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The Electronic Origin of Far-Red-Light-Driven Oxygenic Photosynthesis.

ABSTRACT: Photosystem-II uses sunlight to trigger charge separation and catalyze water oxidation. Intrinsic properties of chlorophyll a pigments define a natural "red limit" of photosynthesis at ≈680 nm. Nevertheless, charge separation can be triggered with far-red photons up to 800 nm, without altering the nature of light-harvesting pigments. Here we identify the electronic origin of this remarkable phenomenon using quantum chemical and multiscale simulations on a native Photosystem-II model. We find that the reaction center is preorganized for charge separation in the far-red region by specific chlorophyll-pheophytin pairs, potentially bypassing the light-harvesting apparatus. Charge transfer can occur along two distinct pathways with one and the same pheophytin acceptor (Pheo_D1 ). The identity of the donor chlorophyll (Chl_D1 or P_D1 ) is wavelength-dependent and conformational dynamics broaden the sampling of the far-red region by the two charge-transfer states. The two pathways rationalize spectroscopic observations and underpin designed extensions of the photosynthetically active radiation limit.

SUBMITTER: Sirohiwal A

PROVIDER: S-EPMC9304563 | biostudies-literature | 2022 Apr

REPOSITORIES: biostudies-literature

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The Electronic Origin of Far-Red-Light-Driven Oxygenic Photosynthesis.

Sirohiwal Abhishek A Pantazis Dimitrios A DA

Angewandte Chemie (International ed. in English) 20220221 16

Photosystem-II uses sunlight to trigger charge separation and catalyze water oxidation. Intrinsic properties of chlorophyll a pigments define a natural "red limit" of photosynthesis at ≈680 nm. Nevertheless, charge separation can be triggered with far-red photons up to 800 nm, without altering the nature of light-harvesting pigments. Here we identify the electronic origin of this remarkable phenomenon using quantum chemical and multiscale simulations on a native Photosystem-II model. We find tha ...[more]

PMID: 35142017

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Project description:Background and aimsLong-term exposure over several days to far-red light (FR) increases leaf expansion, whereas short-term exposure (minutes) might enhance the photosystem II operating efficiency (ϕPSII). The interaction between these responses at different time scales and their impact on photosynthesis at the whole-plant level are not well understood. We aimed to assess the effects of FR in an irradiance mimicking the spectrum of sunlight (referred to as artificial solar irradiance), in both the long and short term, on whole-plant CO2 assimilation rates and in leaves at different positions in the plant.MethodsTomato (Solanum lycopersicum) plants were grown under artificial solar irradiance conditions with either a severely reduced or normal fraction of FR [SUN(FR-) vs. SUN]. To elucidate the interplay between the growth light treatment and the short-term reduction of FR, we investigated this interaction at both the whole-plant and leaf levels. At the whole-plant level, CO2 assimilation rates were assessed under artificial solar irradiance with a normal fraction and a reduced fraction of FR. At the leaf level, the effects of removal and presence of FR (0FR and 60FR) during transition from high to low light on CO2 assimilation rates and chlorophyll fluorescence were evaluated in upper and lower leaves.Key resultsSUN(FR-) plants had lower leaf area, shorter stems and darker leaves than SUN plants. Although reducing FR during growth did not affect whole-plant photosynthesis under high light intensity, it had a negative impact at low light intensity. Short-term FR removal reduced both plant and leaf CO2 assimilation rates, but only at low light intensity and irrespective of the light treatment during growth and the leaf position. Interestingly, the kinetics of ϕPSII from high to low light were accelerated by 60FR, with a larger effect in lower leaves of SUN than in SUN(FR-) plants.ConclusionsGrowing plants with a reduced amount of FR light lowers whole-plant CO2 assimilation rates at low light intensity through reduced leaf area, despite maintaining similar leaf-level CO2 assimilation to leaves grown with a normal amount of FR. The short-term removal of FR brings about significant but marginal reductions in photosynthetic efficiency at the leaf level, regardless of the long-term growth light treatment.

Project description:BackgroundGrowing evidence demonstrates that the synergistic interaction of far-red light with shorter wavelength lights could evidently improve the photosynthesis efficiency of multiple species. However, whether/how far-red light affects sink organs and consequently modulates the source‒sink relationships are largely unknown.ResultsHere, equal intensities of white and far-red lights were added to natural light for grape plantlets to investigate the effects of far-red light supplementation on grapevine growth and carbon assimilate allocation, as well as to reveal the underlying mechanisms, through physiological and transcriptomic analysis. The results showed that additional far-red light increased stem length and carbohydrate contents in multiple organs and decreased leaf area, specific leaf weight and dry weight of leaves in comparison with their counterparts grown under white light. Compared to white light, the maximum net photosynthetic rate of the leaves was increased by 31.72% by far-red light supplementation, indicating that far-red light indeed elevated the photosynthesis efficiency of grapes. Transcriptome analysis revealed that leaves were most responsive to far-red light, followed by sink organs, including stems and roots. Genes related to light signaling and carbon metabolites were tightly correlated with variations in the aforementioned physiological traits. In particular, VvLHCB1 is involved in light harvesting and restoring the balance of photosystem I and photosystem II excitation, and VvCOP1 and VvPIF3, which regulate light signal transduction, were upregulated under far-red conditions. In addition, the transcript abundances of the sugar transporter-encoding genes VvSWEET1 and VvSWEET3 and the carbon metabolite-encoding genes VvG6PD, VvSUS7 and VvPGAM varied in line with the change in sugar content.ConclusionsThis study showed that far-red light synergistically functioning with white light has a beneficial effect on grape photosystem activity and is able to differentially affect the growth of sink organs, providing evidence for the possible addition of far-red light to the wavelength range of photosynthetically active radiation (PAR).

Dataset Information

The Electronic Origin of Far-Red-Light-Driven Oxygenic Photosynthesis.

Publications

The Electronic Origin of Far-Red-Light-Driven Oxygenic Photosynthesis.

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