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Actinic light (AL)-induced changes in the redox state of P700 in summer pine (SP; A, B) and winter pine (WP; C, D) needles under an ambient O 2 and CO 2 (A, C) atmosphere and an oxygenfree N 2-rich, CO 2-enriched atmosphere (B, D). The AL was applied when steady-state P700 oxidation was reached in the presence of far-red (FR) light. The measurements were performed at 20 °C or 5 °C for SP and WP needles, respectively. The intensity of the AL was 150 lmol photons m ±2 s ±1
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As shown before [C. Ottander et al. (1995) Planta 197:176-183], there is a severe inhibition of the photosystem (PS) II photochemical efficiency of Scots pine (Pinus sylvestris L.) during the winter. In contrast, the in vivo PSI photochemistry is less inhibited during winter as shown by in vivo measurements of (A820/A820 (P700+). There was also...
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The photochemical reflectance index (PRI) is a proxy for the activity of the photoprotective xanthophyll cycle and photosynthetic light use efficiency (LUE) in plants. Evergreen conifers downregulate photosynthesis in autumn in response to low temperature and shorter photoperiod, and the dynamic xanthophyll cycle-mediated non-photochemical quenchin...
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... The well established much-reduced or even disappearance of grana in overwintering conifers (Martin and Öquist 1979;Demmig-Adams et al. 2015;Bag et al. 2020) allowing homogenous distibution and intermixing of PSII and PSI chlorophyll-protein complexes is a prerequisite for the efficient "spillover"-assisted PSI-dependent EEE quenching in conifers (Bag et al. 2020). These energy-dissipation processes are integrated with up-regulation of the PSI-driven cyclic electron flow (CEF) (Ivanov et al. 2001;Bag et al. 2020;Yang et al. 2020) and re-routing excess electrons to oxygen-reducing, alternative pathways involving the plastid terminal oxidase (PTOX) (Savitch et al. 2010;Busch et al. 2008) and/or flavodiiron proteins (Bag et al. 2023) (Fig. 3b). However, the activation of needle photosynthesis in the spring is preceded by the activation of photosynthesis in specific cortical bark chlorenchyma cells, which leads to the activation of needle mesophyll photosynthesis ). ...
Photostasis is the light-dependent maintenance of energy balance associated with cellular homeostasis in photoautotrophs. We review evidence that illustrates how photosynthetic adaptation in polar photoautrophs such as aquatic green algae, cyanobacteria, boreal conifers as well as terrestrial angiosperms exhibit an astonishing plasticity in structure and function of the photosynthetic apparatus. This plasticity contributes to the maintenance of photostasis, which is essential for the long-term survival in the seemingly inhospitable Antarctic and Arctic habitats. However, evidence indicates that polar photoautrophic species exhibit different functional solutions for the maintenance of photostasis. We suggest that this reflects, in part, the genetic diversity symbolized by inherent genetic redundancy characteristic of polar photoautotrophs which enhances their survival in a thermodynamically challenging environment.
... Both AEF and CEF are mediated by various molecular pathways preventing accumulation of electrons inside the electron transport chain and facilitating photoprotective functions under environmental stress conditions (Yamori and Shikanai, 2016;Alric and Johnson, 2017;Alboresi et al., 2019b;Nawrocki et al., 2019). Although previous studies of the seasonal acclimation in boreal evergreen conifers have highlighted the importance of AEF (Savitch et al., 2010;Bag et al., 2023) and CEF (Ivanov et al., 2001;Fréchette et al., 2015;Yang et al., 2020), the underlying dynamics of PSI and PSII remain unresolved. ...
... These allowed us to quantify cY I max (Fig. 3F), revealing a substantial decrease of the maximal PSI activity during spring in response to PSI photoinhibition in both species. These results also highlighted that in boreal evergreen conifers the preservation of maximal PSI activity during winter (Ivanov et al., 2001;Öquist and Huner, 2003) is not necessarily maintained throughout the seasons. During spring, the decline of cY I max (Fig. 3F) was in-line with the continuous decrease of the relative PSI core protein abundance in pine and spruce (PsaB, Fig. 6A, B) and generally supported by significant linear regressions of in vivo and immunoblot data ( Supplementary Fig. S8), despite not being obtained from the same needle samples, which likely contributed to the large variance. ...
... Similar to AEF, also CEF around PSI is considered to be important to maintain photosynthesis under environmental stress conditions by balancing the ATP/NAPDH ratio and protecting both photosystems from photodamage (Yamori and Shikanai, 2016). In conifers, CEF has been suggested to be up-regulated during winter and spring (Ivanov et al., 2001;Fréchette et al., 2015;Yang et al., 2020). While our estimation of steady-state CEF using classical PSI quantum yields (ETR CEF ) supported these results, accounting for PSI photoinhibition with corrected PSI quantum yields (cETR CEF ) showed no seasonal upregulation of CEF in pine (Fig. 5A, C) and spruce (Fig. 5B, D). ...
The photosynthetic acclimation of boreal evergreen conifers is controlled by regulatory and photoprotective mechanisms that allow conifers to cope with extreme environmental changes. However, the underlying dynamics of photosystem II (PSII) and photosystem I (PSI) remain unresolved.
Here, we investigated the dynamics of PSII and PSI during the spring recovery of photosynthesis in Pinus sylvestris and Picea abies using a combination of chlorophyll-a fluorescence, P700 difference absorbance measurements, and quantification of key thylakoid protein abundances. In particular, we derived a new set of PSI quantum yield equations, correcting for the effects of PSI photoinhibition.
Using the corrected equations, we found that the seasonal dynamics of PSII and PSI photochemical yields remained largely in balance, despite substantial seasonal changes in the stoichiometry of PSII and PSI core complexes driven by PSI photoinhibition. Similarly, the previously reported seasonal upregulation of cyclic electron flow was no longer evident, after accounting for PSI photoinhibition.
Overall, our results emphasize the importance of considering the dynamics of PSII and PSI to elucidate the seasonal acclimation of photosynthesis in overwintering evergreens. Beyond the scope of conifers, our corrected PSI quantum yields expand the toolkit for future studies aimed at elucidating the dynamic regulation of PSI.
... It has been shown that during winter P700 in conifers remain in a donor-side limited condition-meaning P700 is mostly in its oxidized state (P700 + ) 23,24,27 . However, we found that in ES thylakoids, PQ remains in a highly reduced state (Fig. 2e) concomitant with three times higher intersystem epool (Fig. 2c) and 5 times higher stromal epool in the intact pine needles 41,55 . In absence or extremely low LEF, this non-photochemical reduction of the PQ (Fig. 2d, Supplementary Fig. 5a-d) might be linked to higher NAD(P)H reduction via chloroplastic NDH II activity as predicted previously 41,51 . ...
... Therefore, CEF is unlikely to be a dominant pathway for scavenging electrons and oxidation of P700 in ES thylakoids. However, as PGR5/ PGRL1 was reported to be more abundant in ES than S 27 , along with higher abundance of ATP in winter acclimated pine needles 55 , hence, we speculate that PGR5-CEF may contribute to ATP production via proton gradient formation 59 . In ES when intersystem e-pool is much higher 29,41 , over reduction of the PQ could prevent CEF 43 and thereby hinder pmf generation 59 which could lower ATP production. ...
... However, electron scavenging by Flvs from the acceptor-side of PSI through O 2 photoreduction upon illumination could shift the PQ/PQH2 balance and restore CEF. This would maintain the pmf and continue ATP generation even if LEF was restricted 23,55 . ...
Green organisms evolve oxygen (O 2) via photosynthesis and consume it by respiration. Generally, net O 2 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 O 2 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 O 2 consumption occurs around photo-system (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 O 2 photoreduction is a major alternative pathway in ES. This photoprotection mechanism in vascular plants indicates that conifers have developed an adaptative evolution trajec-tory for growing in harsh environments.
... Therefore, CEF is unlikely to be a dominant pathway for scavenging electrons and oxidation of P700 in ES thylakoids. However, as Pgr5/Pgrl1 has been reported to be more abundant in ES than S [34], along with higher abundance of ATP in winter acclimated pine needles [66], we speculate that CEF may contribute to ATP production via proton gradient formation [67]. ...
Green organisms evolve O 2 via photosynthesis and consume by respiration. Net O 2 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 demonstrate strong O 2 consumption even in the presence of light when extremely low temperatures coincide with high solar irradiation during early spring. This phenomenon deviates from the general finding that photosynthetic organisms evolve O 2 upon illumination. By using different electron transport chain inhibitors, we showed that O 2 consumption occurred around photosystem (PS) I and correlated with higher abundance of flavodiiron (Flv) A protein in ES thylakoid membranes. Furthermore, by measuring P700 absorption changes, we separated different alternative electron flow pathways and demonstrated that electron scavenging from the acceptor-side of PSI via O 2 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.
... (5) Photosystem I and alternative electron flow: The functional stability of PSII and PSI differs under stress (Ivanov et al., 2001), and this may lead to a difference in their relative contributions to fluorescence emission. Thus, fluorescence emission from both PSII and PSI should be considered when SIF PSII is inferred from atsensor SIF for the broad application of MLR-SIF. ...
Solar‐induced Chl fluorescence (SIF) offers the potential to curb large uncertainties in the estimation of photosynthesis across biomes and climates, and at different spatiotemporal scales. However, it remains unclear how SIF should be used to mechanistically estimate photosynthesis.
In this study, we built a quantitative framework for the estimation of photosynthesis, based on a mechanistic light reaction model with the Chla fluorescence of Photosystem II (SIFPSII) as an input (MLR‐SIF). Utilizing 29 C3 and C4 plant species that are representative of major plant biomes across the globe, we confirmed the validity of this framework at the leaf level.
The MLR‐SIF model is capable of accurately reproducing photosynthesis for all C3 and C4 species under diverse light, temperature, and CO2 conditions. We further tested the robustness of the MLR‐SIF model using Monte Carlo simulations, and found that photosynthesis estimates were much less sensitive to parameter uncertainties relative to the conventional Farquhar, von Caemmerer, Berry (FvCB) model because of the additional independent information contained in SIFPSII.
Once inferred from direct observables of SIF, SIFPSII provides ‘parameter savings’ to the MLR‐SIF model, compared to the mechanistically equivalent FvCB model, and thus avoids the uncertainties arising as a result of imperfect model parameterization. Our findings set the stage for future efforts to employ SIF mechanistically to improve photosynthesis estimates across a variety of scales, functional groups, and environmental conditions.
... Boreal forests of the northern hemisphere consist of both deciduous and evergreen species which exhibit quite distinct strategies as discussed in detail elsewhere Way and Oren, 2010;Way and Yamori, 2014). Due to the seasonal fluctuations in temperature from summer to winter, needles of boreal evergreens are exposed to EEE because they continue to absorb light during the winter even though most of this absorbed energy cannot be used productively due to the low temperature-induced inhibition of photosynthetic CO 2 assimilation (Ensminger et al., 2004;Ivanov et al., 2001;Krivosheeva et al., 1996;Ö quist, 1983;Ö quist and Huner, 1991;Oquist and Hüner, 2003;Ö quist and Martin, 1986;Sveshnikov et al., 2006;Stinziano et al., 2015;Way and Sage, 2008;Busch et al., 2009;Fréchette et al., 2015;Chang et al., 2021). Boreal evergreens develop frost hardiness or freezing tolerance which enables them to survive extreme winter conditions by exploiting two primary environmental cues. ...
The persistent low temperature that characterize polar habitats combined with the requirement for light for all photoautotrophs creates a conundrum. The absorption of too much light at low temperature can cause an energy imbalance that decreases photosynthetic performance that has a negative impact on growth and can affect long-term survival. The goal of this review is to survey the mechanism(s) by which polar photoautotrophs maintain cellular energy balance, that is, photostasis to overcome the potential for cellular energy imbalance in their low temperature environments. Photopsychrophiles are photosynthetic organisms that are obligately adapted to low temperature (0⁰- 15⁰C) but usually die at higher temperatures (≥ 20⁰C). In contrast, photopsychrotolerant species can usually tolerate and survive a broad range of temperatures (5⁰- 40⁰C). First, we summarize the basic concepts of excess excitation energy, energy balance, photoprotection and photostasis and their importance to survival in polar habitats. Second, we compare the photoprotective mechanisms that underlie photostasis and survival in aquatic cyanobacteria and green algae as well as terrestrial Antarctic and Arctic plants. We show that polar photopsychrophilic and photopsychrotolerant organisms attain energy balance at low temperature either through a regulated reduction in the efficiency of light absorption or through enhanced capacity to consume photosynthetic electrons by the induction of O2 as an alternative electron acceptor. Finally, we compare the published genomes of three photopsychrophilic and one photopsychrotolerant alga with five mesophilic green algae including the model green alga, Chlamydomonas reinhardtii. We relate our genomic analyses to photoprotective mechanisms that contribute to the potential attainment of photostasis. Finally, we discuss how the observed genomic redundancy in photopsychrophilic genomes may confer energy balance, photoprotection and resilience to their harsh polar environment. Primary production in aquatic, Antarctic and Arctic environments is dependent on diverse algal and cyanobacterial communities. Although mosses and lichens dominate the Antarctic terrestrial landscape, only two extant angiosperms exist in the Antarctic. The identification of a single ‘molecular key’ to unravel adaptation of photopsychrophily and photopsychrotolerance remains elusive. Since these photoautotrophs represent excellent biomarkers to assess the impact of global warming on polar ecosystems, increased study of these polar photoautotrophs remains essential.
... S1 and S2). This is in agreement with previous studies of various evergreen species (35)(36)(37)(38)(39) and highlights an opportunistic winter acclimation process (40) by ensuring flexible response to environmental changes (38). Comparison of spruce Y(NPQ) between sustained NPQ and nonsustained NPQ winter and summer samples ( Fig. 1D and SI Appendix, Fig. S1) revealed that only upon the induction of sustained NPQ (March 2018 samples) did the capacity for maximal regulatory NPQ decline, but was not completely eliminated. ...
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.
... S1 and S2). This is in agreement with previous studies of various evergreen species (35)(36)(37)(38)(39) and highlights an opportunistic winter acclimation process (40) by ensuring flexible response to environmental changes (38). Comparison of spruce Y(NPQ) between sustained NPQ and nonsustained NPQ winter and summer samples ( Fig. 1D and SI Appendix, Fig. S1) revealed that only upon the induction of sustained NPQ (March 2018 samples) did the capacity for maximal regulatory NPQ decline, but was not completely eliminated. ...
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.
... Ivanov et al. 2012;Mishra et al. 2019). In many plant species, cold-acclimation also leads to changes in the redox potentials of the electron transport chain of PSII, possibly modifying recombination reactions and affecting 1 O 2 yield (Janda et al. 2000;Ivanov et al. 2001;Sane et al. 2003). ...
... Increased production of 1 O 2 in the npq1lut2 mutant of A. thaliana leads to oxidative damage to thylakoid proteins in high light at 10 °C (Alboresi et al. 2011). In different plant species including A. thaliana (Janda et al. 2000;Ivanov et al. 2001;Sane et al. 2003), cold-acclimation causes a decrease in the redox gap between the Q A and Q B electron acceptors of PSII, which favors a direct, non-radiative recombination route (Rappaport and Lavergne 2009) for the elimination of the charge in Q A − (Ivanov 2008). The direct route does not produce 1 O 2 and, therefore, the observed decrease in photoinhibition caused by cold-acclimation might be due to a decrease in 1 O 2 production (for a more comprehensive discussion about the relationship between recombination reactions and 1 O 2 , see Vass and Cser 2009). ...
... It might be possible that temperature induced modifications of PSII are observed only when thermoluminescence is measured from leaves, as done by Sane et al. (2003), but not from isolated thylakoids as used in the present study. We did, however, observe a decrease in the thermoluminescence yield for both B and Q-bands after the 2-week treatment at 4 °C, resembling that reported by Ivanov et al. (2001) and Sane et al. (2003). The intensity of the B-band decreased only little, ~ 4%, in Rschew but the decrease was more pronounced in Tenela (18%), Columbia-0 (20%) and Coimbra (46%). ...
Main conclusions:
Low temperature decreases PSII damage in vivo, confirming earlier in vitro results. Susceptibility to photoinhibition differs among Arabidopsis accessions and moderately decreases after 2-week cold-treatment. Flavonols may alleviate photoinhibition. The rate of light-induced inactivation of photosystem II (PSII) at 22 and 4 °C was measured from natural accessions of Arabidopsis thaliana (Rschew, Tenela, Columbia-0, Coimbra) grown under optimal conditions (21 °C), and at 4 °C from plants shifted to 4 °C for 2 weeks. Measurements were done in the absence and presence of lincomycin (to block repair). PSII activity was assayed with the chlorophyll a fluorescence parameter Fv/Fm and with light-saturated rate of oxygen evolution using a quinone acceptor. When grown at 21 °C, Rschew was the most tolerant to photoinhibition and Coimbra the least. Damage to PSII, judged from fitting the decrease in oxygen evolution or Fv/Fm to a first-order equation, proceeded more slowly or equally at 4 than at 22 °C. The 2-week cold-treatment decreased photoinhibition at 4 °C consistently in Columbia-0 and Coimbra, whereas in Rschew and Tenela the results depended on the method used to assay photoinhibition. The rate of singlet oxygen production by isolated thylakoid membranes, measured with histidine, stayed the same or slightly decreased with decreasing temperature. On the other hand, measurements of singlet oxygen from leaves with Singlet Oxygen Sensor Green suggest that in vivo more singlet oxygen is produced at 4 °C. Under high light, the PSII electron acceptor QA was more reduced at 4 than at 22 °C. Singlet oxygen production, in vitro or in vivo, did not decrease due to the cold-treatment. Epidermal flavonols increased during the cold-treatment and, in Columbia-0 and Coimbra, the amount correlated with photoinhibition tolerance.
... Ivanov et al. 2012;Mishra et al. 2019). In many plant species, cold-acclimation also leads to changes in the redox potentials of the electron transport chain of PSII, possibly modifying recombination reactions and 1 O2 yield ( Janda et al. 2000;Ivanov et al. 2001;Sane et al. 2003). ...
... Increased production of 1 O2 in the npq1lut2 mutant of A. thaliana leads to oxidative damage to thylakoid proteins in high light at 10 °C ( Alboresi et al. 2011). In different plants species including A. thaliana (Janda et al. 2000;Ivanov et al. 2001;Sane et al. 2003), cold-acclimation causes a decrease in the redox gap between the QA and QB electron acceptors of PSII, which favors an indirect, non-radiative recombination route (Rappaport and Lavergne 2009) for the elimination of the charge in QA -(Ivanov 2008). The indirect route does not produce 1 O2 and, therefore, the observed decrease in photoinhibition caused by cold-acclimation might be due to a decrease in 1 O2 production (for a more comprehensive discussion about the relationship between recombination reactions and 1 O2, see Krieger-Liszkay et al. 2008;Vass and Cser 2009). ...
... Mishra et al. 2011;Mishra et al. 2014), but stronger alleviation of photoinhibition was reported when each leaf developed at low temperature ( Strand et al. 1999;Gray et al. 2003). However, we did observe a decrease in the thermoluminescence yield for both B-and Qbands, resembling that reported by Ivanov et al. (2001) and Sane et al. (2003). The intensity of the Bband decreased only little, ~4 %, in Rschew but the decrease was more remarkably in Tenela (18 %), Columbia-0 (20 %) and Coimbra (46 %). ...
To understand the effects of low temperature and cold-acclimation on reactive oxygen species and photoinhibition of photosystem II (PSII), light-induced inactivation of PSII was measured at 22 and 4 °C from four Arabidopsis thaliana accessions (Rschew, Tenela, Columbia-0 and Coimbra) grown under optimal conditions. Photoinhibition was also measured at 4 °C from plants cold-acclimated at 4 °C for two weeks. Measurements were done in the absence and presence of lincomycin that blocks PSII repair, and PSII activity was assayed with the ratio of variable to maximum chlorophyll a fluorescence (F V /F M ) and with light-saturated rate of oxygen evolution using a quinone acceptor. Of the non-acclimated accessions, Rschew was the most tolerant to photoinhibition and Coimbra the least; the rate constants of photoinhibition of the most sensitive accession were 1.3-1.9 times as high as those of the tolerant ones. The damaging reaction of photoinhibition in non-acclimated plants was slower or equal at 4 °C than at 22 °C. The rate constants of photoinhibition of cold-acclimated plants, at 4 °C, were 0.55 to 1.25 times as high as those of non-acclimated plants; the protective effect of cold-acclimation on photoinhibition was consistent in Columbia-0 and Coimbra whereas Rschew and Tenela were either slightly more tolerant or susceptible, depending on the method used to assay photoinhibition. Production of singlet oxygen, measured from thylakoid membranes isolated from non-acclimated and cold-acclimated plants, did not decrease due to cold-acclimation, nor did singlet oxygen production correlate with the rate of photoinhibition or with flavonol contents of the leaves.
