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Light quality modulates metabolic synchronization over the diel phases of crassulacean acid metabolism.

ABSTRACT: Temporal compartmentation of carboxylation processes is a defining feature of crassulacean acid metabolism and involves circadian control of key metabolic and transport steps that regulate the supply and demand for carbon over a 24h cycle. Recent insights on the molecular workings of the circadian clock and its connection with environmental inputs raise new questions on the importance of light quality and, by analogy, certain photoreceptors for synchronizing the metabolic components of CAM. The present work tested the hypothesis that optimal coupling of stomatal conductance, net CO2 uptake, and the reciprocal turnover of carbohydrates and organic acids over the diel CAM cycle requires both blue and red light input signals. Contrasting monochromatic wavelengths of blue, green, and red light (i.e. 475, 530, 630nm) with low fluence rates (10 ?mol m(-2) s(-1)) were administered for 16 hours each diel cycle for a total treatment time of 48 hours to the obligate CAM bromeliad, Aechmea 'Maya'. Of the light treatments imposed, low-fluence blue light was a key determinant in regulating stomatal responses, organic acid mobilization from the vacuole, and daytime decarboxylation. However, the reciprocal relationship between starch and organic acid turnover that is typical for CAM was uncoupled under low-fluence blue light. Under low-fluence red or green light, the diel turnover of storage carbohydrates was orchestrated in line with the requirements of CAM, but a consistent delay in acid consumption at dawn compared with plants under white or low-fluence blue light was noted. Consistent with the acknowledged influences of both red and blue light as input signals for the circadian clock, the data stress the importance of both red and blue-light signalling pathways for synchronizing the metabolic and physiological components of CAM over the day/night cycle.

SUBMITTER: Ceusters J

PROVIDER: S-EPMC4085966 | biostudies-literature | 2014 Jul

REPOSITORIES: biostudies-literature

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Light quality modulates metabolic synchronization over the diel phases of crassulacean acid metabolism.

Ceusters Johan J Borland Anne M AM Taybi Tahar T Frans Mario M Godts Christof C De Proft Maurice P MP

Journal of experimental botany 20140506 13

Temporal compartmentation of carboxylation processes is a defining feature of crassulacean acid metabolism and involves circadian control of key metabolic and transport steps that regulate the supply and demand for carbon over a 24h cycle. Recent insights on the molecular workings of the circadian clock and its connection with environmental inputs raise new questions on the importance of light quality and, by analogy, certain photoreceptors for synchronizing the metabolic components of CAM. The ...[more]

PMID: 24803500

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Project description:BACKGROUND:Crassulacean acid metabolism (CAM), a specialized mode of photosynthesis, enables plant adaptation to water-limited environments and improves photosynthetic efficiency via an inorganic carbon-concentrating mechanism. Kalanchoë fedtschenkoi is an obligate CAM model featuring a relatively small genome and easy stable transformation. However, the molecular responses to light quality and intensity in CAM plants remain understudied. RESULTS:Here we present a genome-wide expression atlas of K. fedtschenkoi plants grown under 12 h/12 h photoperiod with different light quality (blue, red, far-red, white light) and intensity (0, 150, 440, and 1,000 ?mol m-2 s-1) based on RNA sequencing performed for mature leaf samples collected at dawn (2 h before the light period) and dusk (2 h before the dark period). An eFP web browser was created for easy access of the gene expression data. Based on the expression atlas, we constructed a light-responsive co-expression network to reveal the potential regulatory relationships in K. fedtschenkoi. Measurements of leaf titratable acidity, soluble sugar, and starch turnover provided metabolic indicators of the magnitude of CAM under the different light treatments and were used to provide biological context for the expression dataset. Furthermore, CAM-related subnetworks were highlighted to showcase genes relevant to CAM pathway, circadian clock, and stomatal movement. In comparison with white light, monochrome blue/red/far-red light treatments repressed the expression of several CAM-related genes at dusk, along with a major reduction in acid accumulation. Increasing light intensity from an intermediate level (440 ?mol m-2 s-1) of white light to a high light treatment (1,000 ?mol m-2 s-1) increased expression of several genes involved in dark CO2 fixation and malate transport at dawn, along with an increase in organic acid accumulation. CONCLUSIONS:This study provides a useful genomics resource for investigating the molecular mechanism underlying the light regulation of physiology and metabolism in CAM plants. Our results support the hypothesis that both light intensity and light quality can modulate the CAM pathway through regulation of CAM-related genes in K. fedtschenkoi.

Project description:The cold acclimation process is regulated by many factors like ambient temperature, day length, light intensity, or hormonal status. Experiments with plants grown under different light quality conditions indicate that the plant response to cold is also a light-quality-dependent process. Here, the role of light quality in the cold response was studied in 1-month-old Arabidopsis thaliana (Col-0) plants exposed for 1 week to 4°C at short-day conditions under white (100 and 20 μmol m-2s-1), blue, or red (20 μmol m-2s-1) light conditions. An upregulated expression of CBF1, inhibition of photosynthesis, and an increase in membrane damage showed that blue light enhanced the effect of low temperature. Interestingly, cold-treated plants under blue and red light showed only limited freezing tolerance compared to white light cold-treated plants. Next, the specificity of the light quality signal in cold response was evaluated in Arabidopsis accessions originating from different and contrasting latitudes. In all but one Arabidopsis accession, blue light increased the effect of cold on photosynthetic parameters and electrolyte leakage. This effect was not found for Ws-0, which lacks functional CRY2 protein, indicating its role in the cold response. Proteomics data confirmed significant differences between red and blue light-treated plants at low temperatures and showed that the cold response is highly accession-specific. In general, blue light increased mainly the cold-stress-related proteins and red light-induced higher expression of chloroplast-related proteins, which correlated with higher photosynthetic parameters in red light cold-treated plants. Altogether, our data suggest that light modulates two distinct mechanisms during the cold treatment - red light-driven cell function maintaining program and blue light-activated specific cold response. The importance of mutual complementarity of these mechanisms was demonstrated by significantly higher freezing tolerance of cold-treated plants under white light.

Project description:The cold acclimation process is regulated by many factors like ambient temperature, day length, light intensity, or hormonal status. Experiments with plants grown under different light-quality conditions indicate that the plant response to cold is also a light-quality-dependent process. Here, the role of light quality in the cold response was studied in one-month-old Arabidopsis thaliana (Col‐0) plants exposed for one week to 4 °C at short‐day conditions under white (100 and 20 μmol m‐2s‐1), blue or red (20 μmol m‐2s‐1) light conditions. An upregulated expression of CBF1, an inhibition of photosynthesis, and an increase in membrane damage showed that blue light enhanced the effect of low temperature. Interestingly, cold-treated plants under blue and red light showed only limited freezing tolerance compared to white light cold-treated plants. Next, the specificity of the light quality signal in cold response was evaluated in Arabidopsis accessions originating from different and contrasting latitudes. In all but one Arabidopsis accessions, blue light increased the effect of cold on photosynthetic parameters and electrolyte leakage. This effect was not found for Ws-0, which lacks functional CRY2 protein, indicating its role in the cold response. Proteomics data confirmed significant differences between red and blue light treated plants at low temperature and showed that the cold response is highly accession specific. In general, blue light increased mainly the cold-stress related proteins and red light induced higher expression of chloroplast-related proteins, which correlated with higher photosynthetic parameters in red light cold-treated plants. Altogether, our data suggest that light modulates two distinct mechanisms during the cold treatment - red light driven cell function maintaining program and blue light activated specific cold response. The importance of mutual complementarity of these mechanisms was demonstrated by significantly higher freezing tolerance of cold-treated plants under white light.

Dataset Information

Light quality modulates metabolic synchronization over the diel phases of crassulacean acid metabolism.

Publications

Light quality modulates metabolic synchronization over the diel phases of crassulacean acid metabolism.

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