A comprehensive assessment of photosynthetic acclimation to shade in C4 grass (Cynodon dactylon (L.) Pers.).

BACKGROUND: Light deficit in shaded environment critically impacts the growth and development of turf plants. Despite this fact, past research has predominantly concentrated on shade avoidance rather than shade tolerance. To address this, our study examined the photosynthetic adjustments of Bermudagrass when exposed to varying intensities of shade to gain an integrative understanding of the shade response of C4 turfgrass. RESULTS: We observed alterations in photosynthetic pigment-proteins, electron transport and its associated carbon and nitrogen assimilation, along with ROS-scavenging enzyme activity in shaded conditions. Mild shade enriched Chl b and LHC transcripts, while severe shade promoted Chl a, carotenoids and photosynthetic electron transfer beyond QA- (ET0/RC, φE0, Ψ0). The study also highlighted differential effects of shade on leaf and root components. For example, Soluble sugar content varied between leaves and roots as shade diminished SPS, SUT1 but upregulated BAM. Furthermore, we observed that shading decreased the transcriptional level of genes involving in nitrogen assimilation (e.g. NR) and SOD, POD, CAT enzyme activities in leaves, even though it increased in roots. CONCLUSIONS: As shade intensity increased, considerable changes were noted in light energy conversion and photosynthetic metabolism processes along the electron transport chain axis. Our study thus provides valuable theoretical groundwork for understanding how C4 grass acclimates to shade tolerance.

Biological nitrogen fixation maintains carbon/nitrogen balance and photosynthesis at elevated CO2.

Understanding crop responses to elevated CO2 is necessary to meet increasing agricultural demands. Crops may not achieve maximum potential yields at high CO2 due to photosynthetic downregulation, often associated with nitrogen limitation. Legumes have been proposed to have an advantage at elevated CO2 due to their ability to exchange carbon for nitrogen. Here, the effects of biological nitrogen fixation (BNF) on the physiological and gene expression responses to elevated CO2 were examined at multiple nitrogen levels by comparing alfalfa mutants incapable of nitrogen fixation to wild-type. Elemental analysis revealed a role for BNF in maintaining shoot carbon/nitrogen (C/N) balance under all nitrogen treatments at elevated CO2, whereas the effect of BNF on biomass was only observed at elevated CO2 and the lowest nitrogen dose. Lower photosynthetic rates at were associated with the imbalance in shoot C/N. Genome-wide transcriptional responses were used to identify carbon and nitrogen metabolism genes underlying the traits. Transcription factors important to C/N signalling were identified from inferred regulatory networks. This work supports the hypothesis that maintenance of C/N homoeostasis at elevated CO2 can be achieved in plants capable of BNF and revealed important regulators in the underlying networks including an alfalfa (Golden2-like) GLK ortholog.

Variation in leaf photosynthetic capacity within plant canopies: optimization, structural, and physiological constraints and inefficiencies.

Leaf photosynthetic capacity (light-saturated net assimilation rate, AA) increases from bottom to top of plant canopies as the most prominent acclimation response to the conspicuous within-canopy gradients in light availability. Light-dependent variation in AA through plant canopies is associated with changes in key leaf structural (leaf dry mass per unit leaf area), chemical (nitrogen (N) content per area and dry mass, N partitioning between components of photosynthetic machinery), and physiological (stomatal and mesophyll conductance) traits, whereas the contribution of different traits to within-canopy AA gradients varies across sites, species, and plant functional types. Optimality models maximizing canopy carbon gain for a given total canopy N content predict that AA should be proportionally related to canopy light availability. However, comparison of model expectations with experimental data of within-canopy photosynthetic trait variations in representative plant functional types indicates that such proportionality is not observed in real canopies, and AA vs. canopy light relationships are curvilinear. The factors responsible for deviations from full optimality include stronger stomatal and mesophyll diffusion limitations at higher light, reflecting greater water limitations and more robust foliage in higher light. In addition, limits on efficient packing of photosynthetic machinery within leaf structural scaffolding, high costs of N redistribution among leaves, and limited plasticity of N partitioning among components of photosynthesis machinery constrain AA plasticity. Overall, this review highlights that the variation of AA through plant canopies reflects a complex interplay between adjustments of leaf structure and function to multiple environmental drivers, and that AA plasticity is limited by inherent constraints on and trade-offs between structural, chemical, and physiological traits. I conclude that models trying to simulate photosynthesis gradients in plant canopies should consider co-variations among environmental drivers, and the limitation of functional trait variation by physical constraints and include the key trade-offs between structural, chemical, and physiological leaf characteristics.

Nitrogen use strategy drives interspecific differences in plant photosynthetic CO2 acclimation.

Rising atmospheric CO2 concentration triggers an emergent phenomenon called plant photosynthetic acclimation to elevated CO2 (PAC). PAC is often characterized by a reduction in leaf photosynthetic capacity (Asat ), which varies dramatically along the continuum of plant phylogeny. However, it remains unclear whether the mechanisms responsible for PAC are also different across plant phylogeny, especially between gymnosperms and angiosperms. Here, by compiling a dataset of 73 species, we found that although leaf Asat increased significantly from gymnosperms to angiosperms, there was no phylogenetic signal in the PAC magnitude along the phylogenetic continuum. Physio-morphologically, leaf nitrogen concentration (Nm ), photosynthetic nitrogen-use efficiency (PNUE), and leaf mass per area (LMA) dominated PAC for 36, 29, and 8 species, respectively. However, there was no apparent difference in PAC mechanisms across major evolutionary clades, with 75% of gymnosperms and 92% of angiosperms regulated by the combination of Nm and PNUE. There was a trade-off between Nm and PNUE in driving PAC across species, and PNUE dominated the long-term changes and inter-specific differences in Asat under elevated CO2 . These findings indicate that nitrogen-use strategy drives the acclimation of leaf photosynthetic capacity to elevated CO2 across terrestrial plant species.

Moderate heat stress prevented the observed biomass and yield stimulation caused by elevated CO2 in two well-watered wheat cultivars.

KEY MESSAGE: Heat stress (HS) under well-watered conditions was not detrimental to leaf photosynthesis or yield but modified the elevated CO2 response of photosynthesis and yield in two contrasting wheat cultivars. Climate change is increasing the frequency of extreme events such as heat waves, adversely affecting crop productivity. While positive impacts of elevated carbon dioxide (eCO2) on crop productivity are evident, the interactive effects of eCO2 and environmental stresses are still unclear. To investigate the interactive effects of elevated CO2 and heat stress (HS), we grew two contrasting wheat cultivars, early-maturing Scout and high-tillering Yitpi, under non-limiting water and nutrients at ambient (aCO2, 450 ppm) or elevated (eCO2, 650 ppm) CO2 and 22 °C in the glasshouse. Plants were exposed to two 3-day HS cycles at the vegetative (38.1 °C) and/or flowering (33.5 °C) stage. At aCO2, both wheat cultivars showed similar responses of photosynthesis and mesophyll conductance to temperature and produced similar grain yield. Relative to aCO2, eCO2 enhanced photosynthesis rate and reduced stomatal conductance and maximal carboxylation rate (Vcmax). During HS, high temperature stimulated photosynthesis at eCO2 in both cultivars, while eCO2 stimulated photosynthesis in Scout. Electron transport rate (Jmax) was unaffected by any treatment. eCO2 equally enhanced biomass and grain yield of both cultivars in control, but not HS, plants. HS reduced biomass and yield of Scout at eCO2. Yitpi, the cultivar with higher grain nitrogen, underwent a trade-off between grain yield and nitrogen. In conclusion, eCO2 improved photosynthesis of control and HS wheat, and improved biomass and grain yield of control plants only. Under well-watered conditions, HS was not detrimental to photosynthesis or growth but precluded a yield response to eCO2.

Genotype-dependent contribution of CBF transcription factors to long-term acclimation to high light and cool temperature.

When grown under cool temperature, winter annuals upregulate photosynthetic capacity as well as freezing tolerance. Here, the role of three cold-induced C-repeat-binding factor (CBF1-3) transcription factors in photosynthetic upregulation and freezing tolerance was examined in two Arabidopsis thaliana ecotypes originating from Italy (IT) or Sweden (SW), and their corresponding CBF1-3-deficient mutant lines it:cbf123 and sw:cbf123. Photosynthetic, morphological and freezing-tolerance phenotypes, as well as gene expression profiles, were characterized in plants grown from the seedling stage under different combinations of light level and temperature. Under high light and cool (HLC) growth temperature, a greater role of CBF1-3 in IT versus SW was evident from both phenotypic and transcriptomic data, especially with respect to photosynthetic upregulation and freezing tolerance of whole plants. Overall, features of SW were consistent with a different approach to HLC acclimation than seen in IT, and an ability of SW to reach the new homeostasis through the involvement of transcriptional controls other than CBF1-3. These results provide tools and direction for further mechanistic analysis of the transcriptional control of approaches to cold acclimation suitable for either persistence through brief cold spells or for maximisation of productivity in environments with continuous low temperatures.

Do rapid photosynthetic responses protect maize leaves against photoinhibition under fluctuating light?

Plants in their natural environment are often exposed to fluctuating light because of self-shading and cloud movements. As changing frequency is a key characteristic of fluctuating light, we speculated that rapid light fluctuation may induce rapid photosynthetic responses, which may protect leaves against photoinhibition. To test this hypothesis, maize seedlings were grown under fluctuating light with various frequencies (1, 10, and 100 cycles of fluctuations/10 h), and changes in growth, chlorophyll content, gas exchange, chlorophyll a fluorescence, and P700 were analyzed carefully. Our data show that though the growth and light-saturated photosynthetic rate were depressed by rapidly fluctuating light, photosynthesis induction was clearly speeded up. Furthermore, more rapid fluctuation of light strikingly reduced the chlorophyll content, while thermal dissipation was triggered and enhanced. The chlorophyll a fluorescence induction kinetics and P700 absorption results showed that the activities of both photosystem II and photosystem I decreased as the frequency of the fluctuating light increased. In all treatments, the light intensities of the fluctuating light were kept constant. Therefore, rapid light fluctuation frequency itself induced the acceleration of photosynthetic induction and the enhancement of photoprotection in maize seedlings, which play important roles in protecting photosynthetic apparatus against fluctuating high light to a certain extent.

Carbon sink strength of nodules but not other organs modulates photosynthesis of faba bean (Vicia faba) grown under elevated [CO2 ] and different water supply.

Photosynthetic stimulation by elevated [CO2 ] (e[CO2 ]) may be limited by the capacity of sink organs to use photosynthates. In many legumes, N2 -fixing symbionts in root nodules provide an additional sink, so that legumes may be better able to profit from e[CO2 ]. However, drought not only constrains photosynthesis but also the size and activity of sinks, and little is known about the interaction of e[CO2 ] and drought on carbon sink strength of nodules and other organs. To compare carbon sink strength, faba bean was grown under ambient (400 ppm) or elevated (700 ppm) atmospheric [CO2 ] and subjected to well-watered or drought treatments, and then exposed to 13 C pulse-labelling using custom-built chambers to track the fate of new photosynthates. Drought decreased 13 C uptake and nodule sink strength, and this effect was even greater under e[CO2 ], and was associated with an accumulation of amino acids in nodules. This resulted in decreased N2 fixation, and increased accumulation of new photosynthates (13 C/sugars) in leaves, which in turn can feed back on photosynthesis. Our study suggests that nodule C sink activity is key to avoid sink limitation in legumes under e[CO2 ], and legumes may only be able to achieve greater C gain if nodule activity is maintained.

Nitrogen sources and CO2 concentration synergistically affect the growth and metabolism of tobacco plants.

The initial stimulation of photosynthesis under elevated CO2 concentrations (eCO2) is often followed by a decline in photosynthesis, known as CO2 acclimation. Changes in N levels under eCO2 can have different effects in plants fertilized with nitrate (NO3-) or ammonium (NH4+) as the N source. NO3- assimilation consumes approximately 25% of the energy produced by an expanded leaf, whereas NH4+ requires less energy to be incorporated into organic compounds. Although plant-N interactions are important for the productivity and nutritional value of food crops worldwide, most studies have not compared the performance of plants supplied with different forms of N. Therefore, this study aims to go beyond treating N as the total N in the soil or the plant because the specific N compounds formed from the available N forms become highly engaged in all aspects of plant metabolism. To this end, plant N metabolism was analyzed through an experiment with eCO2 and fertigation with NO3- and/or NH4+ as N sources for tobacco (Nicotiana tabacum) plants. The results showed that the plants that received only NO3- as a source of N grew more slowly when exposed to a CO2 concentration of 760 µmol mol-1 than when they were exposed to ambient CO2 conditions. On the other hand, in plants fertigated with only NH4+, eCO2 enhanced photosynthesis. This was essential for the maintenance of the metabolic pathways responsible for N assimilation and distribution in growing tissues. These data show that the physiological performance of tobacco plants exposed to eCO2 depends on the form of inorganic N that is absorbed and assimilated.

Environmental triggers for photosynthetic protein turnover determine the optimal nitrogen distribution and partitioning in the canopy.

Plants continually adjust the photosynthetic functions in their leaves to fluctuating light, thereby optimizing the use of photosynthetic nitrogen (Nph) at the canopy level. To investigate the complex interplay between external signals during the acclimation processes, a mechanistic model based on the concept of protein turnover (synthesis and degradation) was proposed and parameterized using cucumber grown under nine combinations of nitrogen and light in growth chambers. Integrating this dynamic model into a multi-layer canopy model provided accurate predictions of photosynthetic acclimation of greenhouse cucumber canopies grown under high and low nitrogen supply in combination with day-to-day fluctuations in light at two different levels. This allowed us to quantify the degree of optimality in canopy nitrogen use for maximizing canopy carbon assimilation, which was influenced by Nph distribution along canopy depth or Nph partitioning between functional pools. Our analyses suggest that Nph distribution is close to optimum and Nph reallocation is more important under low nitrogen. Nph partitioning is only optimal under a light level similar to the average light intensity during acclimation, meaning that day-to-day light fluctuations inevitably result in suboptimal Nph partitioning. Our results provide insights into photoacclimation and can be applied to crop model improvement.

Elevated CO2 alleviates the negative impact of heat stress on wheat physiology but not on grain yield.

Hot days are becoming hotter and more frequent, threatening wheat yields worldwide. Developing wheat varieties ready for future climates calls for improved understanding of how elevated CO2 (eCO2) and heat stress (HS) interactively impact wheat yields. We grew a modern, high-yielding wheat cultivar (Scout) at ambient CO2 (aCO2, 419 µl l -1) or eCO2 (654 µl l-1) in a glasshouse maintained at 22/15 °C (day/night). Half of the plants were exposed to HS (40/24 °C) for 5 d at anthesis. In non-HS plants, eCO2 enhanced (+36%) CO2 assimilation rates (Asat) measured at growth CO2 despite down-regulation of photosynthetic capacity. HS reduced Asat (-42%) in aCO2- but not in eCO2-grown plants because eCO2 protected photosynthesis by increasing ribulose bisphosphate regeneration capacity and reducing photochemical damage under HS. eCO2 stimulated biomass (+35%) of all plants and grain yield (+30%) of non-HS plants only. Plant biomass initially decreased following HS but recovered at maturity due to late tillering. HS equally reduced grain yield (-40%) in aCO2- and eCO2-grown plants due to grain abortion and reduced grain filling. While eCO2 mitigated the negative impacts of HS at anthesis on wheat photosynthesis and biomass, grain yield was reduced by HS in both CO2 treatments.

Strong photosynthetic acclimation and enhanced water-use efficiency in grassland functional groups persist over 21 years of CO2 enrichment, independent of nitrogen supply.

Uncertainty about long-term leaf-level responses to atmospheric CO2 rise is a major knowledge gap that exists because of limited empirical data. Thus, it remains unclear how responses of leaf gas exchange to elevated CO2 (eCO2 ) vary among plant species and functional groups, or across different levels of nutrient supply, and whether they persist over time for long-lived perennials. Here, we report the effects of eCO2 on rates of net photosynthesis and stomatal conductance in 14 perennial grassland species from four functional groups over two decades in a Minnesota Free-Air CO2 Enrichment experiment, BioCON. Monocultures of species belonging to C3 grasses, C4 grasses, forbs, and legumes were exposed to two levels of CO2 and nitrogen supply in factorial combinations over 21 years. eCO2 increased photosynthesis by 12.9% on average in C3 species, substantially less than model predictions of instantaneous responses based on physiological theory and results of other studies, even those spanning multiple years. Acclimation of photosynthesis to eCO2 was observed beginning in the first year and did not strengthen through time. Yet, contrary to expectations, the response of photosynthesis to eCO2 was not enhanced by increased nitrogen supply. Differences in responses among herbaceous plant functional groups were modest, with legumes responding the most and C4 grasses the least as expected, but did not further diverge over time. Leaf-level water-use efficiency increased by 50% under eCO2 primarily because of reduced stomatal conductance. Our results imply that enhanced nitrogen supply will not necessarily diminish photosynthetic acclimation to eCO2 in nitrogen-limited systems, and that significant and consistent declines in stomatal conductance and increases in water-use efficiency under eCO2 may allow plants to better withstand drought.

Metabolic and Transcriptional Analysis of Durum Wheat Responses to Elevated CO2 at Low and High Nitrate Supply.

Elevated [CO2] (eCO2) can lead to photosynthetic acclimation and this is often intensified by low nitrogen (N). Despite intensive studies of plant responses to eCO2, the regulation mechanism of primary metabolism at the whole-plant level in interaction with [Formula: see text] supply remains unclear. We examined the metabolic and transcriptional responses triggered by eCO2 in association with physiological-biochemical traits in flag leaves and roots of durum wheat grown hydroponically in ambient and elevated [CO2] with low (LN) and high (HN) [Formula: see text] supply. Multivariate analysis revealed a strong interaction between eCO2 and [Formula: see text] supply. Photosynthetic acclimation induced by eCO2 in LN plants was accompanied by an increase in biomass and carbohydrates, and decreases of leaf organic N per unit area, organic acids, inorganic ions, Calvin-Benson cycle intermediates, Rubisco, nitrate reductase activity, amino acids and transcripts for N metabolism, particularly in leaves, whereas [Formula: see text] uptake was unaffected. In HN plants, eCO2 did not decrease photosynthetic capacity or leaf organic N per unit area, but induced transcripts for N metabolism, especially in roots. In conclusion, the photosynthetic acclimation in LN plants was associated with an inhibition of leaf [Formula: see text] assimilation, whereas up-regulation of N metabolism in roots could have mitigated the acclimatory effect of eCO2 in HN plants.

Sustained enhancement of photosynthesis in coffee trees grown under free-air CO2 enrichment conditions: disentangling the contributions of stomatal, mesophyll, and biochemical limitations.

Coffee (Coffea spp.), a globally traded commodity, is a slow-growing tropical tree species that displays an improved photosynthetic performance when grown under elevated atmospheric CO2 concentrations ([CO2]). To investigate the mechanisms underlying this response, two commercial coffee cultivars (Catuaí and Obatã) were grown using the first free-air CO2 enrichment (FACE) facility in Latin America. Measurements were conducted in two contrasting growth seasons, which were characterized by the high (February) and low (August) sink demand. Elevated [CO2] led to increases in net photosynthetic rates (A) in parallel with decreased photorespiration rates, with no photochemical limitations to A. The stimulation of A by elevated CO2 supply was more prominent in August (56% on average) than in February (40% on average). Overall, the stomatal and mesophyll conductances, as well as the leaf nitrogen and phosphorus concentrations, were unresponsive to the treatments. Photosynthesis was strongly limited by diffusional constraints, particularly at the stomata level, and this pattern was little, if at all, affected by elevated [CO2]. Relative to February, starch pools (but not soluble sugars) increased remarkably (>500%) in August, with no detectable alteration in the maximum carboxylation capacity estimated on a chloroplast [CO2] basis. Upregulation of A by elevated [CO2] took place with no signs of photosynthetic downregulation, even during the period of low sink demand, when acclimation would be expected to be greatest.

The determiner of photosynthetic acclimation induced by biochemical limitation under elevated CO2 in japonica rice.

Photosynthetic acclimation to prolonged elevated CO2 could be attributed to the two limited biochemical capacity, ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) carboxylation and ribulose-1,5-bisphosphate (RuBP) regeneration, however, which one is the primary driver is unclear. To quantify photosynthetic acclimation induced by biochemical limitation, we investigated photosynthetic characteristics and leaf nitrogen allocation to photosynthetic apparatus (Rubisco, bioenergetics, and light-harvesting complex) in a japonica rice grown in open-top chambers at ambient CO2 and ambient CO2+200 µmol mol-1 (e [CO2]). Results showed that photosynthesis was stimulated under e [CO2], but concomitantly, photosynthetic acclimation obviously occurred across the whole growth stages. The content of leaf nitrogen allocation to Rubisco and biogenetics was reduced by e [CO2], while not in light-harvesting complex. Unlike the content, there was little effects of CO2 enrichment on the percentage of nitrogen allocation to photosynthetic components. Additionally, leaf nitrogen did not reallocate within photosynthetic apparatus until the imbalance of sink-source under e [CO2]. The contribution of biochemical limitations, including Rubisco carboxylation and RuBP regeneration, to photosynthetic acclimation averaged 36.2% and 63.8% over the growing seasons, respectively. This study suggests that acclimation of photosynthesis is mainly driven by RuBP regeneration limitation and highlights the importance of RuBP regeneration relative to Rubisco carboxylation in the future CO2 enrichment.

Photosynthetic regulation in response to strontium stress in moss Racomitrium japonicum L.

Strontium (Sr2+) pollution and its biological effects are of great concern including photosynthetic regulation, which is fundamental to environmental responses, especially for bryophytes during their terrestrial adaptation. Alternative electron flows mediated by flavodiiron proteins (FLVs) and cyclic electron flow (CEF) in photosystem I (PSI) are crucial to abiotic stresses moss responses; however, little is known about the moss photosynthesis regulation under nuclide treatment. We measured chlorophyll fluorescence parameters in PSI, photosystem II (PSII) and the P700 redox state, oxidative stress in the moss Racomitrium japonicum under low (5 mg/L), moderate (50 mg/L) and high (500 mg/L) Sr2+ stress level. Moderate and high Sr2+ stress triggered H2O2 and malondialdehyde (MDA) generation, and catalase (CAT) activity increases, which are involved in reactive oxygen species regulation. The significant PSII photochemistry (Fv/Fm), Chla/chlb, Y(I)/Y(II), Y(NA), Y(ND) and ETRI-ETRII decreases at moderate and high Sr2+, and the Y(I), Y(II) decreases at high Sr2+ revealed the photo-inhibition and photo-damage in PSI and PSII by moderate and high Sr2+ stress. The nonphotochemical quenching (NPQ) increased significantly at moderate and high Sr2+ stress, reflecting a heat-dissipation-related photo-protective mechanism in antenna system and reaction centers. Moreover, rapid re-oxidation of P700 indicated that FLV-dependent flows significantly regulated PSI redox state under moderate and high Sr2+ stress. and CEF upregulation was found at low Sr2+. Finally, photosynthetic acclimation to Sr2+ stress in R. japonicum was linked to FLVs and CEF adjustments.

Structure and chlorophyll fluorescence of heteroblastic foliage affect first-year growth in Pinus massoniana Lamb. seedlings.

Pine seedlings exhibit heteroblastic foliage (primary and secondary needles) during seedling development. However, few trials have studied how heteroblastic foliage influences pine seedling growth by seasonal variation. This study first investigated the anatomical differences between the primary and secondary needles of one-year-old Pinus massoniana seedlings. We measured chlorophyll fluorescence (ChlF) and evaluated the photoprotective mechanisms and light energy partitioning of these heteroblastic leaves from September to November. The results showed that the primary needles, as juvenile foliage, had a greater fraction of mesophyll tissue and stomata. In addition, the primary needles had two vascular bundles, and shorter distance from xylem and phloem to mesophyll cells, exhibiting a luxury growth strategy of rapidly obtaining high returns. The ChlF parameters indicated that the primary needles maintained a relatively high level of photoprotection by thermal dissipation (nonphotochemical quenching (NPQ)) and nonregulated energy dissipation (Y(NO)). The secondary needles, representing mature foliage, had greater area of xylem and phloem tissues. The contents of Chl b and carotenoids (Car) significantly increased in November, promoting φPo and photoprotection, which suggested that the secondary needles were more resistant to low temperatures. During the whole light response process of secondary needles, the increases in the electron transfer rate (ETR) and light energy utilization efficiency (α) helped to increase the actual photosynthetic quantum yield (Y(II)) by reducing energy dissipation by decreasing the proportion of regulated energy dissipation (Y(NPQ)) and Y(NO). Given the sensitivity of this heteroblastic foliage to environmental changes, the practical use and extension of P. massoniana for afforestation purposes should be carried out with caution.

NaCl Pretreatment Enhances the Low Temperature Tolerance of Tomato Through Photosynthetic Acclimation.

Plants often need to withstand multiple types of environmental stresses (e.g., salt and low temperature stress) because of their sessile nature. Although the physiological responses of plants to single stressor have been well-characterized, few studies have evaluated the extent to which pretreatment with non-lethal stressors can maintain the photosynthetic performance of plants in adverse environments (i.e., acclimation-induced cross-tolerance). Here, we studied the effects of sodium chloride (NaCl) pretreatment on the photosynthetic performance of tomato plants exposed to low temperature stress by measuring photosynthetic and chlorophyll fluorescence parameters, stomatal aperture, chloroplast quality, and the expression of stress signaling pathway-related genes. NaCl pretreatment significantly reduced the carbon dioxide assimilation rate, transpiration rate, and stomatal aperture of tomato leaves, but these physiological acclimations could mitigate the adverse effects of subsequent low temperatures compared with non-pretreated tomato plants. The content of photosynthetic pigments decreased and the ultra-microstructure of chloroplasts was damaged under low temperature stress, and the magnitude of these adverse effects was alleviated by NaCl pretreatment. The quantum yield of photosystem I (PSI) and photosystem II (PSII), the quantum yield of regulatory energy dissipation, and non-photochemical energy dissipation owing to donor-side limitation decreased following NaCl treatment; however, the opposite patterns were observed when NaCl-pretreated plants were exposed to low temperature stress. Similar results were obtained for the electron transfer rate of PSI, the electron transfer rate of PSII, and the estimated cyclic electron flow value (CEF). The production of reactive oxygen species induced by low temperature stress was also significantly alleviated by NaCl pretreatment. The expression of ion channel and tubulin-related genes affecting stomatal aperture, chlorophyll synthesis genes, antioxidant enzyme-related genes, and abscisic acid (ABA) and low temperature signaling-related genes was up-regulated in NaCl-pretreated plants under low temperature stress. Our findings indicated that CEF-mediated photoprotection, stomatal movement, the maintenance of chloroplast quality, and ABA and low temperature signaling pathways all play key roles in maintaining the photosynthetic capacity of NaCl-treated tomato plants under low temperature stress.