under FL. Therefore, drought stress has large effects on photosynthetic dark and light reactions under FL.