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Dynamics of metabolic responses to periods of combined heat and drought in Arabidopsis thaliana under ambient and elevated atmospheric CO2.

ABSTRACT: As a consequence of global change processes, plants will increasingly be challenged by extreme climatic events, against a background of elevated atmospheric CO2. We analysed responses of Arabidopsis thaliana to periods of a combination of elevated heat and water deficit at ambient and elevated CO2 in order to gain mechanistic insights regarding changes in primary metabolism. Metabolic changes induced by extremes of climate are dynamic and specific to different classes of molecules. Concentrations of soluble sugars and amino acids increased transiently after short (4-d) exposure to heat and drought, and readjusted to control levels under prolonged (8-d) stress. In contrast, fatty acids showed persistent changes during the stress period. Elevated CO2 reduced the impact of stress on sugar and amino acid metabolism, but not on fatty acids. Integrating metabolite data with transcriptome results revealed that some of the metabolic changes were regulated at the transcriptional level. Multivariate analyses grouped metabolites on the basis of stress exposure time, indicating specificity in metabolic responses to short and prolonged stress. Taken together, the results indicate that dynamic metabolic reprograming plays an important role in plant acclimation to climatic extremes. The extent of such metabolic adjustments is less under high CO2, further pointing towards the role of high CO2 in stress mitigation.

SUBMITTER: Zinta G

PROVIDER: S-EPMC6019062 | biostudies-literature | 2018 Apr

REPOSITORIES: biostudies-literature

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Dynamics of metabolic responses to periods of combined heat and drought in Arabidopsis thaliana under ambient and elevated atmospheric CO2.

Zinta Gaurav G AbdElgawad Hamada H Peshev Darin D Weedon James T JT Van den Ende Wim W Nijs Ivan I Janssens Ivan A IA Beemster Gerrit T S GTS Asard Han H

Journal of experimental botany 20180401 8

As a consequence of global change processes, plants will increasingly be challenged by extreme climatic events, against a background of elevated atmospheric CO2. We analysed responses of Arabidopsis thaliana to periods of a combination of elevated heat and water deficit at ambient and elevated CO2 in order to gain mechanistic insights regarding changes in primary metabolism. Metabolic changes induced by extremes of climate are dynamic and specific to different classes of molecules. Concentration ...[more]

PMID: 29462345

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Project description:We were awarded a BBSRC grant about a year ago to undertake some affymetrix gene chip profiling of light and CO2 systemic signalling in Arabidopsis. The design of the proposed experiment is given below and the appropriate funding has been provided by the BBSRC. The aim of the project is to identify the temporal profile of those genes that respond to light and CO2 systemic signals in developing leaves. Moreover, as thes two signals have opposing effects on leaf development to ascertain whether they involve similar or parallel signalling pathways. The experiment is to examine the effect of exposing mature leaves to high CO2 or low light or both on the gene expression profile of developing leaves. We already have data for maize that changes in gene expression profile occur within 4h and that there are a variety of temporal responses that differ between individual gene transcripts. We have also demonstrated that Arabidopsis leaf development is altered by these systemmic signals and that lesions in the jasmonate and ethylene signalling pathways block these responses. Our experimental design is shown below: We have 4 treatments and 7 timepoints. (0, 2, 4, 12, 24, 48, 96 h) We would sample from 5 individual plants that would be pooled for each RNA preparation. This would require 28 chips and this would include extra replication of the 0 time-point control (deemed by many as nessary). Experimental details: All plants were germinated for 7 days under the following conditions: Humax multi-purpose compost, ambient carbon dioxide (370 ppm) and ambient light (250 µmol/m/s), constant temperature of 20°C and a 10 h photoperiod (8 am until 6 pm). After a week the the seedlings were potted up into 104-cell plug trays for a further 2 weeks and then potted up into 10 cm pots and the bottom part of the signalling cuvette system attached (see Lake et al., Nature 10th May 2001 Vol. 411, pp 154). Twenty four, 4 week old plants, then had the top part of the signalling system attached, trapping leaf insertions 5-13. Humidified, ambient air was passed through them at 500 mls/min via an oil-free air compressor. The three target leaves (19-21) were then marked with non-toxic, acrylic paint. After a 24 h period (the plants were sealed into the cuvettes from 10 am until 10am) of adjustment, the experiment was started by harvesting the target leaves from 4 plants and immediately freezing the tissue in liquid nitrogen to give the 0 h sample before RNA extraction. The remaining 20 plants were divided into 4 groups of five and given one of the following treatments: Ambient carbon dioxide/ambient light (Control) (A) Elevated carbon dioxide (750 ppm)/ambient light (E) Ambient carbon dioxide/low light (50 µmol/m/s) (AS) Elevated carbon dioxide/low light (ES) - For the Elevated CO2, elevated CO2 was pumped in using a CT room next door set to same temperature but with a CO2 cylinder inside and the same pump as used in the ambient room to supply the elevated CO2 laden, humidified air into the signalling room using rubber tubing. - Shade treatment consisted of neutral density filter (Cat. 210 0.6ND, Lee Filters) that had a hole cut in the middle to allow the middle developing leaves to grow through. A timecourse of 2, 4, 12, 24, 48 and 96 h were carried out each using a batch of 24 plants. This whole process was repeated with another batch of 24 plants at the same developmental stage to give a 2, 4, 12, 24, 48 and 96 hour sample from each of the four treatments. The whole timecourse was then repeated 4 times. For the mature leaves: We had 8 chips left over so we devised this little experiment to assess the gene changes that were occurring in the enclosed, treated, mature leaves that were signalling the environment to the young developing leaves. Experimenter name = Simon Coupe Experimenter phone = 0114 222 4115 Experimenter fax = 0114 222 0002 Experimenter institute = University of Sheffield Experimenter address = Animal and Plant Sciences Experimenter address = University of Sheffield Experimenter address = Western Bank Experimenter address = Sheffield Experimenter zip/postal_code = S10 2TN Experimenter country = UK Keywords: development_or_differentiation_design; growth_condition_design

Project description:Genome-wide transcriptional profiling of Arabidopsis thaliana to a combination of heatwave and drought under ambient and elevated CO2. Goal of this study was elucidate the transcriptional responses to a combination of heat wave and drought, and to see how these responses are modifed under future climate (high) CO2. Climate changes increasingly threaten plant growth and productivity. Such changes are complex and involve multiple environmental factors, including rising CO2 levels and climate extreme events. As the molecular and physiological mechanisms underlying plant responses to realistic future climate extreme conditions are still poorly understood, a multiple organizational level-analysis (i.e. eco-physiological, biochemical and transcriptional) was performed, using Arabidopsis exposed to incremental heat wave and water deficit under elevated CO2.The climate extreme resulted in biomass reduction, photosynthesis inhibition, and considerable increases in stress parameters. Photosynthesis was a major target as demonstrated at the physiological and transcriptional levels. In contrast, the climate extreme treatment induced a protective effect on oxidative membrane damage, most likely as a result of strongly increased lipophilic antioxidants and membrane-protecting enzymes. Elevated CO2 significantly mitigated the negative impact of a combined heat and drought, as apparent in biomass reduction, photosynthesis inhibition, chlorophyll fluorescence decline, H2O2 production and protein oxidation. Analysis of enzymatic and molecular antioxidants revealed that the stress-mitigating CO2 effect operates through up-regulation of antioxidant defense metabolism, as well as by reduced photorespiration resulting in lowered oxidative pressure. Therefore, exposure to future climate extreme episodes will negatively impact plant growth and production, but elevated CO2 is likely to mitigate this effect. Transcriptome analysis was performed by Agilent Arabidopsis (V4) 4x44K platform which represented all known genes in the Arabidopsisgenome. Experiments were performed using a modified loop design (Knapen et al., 2009). This design consisted of total 8 arrays; sample from each treatment was labelled once and has 4 biological replicates, two of which were labelled in red and two in green

Dataset Information

Dynamics of metabolic responses to periods of combined heat and drought in Arabidopsis thaliana under ambient and elevated atmospheric CO2.

Publications

Dynamics of metabolic responses to periods of combined heat and drought in Arabidopsis thaliana under ambient and elevated atmospheric CO2.

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