Short-term Acclimation Responses Research Articles

NTRC and thioredoxins m1/m2 underpin the light acclimation of plants on proteome and metabolome levels.

During photosynthesis, plants must manage strong fluctuations in light availability on different time scales, leading to long-term acclimation and short-term responses. However, little is known about the regulation and coordination of these processes and the modulators involved. In this study, we used proteomics, metabolomics, and reverse genetics to investigate how different light environmental factors, such as intensity or variability, affect long-term and short-term acclimation responses of Arabidopsis (Arabidopsis thaliana) and the importance of the chloroplast redox network in their regulation. In the wild type, high light, but not fluctuating light, led to large quantitative changes in the proteome and metabolome, accompanied by increased photosynthetic dynamics and plant growth. This finding supports light intensity as a stronger driver for acclimation than variability. Deficiencies in NADPH-thioredoxin reductase C (NTRC) or thioredoxins m1/m2, but not thioredoxin f1, almost completely suppressed the re-engineering of the proteome and metabolome, with both the induction of proteins involved in stress and redox responses and the repression of those involved in cytosolic and plastid protein synthesis and translation being strongly attenuated. Moreover, the correlations of protein or metabolite levels with light intensity were severely disturbed, suggesting a general defect in the light-dependent acclimation response, resulting in impaired photosynthetic dynamics. These results indicate a previously unknown role of NTRC and thioredoxins m1/m2 in modulating light acclimation at proteome and metabolome levels to control dynamic light responses. NTRC, but not thioredoxins m1/m2 or f1, also improves short-term photosynthetic responses by balancing the Calvin-Benson cycle in fluctuating light.

MITOGEN-ACTIVATED PROTEIN KINASE 4 impacts leaf development, temperature, and stomatal movement in hybrid aspen.

Stomatal movement and density influence plant water use efficiency and thus biomass production. Studies in model plants within controlled environments suggest MITOGEN-ACTIVATED PROTEIN KINASE 4 (MPK4) may be crucial for stomatal regulation. We present functional analysis of MPK4 for hybrid aspen (Populus tremula × tremuloides) grown under natural field conditions for several seasons. We provide evidence of the role of MPK4 in the genetic and environmental regulation of stomatal formation, differentiation, signaling, and function; control of the photosynthetic and thermal status of leaves; and growth and acclimation responses. The long-term acclimation manifested as variations in stomatal density and distribution. Short-term acclimation responses were derived from changes in the stomatal aperture. MPK4 localized in the cytoplasm of guard cells (GCs) was a positive regulator of abscisic acid (ABA)-dependent stomatal closure and nitric oxide metabolism in the ABA-dependent pathways, while to a lesser extent, it was involved in ABA-induced hydrogen peroxide accumulation. MPK4 also affected the stomatal aperture through deregulation of microtubule patterns and cell wall structure and composition, including via pectin methyl-esterification, and extensin levels in the GC wall. Deregulation of leaf anatomy (cell compaction) and stomatal movement, together with increased light energy absorption, resulted in altered leaf temperature, photosynthesis, cell death, and biomass accumulation in mpk4 transgenic plants. Divergence between absorbed energy and assimilated energy is a bottleneck, and MPK4 can participate in the control of energy dissipation (thermal effects). Furthermore, MPK4 can participate in balancing the photosynthetic energy distribution via its effective use in growth or redirection to acclimation/defense responses.

Increased Thermal Sensitivity of a Tropical Marine Gastropod Under Combined CO2 and Temperature Stress

The ability of an organism to alter its physiology in response to environmental conditions offers a short-term defense mechanism in the face of weather extremes resulting from climate change. These often manifest as multiple, interacting drivers, especially pH and temperature. In particular, decreased pH can impose constraints on the biological mechanisms which define thermal limits by throwing off energetic equilibrium and diminishing physiological functions (e.g., in many marine ectotherms). For many species, however, we do not have a detailed understanding of these interactive effects, especially on short-term acclimation responses. Here, we investigated the metabolic plasticity of a tropical subtidal gastropod (Trochus maculatus) to increased levels of CO2 (700 ppm) and heating (+3°C), measuring metabolic performance (Q10 coefficient) and thermal sensitivity [temperature of maximum metabolic rate (TMMR), and upper lethal temperature (ULT)]. Individuals demonstrated metabolic acclimation in response to the stressors, with TMMR increasing by +4.1°C under higher temperatures, +2.7°C under elevated CO2, and +4.4°C under the combined stressors. In contrast, the ULT only increased marginally in response to heating (+0.3°C), but decreased by −2.3°C under CO2, and −8.7°C under combined stressors. Therefore, although phenotypic plasticity is evident with metabolic acclimation, acute lethal temperature limits seem to be less flexible during short-term acclimation.

Differential eco-physiological performances of two pseudocryptic species of the Eurytemora affinis complex (Copepoda, Calanoida) in the St. Lawrence estuarine transition zone: a reciprocal transplant experiment

Abstract The goal of this study was to evaluate and compare the short-term performances and the physiological plasticity of two cryptic species Eurytemora carolleeae and Eurytemora affinis (North-Atlantic clade) by simulating rapid advection from freshwater to brackish water conditions and reciprocally. To do so, two reciprocal transplant experiments without acclimation and under non-limited food condition were performed in the St. Lawrence estuarine transition zone during summer 2011. Results revealed that both species diverged in their short-term acclimation response when facing acute salinity changes that they might encounter when advected through the highly dynamic estuarine transition zone. We show that E. carolleeae could use the brackish environment without loss of performance and energy, while E. affinis needed to reallocate energy from other processes (i.e., reproduction) and required food intake to maintain itself in the freshwater environment. In addition, the transplant experiment highlighted that only 40% of the E. affinis showed short term capacity to acclimate to freshwater conditions, indicating that in situ advection by currents from brackish water to fresh water could be dramatic even for a short time period. Furthermore, the survivors of E. affinis in fresh water might not be able to reproduce, which limits establishment of a sustainable population of E. affinis (North-Atlantic clade) in the tidal freshwater part of the estuarine transition zone. Finally, we highlighted for the first time that both species of this pseudocryptic complex could use lipid remodelling to overcome temperature effects on membrane structure, but further studies are needed to determine the influence of membrane lipid remodelling on salinity tolerance.

Short- and long-term low-salinity acclimation effects on the branchial and intestinal gene expression in the European seabass (Dicentrarchus labrax)

The European seabass (Dicentrarchus labrax) is a teleost remarkably adapted to a wide range of water salinity, through osmoregulatory mechanisms, mainly operating in the gills and the intestine. As an important aquaculture species, its rearing in low-salinity conditions offers benefits for its inland culture. However, this demands a full comprehension of the European seabass osmoregulatory mechanisms and its response to acclimation protocols. The purpose of this study was to evaluate different acclimation protocols in terms of osmoregularity and stress response, following transferring of European seabass juveniles from seawater to freshwater. In addition, nutrient absorption was also examined since drinking rates are sensitive to salinity. The acclimation challenge was applied through three protocols: direct transfer (0 h) to freshwater, gradual transfer during 3 h and during 72 h. The short- (1 h after complete change to freshwater) and long-term effects (after 2 months) of each acclimation protocol were evaluated by assessing the expression of 1. The osmoregulatory genes: Na+/K+-ATPase α1, Na+/K+/2Cl− 1 co-transporter, aquaporins 1 and 3, and the cystic fibrosis transmembrane conductance regulator; 2. The heat shock protein 70 gene; 3. The peptide transporter genes corresponding to PepT1a, PepT1b and PepT2. The short-term acclimation response was pronounced in both gills and the intestine affecting stress-, osmoregulatory- and nutrient-related gene expression. Long-term effects were only evident in the intestine. Direct transfer in freshwater mainly induced a long-term stress response, while the short-term effect was more pronounced in the 3 h-transfer, potentially due to handling. Our results suggest that although the European seabass can withstand direct transfer to low-salinity conditions, a gradual transfer is recommended to prevent long-term stress effects.

Primed Acclimation of Papaya Increases Short-term Water Use But Does Not Confer Long-term Drought Tolerance

Primed acclimation (PA) is a regulated deficit irrigation (RDI) strategy designed to improve or maintain yield under subsequent drought stress. A previous study showed photosynthetic increases in papaya in response to a PA treatment. The present study was undertaken to test the duration of the PA effect when papaya plants were challenged with severe drought stress. Potted plants were stressed at 1, 2, and 3 months after conclusion of a PA treatment consisting of 3 weeks at soil water tension (SWT) of −20 kPa. Measurements included leaf gas exchange, root growth, and organ dry mass partitioning. PA did not reduce net CO2 assimilation (A) during the deficit period. At the end of the PA period, total dry matter accumulation per plant and for each organ was unaffected, but proportional dry matter partitioning to roots was favored. After resuming full irrigation, A increased and whole plant water use was more than doubled in PA-treated plants. However, water use and A of PA-treated plants decreased to reconverge with those of control plants by 6 weeks after the PA treatment. Over the course of the study, PA plants maintained lower stem height to stem diameter ratios, and shorter internode lengths. However, these changes did not improve photosynthetic response to any of the water-deficit treatments. We conclude that papaya exhibits some signs of stress memory, but that rapid short-term acclimation responses dominate papaya responses to soil water deficit.

Physiological traits for improving high temperature stress tolerance in rice

High temperature stress is projected to be one of the major stresses of limiting rice productivity worldwide in future climate change scenario. This review explicates the key physiological traits for tailoring high temperature tolerance in rice. These physiological traits can be used to explore the genetic variability among rice germplasm and to develop the improved genotypes through breeding programs. Traits influenced under high day and night temperature are highlighted for understanding differential temporal and phenological regulation. Application of plant hormones and inorganic elicitor molecules to induce short term acclimation response have been shown to be useful for mitigating high temperature stress effects specifically when applied at critical growth stge.

Effects of elevated carbon dioxide on stomatal characteristics and carbon isotope ratio of Arabidopsis thaliana ecotypes originating from an altitudinal gradient.

Stomatal functioning regulates the fluxes of CO2 and water vapor between vegetation and atmosphere and thereby influences plant adaptation to their habitats. Stomatal traits are controlled by external environmental and internal cellular signaling. The objective of this study was to quantify the effects of CO2 enrichment (CE) on stomatal density (SD)-related properties, guard cell length (GCL) and carbon isotope ratio (δ13 C) of a range of Arabidopsis thaliana ecotypes originating from a wide altitudinal range [50-1260 m above sea level (asl)], and grown at 400 and 800 ppm [CO2 ], and thereby elucidate the possible adaptation and acclimation responses controlling stomatal traits and water use efficiency (WUE). There was a highly significant variation among ecotypes in the magnitude and direction of response of stomatal traits namely, SD and stomatal index (SI) and GCL, and δ13 C to CE, which represented a short-term acclimation response. A majority of ecotypes showed increased SD and SI with CE with the response not depending on the altitude of origin. Significant ecotypic variation was shown in all stomatal traits and δ13 C at each [CO2 ]. At 400 ppm, means of SD, SI and GCL for broad altitudinal ranges, i.e. low (<100 m), mid (100-400 m) and high (>400 m), increased with increasing altitude, which represented an adaptation response to decreased availability of CO2 with altitude. δ13 C was negatively correlated to SD and SI at 800 ppm but not at 400 ppm. Our results highlight the diversity in the response of key stomatal characters to CE and altitude within the germplasm of A. thaliana and the need to consider this diversity when using A. thaliana as a model plant.

Latitudinal and seasonal effects on short-term acclimation of floating kelp species from the South-East Pacific

Floating seaweeds are important dispersal vehicles for many organisms in cold-temperate waters between latitudes 30° and 60°. Molecular studies suggested that long-distance rafting of seaweeds is more prevalent at the polar edges of their distribution but knowledge about their physiological status at high latitudes is limited. Seasonal short-term field experiments were conducted along a latitudinal gradient (30°, 37° and 54°S) with floating kelps Macrocystis pyrifera and Durvillaea antarctica. Kelps were tethered at the sea surface for 14d during austral winter and summer to examine their acclimation potential in floating conditions. Biomass changes, reproductive status and physiological traits (chlorophyll a fluorescence, pigments, phlorotannins and antioxidant capacity) were evaluated after 7d and 14d of floating. Biomass changes (positive or negative) depended on species and latitude: at low latitudes (Coquimbo) both species lost biomass during both seasons while at mid latitudes (Concepción) they grew during summer but not in winter. Species-specific responses were observed at high latitudes (Pta. Arenas) with floating M. pyrifera growing in summer and D. antarctica in winter. Both species were able to maintain reproductive status mainly in winter, but at mid latitudes M. pyrifera also showed high reproductive activity during summer. Physiological adjustment was detected for both species at day 7 and upheld until the end of the experiment (14d). Latitudinal changes in photosynthetic variables (maximum quantum yield and pigments) were more evident in summer conditions, M. pyrifera showing decreases in Fv/Fm and pigment levels at low and high latitudes while in D. antarctica these variables increased with latitude. Phlorotannin contents varied with latitude but showed an opposing pattern in the two kelp species, with high concentrations at low latitudes for M. pyrifera and at high latitudes for D. antarctica. The floating kelps maintained high antioxidant capacity during the experiments. The short-term acclimation responses support the hypothesis of long-distance dispersal at high latitudes for both floating kelp species. The acclimation potential differed between the two species depending on the season, especially at mid and high latitudes. Summer conditions were favorable for floating M. pyrifera at high latitudes and for both species at mid latitudes in which a combination of increasing radiation and moderate temperature can stimulate growth. The results confirm that kelp rafting is favored at mid/high latitudes but suggest that in polar waters (>60°) low temperatures and light limitations might suppress growth of floating seaweeds.

Evolution of salt tolerance in a laboratory reared population of Chlamydomonas reinhardtii

Understanding the genetic underpinnings of adaptive traits in microalgae is important for the study of evolution and for applied uses. We used long-term selection under a regime of serial transfers with haploid populations of the green alga Chlamydomonas reinhardtii raised in liquid TAP medium containing 200 mM NaCl. After 1255 generations, evolved salt (ES) populations could grow as rapidly in high salt medium as progenitor cells (progenitor light [PL]). Transcriptome data were analysed to elucidate the basis of salt tolerance in ES cells when compared with PL cells and to cells incubated for 48 h in high salt medium (progenitor salt [PS], the short-term acclimation response). These data demonstrate that evolved and short-term acclimation responses to salt stress differ fundamentally from each other. Progenitor salt cells exhibit well-known responses to salt stress such as reduction in photosynthesis, upregulation of glycerophospholipid signaling, and upregulation of the transcription and translation machinery. In contrast, ES cells show downregulation of genes involved in the stress response and in transcription/translation. Our results suggest that gene-rich mixotrophic lineages such as C. reinhardtii may be able to adapt rapidly to abiotic stress engendered either by a rapidly changing climate or physical vicariance events that isolate populations in stressful environments.

Population-level variation of Fraxinus americana (white ash) is influenced by precipitation differences across the native range

We investigated the potential of Fraxinus americana L. to adapt to climate change by comparing diameter growth, survival and physiological status of 44 populations of 30-year-old trees originating from throughout the species range and grown in a common garden. Populations originating closest to the latitude of the common garden had the most rapid diameter growth and the highest survival. Among populations originating within a narrow latitudinal band along an east-west gradient of decreasing precipitation, those from the drier western end were best adapted to the dry climate of the common garden site, as judged by survival, stem circumference, leaf and wood carbon isotope ratios, leaf mass per area and leaf nitrogen concentration. These findings suggest that eastern populations may not perform well under the hotter and drier conditions predicted by climate change scenarios. Moreover, in the event of significant climate change, the short-term acclimation responses (within a generation) of F. americana may be insufficient to ensure the continued vigor or survival of this species throughout much of its present range.

Ontogeny of salinity tolerance and hyper-osmoregulation by embryos of the intertidal crabs Hemigrapsus edwardsii and Hemigrapsus crenulatus (Decapoda, Grapsidae): Survival of acute hyposaline exposure

The adults of Hemigrapsus edwardsii and Hemigrapsus crenulatus are euryhaline crabs and strong hyper-osmoregulators. Their embryos are carried externally attached to the abdominal pleopods of female crabs, where they are exposed to temporal and spatial changes in salinity associated with their intertidal and estuarine habitats. Although embryos lack the branchial and excretory organs responsible for adult osmoregulation, post-gastrula embryos were highly tolerant of exposure to hypo-osmotic sea water. Detached eggs (embryos + envelopes), of both species, at all developmental stages between gastrulation and hatching, exhibited 80–100% survival for periods up to 96 h in sea water (osmolality, 1050 mmol kg − 1 ) and in dilutions to 50%, 10%, and 1%. Cleavage stages were less tolerant of dilution; H. edwardsii, < 50% survived 24 h in 10% sea water; H. crenulatus < 50% survived 6 h in 10% sea water. Post-gastrulation stages strongly hyper-osmoregulated but cleavage stages were hyper-osmoconformers (maintaining internal osmolality ≈ 150 mmol kg − 1 above external). Osmoregulatory capacity was reduced just prior hatching, particularly in H. crenulatus, although salinity tolerance remained high. Gastrulation therefore marks a critical stage in the ontogeny of osmoregulation and salinity tolerance. Total Na +/K +-ATPase activity increased greatly during embryogenesis of H. crenulatus (undetectable in blastulae; gastrulae 0.31 ± 0.05 pmol P i embryo − 1 min − 1 ; pre-hatching 16.4 ± 1.0 pmol P i embryo − 1 min − 1 ). Na +/K +-ATPase activity increased in embryos exposed to dilute sea water for 24 h implicating regulation of this transporter in a short-term acclimation response.