Differential Roles of Carotenes and Xanthophylls in Photosystem I Photoprotection

Abstract

Carotenes and their oxygenated derivatives, xanthophylls, are structural elements of the photosynthetic apparatus and contribute to increasing both the light-harvesting and photoprotective capacity of the photosystems. β-Carotene is present in both the core complexes and light-harvesting system (LHCI) of Photosystem (PS) I, while xanthophylls lutein and violaxanthin bind exclusively to its antenna moiety; another xanthophyll, zeaxanthin, which protects chloroplasts against photooxidative damage, binds to the LHCI complexes under conditions of excess light. We functionally dissected various components of the xanthophyll- and carotene-dependent photoprotection mechanism of PSI by analyzing two Arabidopsis mutants: szl1 plants, with a carotene content lower than that of the wild type, and npq1, with suppressed zeaxanthin formation. When exposed to excess light, the szl1 genotype displayed PSI photoinhibition stronger than that of wild-type plants, while removing zeaxanthin had no such effect. The PSI-LHCI complex purified from szl1 was more photosensitive than the corresponding wild-type and npq1 complexes, as is evident from its faster photobleaching and increased rate of singlet oxygen release, suggesting that β-carotene is crucial in controlling chlorophyll triplet formation. Accordingly, fluorescence-detected magnetic resonance analysis showed an increase in the amplitude of signals assigned to chlorophyll triplets in β-carotene-depleted complexes. When PSI was fractioned into its functional moieties, it was revealed that the boost in the rate of singlet oxygen release caused by β-carotene depletion was greater in LHCI than in the core complex. We conclude that PSI-LHCI complex-bound β-carotene elicits a protective response, consisting of a reduction in the yield of harmful triplet excited states, while accumulation of zeaxanthin plays a minor role in restoring phototolerance.

Turning a green alga red: engineering astaxanthin biosynthesis by intragenic pseudogene revival in Chlamydomonas reinhardtii

“…It is possible that by rapidly converting carotenoids into ketocarotenoids, photosystem assembly is hindered, and lower chlorophyll amounts accumulate in the algal cell. Another possible reason for the observed decrease of chlorophyll contents in cells expressing CrBKT could be that photosynthetic complexes, assembled without proper carotenoids, generate more ROS that damage photosynthetic membrane (Cazzaniga et al, 2016), however, this hypothesis is less probable as not perturbation in growth rates were observed. In addition, high-light intensities were tolerated by cells, and ketocarotenoids exhibit high antioxidant capacities which would likely protect membranes from ROS damage.…”

“…The xanthophylls lutein, violaxanthin and neoxanthin are ligands for the photosystem antenna subunits, β-carotene is a ligand for both photosystem core complexes and antenna, while astaxanthin, in H. lacustris, is manly accumulated as a free form in the membrane, although it has been reported to bind photosystems (Mascia et al, 2017) . In a photosynthetic cell, the absence of carotenoids hinders photosystem assembly and reduces chlorophyll content (Cazzaniga et al, 2016). It is possible that by rapidly converting carotenoids into ketocarotenoids, photosystem assembly is hindered, and lower chlorophyll amounts accumulate in the algal cell.…”

Diversity of strategies for escaping reactive oxygen species production within photosystem I among land plants: P700 oxidation system is prerequisite for alleviating photoinhibition in photosystem I

“…These results indicated that the concentration of O 2 required to induce PSI photoinhibition in the fluctuating‐light analysis and under rSP illumination is sufficiently higher than the O 2 concentration required for O 2 reduction in the thylakoid membrane. Recent studies have suggested that 1 O 2 is involved in PSI photoinhibition, although it was assumed that 1 O 2 is not generated in PSI (Hideg and Vass , Cazzaniga et al , , Takagi et al ). Under the highly reducing conditions of PSI, triplet‐state P700 ( 3 P700), which is a source of 1 O 2 production in PSI, is generated by the back reaction of P700 + and A 0 − from P700 + and A 1 − within PSI (Frank et al , Rutherford and Mullet , Setif et al , Ikegami et al , Sétif and Brettel , Polm and Brettel , Rutherford et al ).…”

Oxidation of P700 in Photosystem I Is Essential for the Growth of Cyanobacteria

“…P700 oxidation is expected to negate the effect of hydroxyl radicals by suppressing O 2 2 generation and by oxidizing the ironsulfur centers (Sonoike 1996). Recently, it was suggested that 1 O 2 triggers PSI photoinhibition (Cazzaniga et al, 2012(Cazzaniga et al, , 2016Takagi et al, 2016). Keeping P700 oxidized should help suppress 1 O 2 generation.…”