Flavodiiron-mediated O2 photoreduction at photosystem I acceptor-side provides photoprotection to conifer thylakoids in early spring

Abstract

Green organisms evolve oxygen (O2) via photosynthesis and consume it by respiration. Generally, net O2 consumption only becomes dominant when photosynthesis is suppressed at night. Here, we show that green thylakoid membranes of Scots pine (Pinus sylvestris L) and Norway spruce (Picea abies) needles display strong O2 consumption even in the presence of light when extremely low temperatures coincide with high solar irradiation during early spring (ES). By employing different electron transport chain inhibitors, we show that this unusual light-induced O2 consumption occurs around photosystem (PS) I and correlates with higher abundance of flavodiiron (Flv) A protein in ES thylakoids. With P700 absorption changes, we demonstrate that electron scavenging from the acceptor-side of PSI via O2 photoreduction is a major alternative pathway in ES. This photoprotection mechanism in vascular plants indicates that conifers have developed an adaptative evolution trajectory for growing in harsh environments.

Possible Contribution of Corticular Photosynthesis to Grapevine Winter Hardiness

“…The seasonal variation in the activity of photosynthesis was previously studied mainly on the needles of evergreen plants [27]. By now, several molecular mechanisms responsible for the acclimatization to low-temperature winter conditions are known, including the alterations in the organization of the PSII antenna, induction of chlororespiration, cyclic electron transport, and flavodiiron-mediated O2 photoreduction at the acceptor side of PSI [2][3][4]28]. In the needles of Scots pine, the thylakoid destacking leading to the mixing of PSII with PSI complexes, extreme down-regulation of photosystem II activity, and direct energy transfer from PSII to PSI play a major role in winter acclimation and protection [2].…”

“…However, some plants manage to maintain their physiological activity during winter. Conifers, whose needles maintain photosynthesis in winter, are the most studied example, and extensive research on the physiology of overwintering needles has been carried out to elucidate the molecular mechanisms underlying the extremely high freeze tolerance of the photosynthetic apparatus in conifer needles [2][3][4][5]. Unfortunately, at the same time, the activity of the photosynthetic apparatus in the chlorenchymal tissues of the lignified organs of overwintering perennial plants, trees, and vines remains beyond the scope of the studies focusing on plant freeze tolerance.…”

A high-light tolerant alga from the desert is protected from oxidative stress by NPQ-independent responses

“…PUFAs have been suggested to contribute to ROS detoxification by interacting with ROS during lipid peroxidation (Schmid-Siegert et al, 2016). Flavodiiron proteins (Flv1 and Flv2), which act as electron sinks possibly involved in PSII and/or PSI photoprotection (Chaux et al, 2015;Burlacot et al, 2022;Bag et al, 2023), were significantly accumulated in HL-grown cells (2.9-and 8.4-fold change, respectively), providing an additional route for energy dissipation. In contrast, PTOX, another putative electron sink (Nawrocki et al, 2015), was not differentially accumulated in HL-grown cells (0.9-fold change) (Figs.…”

Physcomitrium patensflavodiiron proteins form a redox-dependent heterocomplex

“…Pseudo-cyclic electron flow is either sustained by the Mehler reaction or by the activity of flavodiiron proteins (FLVs), enzymes that function as "safety-valves" when linear electron transport though Ferredoxin-NADP + -Reductase (FNR) and NADPH pool is saturated (6). FLVs were shown to be active during the induction of photosynthesis in different organisms such as cyanobacteria (7)(8)(9), the model microalga Chlamydomonas reinhardtii (10), the bryophytes Marchantia polymorpha (11) and Physcomitrium patens (12) and gymnosperms (13). FLV activity is essential to survive light fluctuations (9,12).…”