Evergreen conifers in boreal forests can survive extremely cold (freezing) temperatures during long dark winter and fully recover during summer. A phenomenon called “sustained quenching” putatively provides photoprotection and enables their survival, but its precise molecular and physiological mechanisms are not understood. To unveil them, here we have analyzed seasonal adjustment of the photosynthetic machinery of Scots pine (Pinus sylvestris) trees by monitoring multi-year changes in weather, chlorophyll fluorescence, chloroplast ultrastructure, and changes in pigment-protein composition. Analysis of Photosystem II and Photosystem I performance parameters indicate that highly dynamic structural and functional seasonal rearrangements of the photosynthetic apparatus occur. Although several mechanisms might contribute to ‘sustained quenching’ of winter/early spring pine needles, time-resolved fluorescence analysis shows that extreme down-regulation of photosystem II activity along with direct energy transfer from photosystem II to photosystem I play a major role. This mechanism is enabled by extensive thylakoid destacking allowing for the mixing of PSII with PSI complexes. These two linked phenomena play crucial roles in winter acclimation and protection.

Coping of evergreen conifers in boreal forests with freezing temperatures on bright winter days puts the photosynthetic machinery in great risk of oxidative damage. To survive harsh winter conditions, conifers have evolved a unique but poorly characterized photoprotection mechanism, a sustained form of nonphotochemical quenching (sustained NPQ). Here we focused on functional properties and underlying molecular mechanisms related to the development of sustained NPQ in Norway spruce (Picea abies). Data were collected during 4 consecutive years (2016 to 2019) from trees growing in sun and shade habitats. When day temperatures dropped below −4 °C, the specific N-terminally triply phosphorylated LHCB1 isoform (3p-LHCII) and phosphorylated PSBS (p-PSBS) could be detected in the thylakoid membrane. Development of sustained NPQ coincided with the highest level of 3p-LHCII and p-PSBS, occurring after prolonged coincidence of bright winter days and temperatures close to −10 °C. Artificial induction of both the sustained NPQ and recovery from naturally induced sustained NPQ provided information on differential dynamics and light-dependence of 3p-LHCII and p-PSBS accumulation as prerequisites for sustained NPQ. Data obtained collectively suggest three components related to sustained NPQ in spruce: 1) Freezing temperatures induce 3p-LHCII accumulation independently of light, which is suggested to initiate destacking of appressed thylakoid membranes due to increased electrostatic repulsion of adjacent membranes; 2) p-PSBS accumulation is both light- and temperature-dependent and closely linked to the initiation of sustained NPQ, which 3) in concert with PSII photoinhibition, is suggested to trigger sustained NPQ in spruce. Significance During overwintering, evergreen conifers of boreal forests must cope with freezing temperatures and high light intensities that often occur simultaneously and expose the photosynthetic apparatus to oxidative damage. To mitigate damage, conifers have developed a specific photoprotection mechanism, called sustained nonphotochemical quenching (sustained NPQ). Here we provide evidence for involvement of unique posttranslational phosphorylations of thylakoid proteins in sustained NPQ of spruce. The triply phosphorylated LHCB1 isoform and phospho-PSBS protein appear as prerequisites for development of sustained NPQ that safely dissipate absorbed light energy as heat. While the induction of Lhcb1 triple phosphorylation requires only freezing temperatures, the triggering of sustained NPQ is additionally dependent on light-induced PSBS phosphorylation, likely in concert with limited photoinhibition of photosystem II.

Photosynthetic light-harvesting antennae are pigment-binding proteins that perform one of the most fundamental tasks on Earth, capturing light and transferring energy that enables life in our biosphere. Adaptation to different light environments led to the evolution of an astonishing diversity of light-harvesting systems. At the same time, several strategies have been developed to optimize the light energy input into photosynthetic membranes in response to fluctuating conditions. The basic feature of these prompt responses is the dynamic nature of antenna complexes, whose function readily adapts to the light available. High-resolution microscopy and spectroscopic studies on membrane dynamics demonstrate the crosstalk between antennae and other thylakoid membrane components. With the increased understanding of light-harvesting mechanisms and their regulation, efforts are focusing on the development of sustainable processes for effective conversion of sunlight into functional bio-products. The major challenge in this approach lies in the application of fundamental discoveries in light-harvesting systems for the improvement of plant or algal photosynthesis. Here, we underline some of the latest fundamental discoveries on the molecular mechanisms and regulation of light harvesting that can potentially be exploited for the optimization of photosynthesis.

Photosynthesis is the major natural process that can harvest and harness solar energy into chemical energy. Photosynthesis is performed by a vast number of organisms from single cellular bacteria to higher plants and to make the process efficient, all photosynthetic organisms possess a special type of pigment protein complex(es) that is (are) capable of trapping light energy, known as photosynthetic light-harvesting antennae. From an evolutionary point of view, simpler (unicellular) organisms typically have a simple antenna, whereas higher plants possess complex antenna systems. The higher complexity of the antenna systems provides efficient fine tuning of photosynthesis. This relationship between the complexity of the antenna and the increasing complexity of the organism is mainly related to the remarkable acclimation capability of complex organisms under fluctuating environmental conditions. These antenna complexes not only harvest light, but also provide photoprotection under fluctuating light conditions. In this review, the evolution, structure, and function of different antenna complexes, from single cellular organisms to higher plants, are discussed in the context of the ability to acclimate and adapt to cope under fluctuating environmental conditions.

Deciduous trees exhibit a spectacular phenomenon of autumn senescence driven by the seasonality of their growth environment, yet there is no consensus which external or internal cues trigger it. Senescence starts at different times in European aspen (Populus tremulaL.) genotypes grown in same location. By integrating omics studies, we demonstrate that aspen genotypes utilize similar transcriptional cascades and metabolic cues to initiate senescence, but at different times during autumn. The timing of autumn senescence initiation appeared to be controlled by two consecutive “switches”; 1) first the environmental variation induced the rewiring of the transcriptional network, stress signalling pathways and metabolic perturbations and 2) the start of senescence process was defined by the ability of the genotype to activate and sustain stress tolerance mechanisms mediated by salicylic acid. We propose that salicylic acid represses the onset of leaf senescence in stressful natural conditions, rather than promoting it as often observed in annual plants.

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.