Photostasis and photosynthetic adaptation to polar life.

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.

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

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.

Palmelloid formation in the Antarctic psychrophile, Chlamydomonas priscuii, is photoprotective.

Cultures of the obligate, Antarctic psychrophile, Chlamydomonas priscuii grown at permissive low temperature (8°C) are composed of flagellated, single cells, as well as non-motile, multicellular palmelloids. The relative proportions of the two cell types are temperature dependent. However, the temperature dependence for palmelloid formation is not restricted to psychrophilic C. priscuii but appears to be a general response of mesophilic Chlamydomonas species (C. reinhardtii and C. raudensis) to non-permissive growth temperatures. To examine potential differences in photosynthetic performance between single cells versus palmelloids of the psychrophile, a cell filtration technique was developed to separate single cells from palmelloids of C. priscuii grown at 8°C. Flow cytometry was used to estimate the diameter of isolated single cells (≤5 µm) versus isolated palmelloids of varying size (≥8 µm). Compared to single cells, palmelloids of C. priscuii showed a decrease in the abundance of light-harvesting complex II (LHCII) proteins with a 2-fold higher Chl a/b ratio. A decrease in both lutein and ß-carotene in palmelloids resulted in carotenoid pools which were 27% lower in palmelloids compared to single cells of the psychrophile. Chlorophyll fluorescence analyses of the isolated fractions revealed that maximum photochemical efficiency of PSII (Fv/Fm) was comparable for both single cells and palmelloids of C. priscuii. However, isolated palmelloids exhibited lower excitation pressure, measured as 1 - qL, but higher yield of PSII (ΦPSII) and 50% higher rates of electron transport (ETR) than single cells exposed to high light at 8°C. This decreased sensitivity to high light in isolated palmelloids compared to single cells was associated with greater non-regulated dissipation of excess absorbed energy (ΦNO) with minimal differences in ΦNPQ in C. priscuii in response to increasing irradiance at low temperature. The ratio ΦNO/ΦNPQ observed for isolated palmelloids of C. priscuii developed at 8°C (1.414 ± 0.036) was 1.38-fold higher than ΦNO/ΦNPQ of isolated single cells (1.021 ± 0.018) exposed to low temperature combined with high light (1,000 µmol m-2 s-1). The differences in the energy quenching capacities between palmelloids and single cells are discussed in terms of enhanced photoprotection of C. priscuii palmelloids against low-temperature photoinhibition.

The Role of Alternative Electron Pathways for Effectiveness of Photosynthetic Performance of Arabidopsis thaliana, Wt and Lut2, under Low Temperature and High Light Intensity.

A recent investigation has suggested that the enhanced capacity for PSI-dependent cyclic electron flow (CEF) and PSI-dependent energy quenching that is related to chloroplast structural changes may explain the lower susceptibility of lut2 to combined stresses-a low temperature and a high light intensity. The possible involvement of alternative electron transport pathways, proton gradient regulator 5 (PGR5)-dependent CEF and plastid terminal oxidase (PTOX)-mediated electron transfer to oxygen in the response of Arabidopsis plants-wild type (wt) and lut2-to treatment with these two stressors was assessed by using specific electron transport inhibitors. Re-reduction kinetics of P700+ indicated that the capacity for CEF was higher in lut2 when this was compared to wt. Exposure of wt plants to the stress conditions caused increased CEF and was accompanied by a substantial raise in PGR5 and PTOX quantities. In contrast, both PGR5 and PTOX levels decreased under the same stress conditions in lut2, and inhibiting PGR5-dependent pathway by AntA did not exhibit any significant effects on CEF during the stress treatment and recovery period. Electron microscopy observations demonstrated that under control conditions the degree of grana stacking was much lower in lut2, and it almost disappeared under the combined stresses, compared to wt. The role of differential responses of alternative electron transport pathways in the acclimation to the stress conditions that are studied is discussed.

The decreased PG content of pgp1 inhibits PSI photochemistry and limits reaction center and light-harvesting polypeptide accumulation in response to cold acclimation.

MAIN CONCLUSION: Decreased PG constrains PSI activity due to inhibition of transcript and polypeptide abundance of light-harvesting and reaction center polypeptides generating a reversible, yellow phenotype during cold acclimation of pgp1. Cold acclimation of the Arabidopsis pgp1 mutant at 5 °C resulted in a pale-yellow phenotype with abnormal chloroplast ultrastructure compared to its green phenotype upon growth at 20 °C despite a normal cold-acclimation response at the transcript level. In contrast, wild type maintained its normal green phenotype and chloroplast ultrastructure irrespective of growth temperature. In contrast to cold acclimation of WT, growth of pgp1 at 5 °C limited the accumulation of Lhcbs and Lhcas assessed by immunoblotting. However, a novel 43 kD polypeptide of Lhcb1 as well as a 29 kD polypeptide of Lhcb3 accumulated in the soluble fraction which was absent in the thylakoid membrane fraction of cold-acclimated pgp1 which was not observed in WT. Cold acclimation of pgp1 destabilized the Chl-protein complexes associated with PSI and predisposed energy distribution in favor of PSII rather than PSI compared to the WT. Functionally, in vivo PSI versus PSII photochemistry was inhibited in cold-acclimated pgp1 to a greater extent than in WT relative to controls. Greening of the pale-yellow pgp1 was induced when cold-acclimated pgp1 was shifted from 5 to 20 °C which resulted in a marked decrease in excitation pressure to a level comparable to WT. Concomitantly, Lhcbs and Lhcas accumulated with a simultaneous decrease in the novel 43 and 29kD polypeptides. We conclude that the reduced levels of phosphatidyldiacylglycerol in the pgp1 limit the capacity of the mutant to maintain the structure and function of its photosynthetic apparatus during cold acclimation. Thus, maintenance of normal thylakoid phosphatidyldiacylglycerol levels is essential to stabilize the photosynthetic apparatus during cold acclimation.

Photosynthetic adaptation to polar life: Energy balance, photoprotection and genetic redundancy.

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 (0°- 15 °C) but usually die at higher temperatures (≥20 °C). In contrast, photopsychrotolerant species can usually tolerate and survive a broad range of temperatures (5°- 40 °C). 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.

Identification and analyses of the chemical composition of a naturally occurring albino mutant chanterelle.

White chanterelles (Basidiomycota), lacking the orange pigments and apricot-like odour of typical chanterelles, were found recently in the Canadian provinces of Québec (QC) and Newfoundland & Labrador (NL). Our phylogenetic analyses confirmed the identification of all white chanterelles from NL and QC as Cantharellus enelensis; we name these forma acolodorus. We characterized carotenoid pigments, lipids, phenolics, and volatile compounds in these and related chanterelles. White mutants of C. enelensis lacked detectable ß-carotene, confirmed to be the primary pigment of wild-type, golden-orange individuals, and could also be distinguished by their profiles of fatty acids and phenolic acids, and by the ketone and terpene composition of their volatiles. We detected single base substitutions in the phytoene desaturase (Al-1) and phytoene synthase (Al-2) genes of the white mutant, which are predicted to result in altered amino acids in their gene products and may be responsible for the loss of ß-carotene synthesis in that form.

Direct energy transfer from photosystem II to photosystem I confers winter sustainability in Scots Pine.

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.

Low temperature and high light dependent dynamic photoprotective strategies in Arabidopsis thaliana.

Arabidopsis thaliana has been recognized as a chilling tolerant species based on analysis of resistance to low temperature stress, however, the mechanisms involved in this tolerance are not yet clarified. The low temperature-induced effects are exacerbated when plants are exposed to low temperatures in the presence of high light irradiance but the experimental data on the impact of light intensity during cold stress and its influence during recovery from stress are rather limited. The main objective of this study was to re-examine the photosynthetic responses of A. thaliana plants to short term (6 days) low temperature stress (12/10°C) under optimal (150 µmol m-2 s-1 ) and high light (500 µmol m-2 s-1 ) intensity and the subsequent recovery from the stress. Simultaneous measurements of the in vivo and in vitro functional performance of both photosystem II (PSII) and photosystem I (PSI), as well as, net photosynthesis, low temperature (77 K) chlorophyll fluorescence and immunoblot analysis of the relative abundance of PSII and PSI reaction center proteins were used to evaluate the role of light in the development of possible protective mechanisms during low temperature stress and the consequent recovery from exposure to low temperature and different light intensities. The results presented clearly suggest that Arabidopsis plants can employ a number of highly dynamic photoprotective strategies depending on the light intensity. These strategies include one based on LHCII quenching and two other quenching mechanisms localized within the PSII and PSI reaction centers, which are all expressed to different extent depending on the severity of the photoinhibitory treatments under low temperature stress conditions.

Cold-Adapted Protein Kinases and Thylakoid Remodeling Impact Energy Distribution in an Antarctic Psychrophile.

The Antarctic psychrophile Chlamydomonas sp. UWO241 evolved in a permanently ice-covered lake whose aquatic environment is characterized not only by constant low temperature and high salt but also by low light during the austral summer coupled with 6 months of complete darkness during the austral winter. Since the UWO241 genome indicated the presence of Stt7 and Stl1 protein kinases, we examined protein phosphorylation and the state transition phenomenon in this psychrophile. Light-dependent [γ-33P]ATP labeling of thylakoid membranes from Chlamydomonas sp. UWO241 exhibited a distinct low temperature-dependent phosphorylation pattern compared to Chlamydomonas reinhardtii despite comparable levels of the Stt7 protein kinase. The sequence and structure of the UWO241 Stt7 kinase domain exhibits substantial alterations, which we suggest predisposes it to be more active at low temperature. Comparative purification of PSII and PSI combined with digitonin fractionation of thylakoid membranes indicated that UWO241 altered its thylakoid membrane architecture and reorganized the distribution of PSI and PSII units between granal and stromal lamellae. Although UWO241 grown at low salt and low temperature exhibited comparable thylakoid membrane appression to that of C. reinhardtii at its optimal growth condition, UWO241 grown under its natural condition of high salt resulted in swelling of the thylakoid lumen. This was associated with an upregulation of PSI cyclic electron flow by 50% compared to growth at low salt. Due to the unique 77K fluorescence emission spectra of intact UWO241 cells, deconvolution was necessary to detect enhancement in energy distribution between PSII and PSI, which was sensitive to the redox state of the plastoquinone pool and to the NaCl concentrations of the growth medium. We conclude that a reorganization of PSII and PSI in UWO241 results in a unique state transition phenomenon that is associated with altered protein phosphorylation and enhanced PSI cyclic electron flow. These data are discussed with respect to a possible PSII-PSI energy spillover mechanism that regulates photosystem energy partitioning and quenching.

Chlorella vulgaris integrates photoperiod and chloroplast redox signals in response to growth at high light.

MAIN CONCLUSION: Photoacclimation to variable light and photoperiod regimes in C. vulgaris represents a complex interplay between "biogenic" phytochrome-mediated sensing and "operational" redox sensing signaling pathways. Chlorella vulgaris Beijerinck UTEX 265 exhibits a yellow-green phenotype when grown under high light (HL) in contrast to a dark green phenotype when grown at low light (LL). The redox state of the photosynthetic electron transport chain (PETC) as estimated by excitation pressure has been proposed to govern this phenotypic response. We hypothesized that if the redox state of the PETC was the sole regulator of the HL phenotype, C. vulgaris should photoacclimate in response to the steady-state excitation pressure during the light period regardless of the length of the photoperiod. As expected, LL-grown cells exhibited a dark green phenotype, low excitation pressure (1 - qP = 0.22 ± 0.02), high chlorophyll (Chl) content (375 ± 77 fg Chl/cell), low Chl a/b ratio (2.97 ± 0.18) as well as high photosynthetic efficiency and photosynthetic capacity regardless of the photoperiod. In contrast, C. vulgaris grown under continuous HL developed a yellow-green phenotype characterized by high excitation pressure (1 - qP = 0.68 ± 0.01), a relatively low Chl content (180 ± 53 fg Chl/cell), high Chl a/b ratio (6.36 ± 0.54) with concomitantly reduced light-harvesting polypeptide abundance, as well as low photosynthetic capacity and efficiency measured on a per cell basis. Although cells grown under HL and an 18 h photoperiod developed a typical yellow-green phenotype, cells grown at HL but a 12 h photoperiod exhibited a dark green phenotype comparable to LL-grown cells despite exhibiting growth under high excitation pressure (1 - qP = 0.80 ± 0.04). The apparent uncoupling of excitation pressure and phenotype in HL-grown cells and a 12 h photoperiod indicates that chloroplast redox status cannot be the sole regulator of photoacclimation in C. vulgaris. We conclude that photoacclimation in C. vulgaris to HL is dependent upon growth history and reflects a complex interaction of endogenous systems that sense changes in photoperiod as well as photosynthetic redox balance.

Differential temperature effects on dissipation of excess light energy and energy partitioning in lut2 mutant of Arabidopsis thaliana under photoinhibitory conditions.

The high-light-induced alterations in photosynthetic performance of photosystem II (PSII) and photosystem I (PSI) as well as effectiveness of dissipation of excessive absorbed light during illumination for different periods of time at room (22 °C) and low (8-10 °C) temperature of leaves of Arabidopsis thaliana, wt and lut2, were followed with the aim of unraveling the role of lutein in the process of photoinhibition. Photosynthetic parameters of PSII and PSI were determined on whole leaves by PAM fluorometer and oxygen evolving activity-by a Clark-type electrode. In thylakoid membranes, isolated from non-illuminated and illuminated for 4.5 h leaves of wt and lut2 the photochemical activity of PSII and PSI and energy interaction between the main pigment-protein complexes was determined. Results indicate that in non-illuminated leaves of lut2 the maximum rate of oxygen evolution and energy utilization in PSII is lower, excitation pressure of PSII is higher and cyclic electron transport around PSI is faster than in wt leaves. Under high-light illumination, lut2 leaves are more sensitive in respect to PSII performance and the extent of increase of excitation pressure of PSII, ΦNO, and cyclic electron transport around PSI are higher than in wt leaves, especially when illumination is performed at low temperature. Significant part of the excessive light energy is dissipated via mechanism, not dependent on ∆pH and to functioning of xanthophyll cycle in LHCII, operating more intensively in lut2 leaves.

Machine Vision System for 3D Plant Phenotyping.

Machine vision for plant phenotyping is an emerging research area for producing high throughput in agriculture and crop science applications. Since 2D based approaches have their inherent limitations, 3D plant analysis is becoming state of the art for current phenotyping technologies. We present an automated system for analyzing plant growth in indoor conditions. A gantry robot system is used to perform scanning tasks in an automated manner throughout the lifetime of the plant. A 3D laser scanner mounted as the robot's payload captures the surface point cloud data of the plant from multiple views. The plant is monitored from the vegetative to reproductive stages in light/dark cycles inside a controllable growth chamber. An efficient 3D reconstruction algorithm is used, by which multiple scans are aligned together to obtain a 3D mesh of the plant, followed by surface area and volume computations. The whole system, including the programmable growth chamber, robot, scanner, data transfer, and analysis is fully automated in such a way that a naive user can, in theory, start the system with a mouse click and get back the growth analysis results at the end of the lifetime of the plant with no intermediate intervention. As evidence of its functionality, we show and analyze quantitative results of the rhythmic growth patterns of the dicot Arabidopsis thaliana (L.), and the monocot barley (Hordeum vulgare L.) plants under their diurnal light/dark cycles.

Contrasting acclimation abilities of two dominant boreal conifers to elevated CO2 and temperature.

High latitude forests will experience large changes in temperature and CO2 concentrations this century. We evaluated the effects of future climate conditions on 2 dominant boreal tree species, Pinus sylvestris L. and Picea abies (L.) H. Karst, exposing seedlings to 3 seasons of ambient (430 ppm) or elevated CO2 (750 ppm) and ambient temperatures, a + 4 °C warming or a + 8 °C warming. Pinus sylvestris responded positively to warming: seedlings developed a larger canopy, maintained high net CO2 assimilation rates (Anet ), and acclimated dark respiration (Rdark ). In contrast, carbon fluxes in Picea abies were negatively impacted by warming: maximum rates of Anet decreased, electron transport was redirected to alternative electron acceptors, and thermal acclimation of Rdark was weak. Elevated CO2 tended to exacerbate these effects in warm-grown Picea abies, and by the end of the experiment Picea abies from the +8 °C, high CO2 treatment produced fewer buds than they had 3 years earlier. Treatments had little effect on leaf and wood anatomy. Our results highlight that species within the same plant functional type may show opposite responses to warming and imply that Picea abies may be particularly vulnerable to warming due to low plasticity in photosynthetic and respiratory metabolism.

Heat stress-induced effects of photosystem I: an overview of structural and functional responses.

Temperature is one of the main factors controlling the formation, development, and functional performance of the photosynthetic apparatus in all photoautotrophs (green plants, algae, and cyanobacteria) on Earth. The projected climate change scenarios predict increases in air temperature across Earth's biomes ranging from moderate (3-4 °C) to extreme (6-8 °C) by the year 2100 (IPCC in Climate change 2007: The physical science basis: summery for policymakers, IPCC WG1 Fourth Assessment Report 2007; Climate change 2014: Mitigation of Climate Change, IPCC WG3 Fifth Assessment Report 2014). In some areas, especially of the Northern hemisphere, even more extreme warm seasonal temperatures may occur, which possibly will cause significant negative effects on the development, growth, and yield of important agricultural crops. It is well documented that high temperatures can cause direct damages of the photosynthetic apparatus and photosystem II (PSII) is generally considered to be the primary target of heat-induced inactivation of photosynthesis. However, since photosystem I (PSI) is considered to determine the global amount of enthalpy in living systems (Nelson in Biochim Biophys Acta 1807:856-863, 2011; Photosynth Res 116:145-151, 2013), the effects of elevated temperatures on PSI might be of vital importance for regulating the photosynthetic response of all photoautotrophs in the changing environment. In this review, we summarize the experimental data that demonstrate the critical impact of heat-induced alterations on the structure, composition, and functional performance of PSI and their significant implications on photosynthesis under future climate change scenarios.

An established Arabidopsis thaliana var. Landsberg erecta cell suspension culture accumulates chlorophyll and exhibits a stay-green phenotype in response to high external sucrose concentrations.

An established cell suspension culture of Arabidopsis thaliana var. Landsberg erecta was grown in liquid media containing 0-15%(w/v) sucrose. Exponential growth rates of about 0.40d-1 were maintained between 1.5-6%(w/v) sucrose, which decreased to about 0.30d-1 between 6 and 15%(w/v) sucrose. Despite the presence of external sucrose, cells maintained a stay-green phenotype at 0-15% (w/v) sucrose. Sucrose stimulated transcript levels of genes involved in the chlorophyll biosynthetic pathway (ChlH, ChlI2, DVR). Although most of the genes associated with photosystem II and photosystem I reaction centers and light harvesting complexes as well as genes associated with the cytochrome b6f and the ATP synthase complexes were downregulated or remained unaffected by high sucrose, immunoblotting indicated that protein levels of PsaA, Lhcb2 and Rubisco per gram fresh weight changed minimallyon a Chl basis as a function of external sucrose concentration. The green cell culture was photosynthetically competent based on light-dependent, CO2-saturated rates of O2 evolution as well as Fv/Fm and P700 oxidation. Similar to Arabidopsis WT seedlings, the suspension cells etiolated in the dark and but remained green in the light. However, the exponential growth rate of the cell suspension cultures in the dark (0.45±0.07d-1) was comparable to that in the light (0.42±0.02d-1). High external sucrose levels induced feedback inhibition of photosynthesis as indicated by the increase in excitation pressure measured as a function of external sucrose concentration. Regardless, the cell suspension culture still maintained a stay-green phenotype in the light at sucrose concentrations from 0 to 15%(w/v) due, in part, to a stimulation of photoprotection through nonphotochemical quenching. The stay-green, sugar-insensitive phenotype of the cell suspension contrasted with the sugar-dependent, non-green phenotype of Arabidopsis Landsberg erecta WT seedlings grown at comparable external sucrose concentrations. It appears that the commonly used Arabidopsis thaliana var. Landsberg erecta cell suspension culture has undergone significant genetic change since its original generation in 1993. We suggest that this genetic alteration has inhibited the sucrose sensing/signaling pathway coupled with a stimulation of chlorophyll an accumulation in the light with minimal effects on the composition and function of its photosynthetic apparatus. Therefore, caution must be exercised in the interpretation of physiological and biochemical data obtained from experimental use of this culture in any comparison with wild-type Arabidopsis seedlings.

Photosynthetic acclimation, vernalization, crop productivity and 'the grand design of photosynthesis'.

Daniel Arnon first proposed the notion of a 'grand design of photosynthesis' in 1982 to illustrate the central role of photosynthesis as the primary energy transformer for all life on Earth. However, we suggest that this concept can be extended to the broad impact of photosynthesis not only in global energy transformation but also in the regulation of plant growth, development, survival and crop productivity through chloroplast redox signalling. We compare and contrast the role of chloroplast redox imbalance, measured as excitation pressure, in governing acclimation to abiotic stress and phenotypic plasticity. Although all photoautrophs sense excessive excitation energy through changes in excitation pressure, the response to this chloroplast redox signal is species dependent. Due to a limited capacity to adjust metabolic sinks, cyanobacteria and green algae induce photoprotective mechanisms which dissipate excess excitation energy at a cost of decreased photosynthetic performance. In contrast, terrestrial, cold tolerant plants such as wheat enhance metabolic sink capacity which leads to enhanced photosynthetic performance and biomass accumulation with minimal dependence on photoprotection. We suggest that the family of nuclear C-repeat binding transcription factors (CBFs) associated with the frost resistance locus, FR2, contiguous with the vernalization locus,VRN1, and mapped to chromosome 5A of wheat, may be critical components that link leaf chloroplast redox regulation to enhanced photosynthetic performance, the accumulation of growth-active gibberellins and the dwarf phenotype during cold acclimation prior to the vegetative to reproductive transition controlled by vernalization in winter cereals. Further genetic, molecular and biochemical research to confirm these links and to elucidate the molecular mechanism by which chloroplast redox modulation of CBF expression leads to enhanced photosynthetic performance is required. Because of the superior abiotic stress tolerance of cold tolerant winter wheat and seed yields that historically exceed those of spring wheat by 30-40%, we discuss the potential to exploit winter cereals for the maintenance or perhaps even the enhancement of cereal productivity under future climate change scenarios that will be required to feed a growing human population.

Global transcriptome analyses provide evidence that chloroplast redox state contributes to intracellular as well as long-distance signalling in response to stress and acclimation in Arabidopsis.

Global transcriptome analyses were used to assess the interactive effects of short-term stress versus long-term acclimation to high light (HL), low temperature (LT) and excitation pressure in Arabidopsis. Microarray analyses indicated that exposure to stress resulted in two times as many modulated transcripts in both, high-light-treated and low-temperature-treated plants, compared to plants that were fully acclimated to either one of these conditions. We showed that 10.9 % of all transcripts were regulated in the same way by both stress conditions, and hence, were categorized as excitation pressure regulated, rather than regulated by either high-light or low-temperature stress per se. This group of chloroplast redox-sensitive genes included various photosynthetic genes as well as genes known to be associated with cold acclimation (cbf3, cor15A, cor15B) and gibberellic acid (GA) metabolism and signalling (ga2ox1, gai). Chemical inhibition of the photosynthetic electron transport by either DCMU or DBMIB indicated that although the plastoquinone pool contributes significantly to redox regulation of the transcriptome (8.6 %), it appears that PSI represents the major source of redox signals (89 %), whereas PSII appears to contribute only 3.1 %. A comparison of the gene expression profiles between stress and acclimated plants indicated that 10 % of the genes induced by a short, 1-h stress were also associated with long-term acclimation to high excitation pressure. This included the APETALA2/ETHYLENE-RESPONSIVE-BINDING PROTEIN family, the MYB domain- and MYB-related transcription factor family as well as the GRAS transcription factor family important in GA signalling confirming that acclimation to stress is a time-nested phenomenon. We suggest that acclimation to photosynthetic redox imbalance extends beyond the chloroplast and the leaf cell to systemic ROS signalling. This is discussed in terms of the control of plant phenotype through regulation of the nuclear encoded cbf regulon and GA metabolism.

Two Hymenophyllaceae species from contrasting natural environments exhibit a homoiochlorophyllous strategy in response to desiccation stress.

Hymenophyllaceae is a desiccation tolerant family of Pteridophytes which are poikilohydric epiphytes. Their fronds are composed by a single layer of cells and lack true mesophyll cells and stomata. Although they are associated with humid and shady environments, their vertical distribution varies along the trunk of the host plant with some species inhabiting the drier sides with a higher irradiance. The aim of this work was to compare the structure and function of the photosynthetic apparatus during desiccation and rehydration in two species, Hymenophyllum dentatum and Hymenoglossum cruentum, isolated from a contrasting vertical distribution along the trunk of their hosts. Both species were subjected to desiccation and rehydration kinetics to analyze frond phenotypic plasticity, as well as the structure, composition and function of the photosynthetic apparatus. Minimal differences in photosynthetic pigments were observed upon dehydration. Measurements of ϕPSII (effective quantum yield of PSII), ϕNPQ (quantum yield of the regulated energy dissipation of PSII), ϕNO (quantum yield of non-regulated energy dissipation of PSII), and TL (thermoluminescence) indicate that both species convert a functional photochemical apparatus into a structure which exhibits maximum quenching capacity in the dehydrated state with minimal changes in photosynthetic pigments and polypeptide compositions. This dehydration-induced conversion in the photosynthetic apparatus is completely reversible upon rehydration. We conclude that H. dentatum and H. cruentum are homoiochlorophyllous with respect to desiccation stress and exhibited no correlation between inherent desiccation tolerance and the vertical distribution along the host tree trunk.