Multilevel genomic analysis of the response of transcripts, enzyme activities and metabolites inArabidopsisrosettes to a progressive decrease of temperature in the non‐freezing range

Abstract

This paper characterizes the transcriptional and metabolic response of a chilling-tolerant species to an increasingly large decrease of the temperature. Arabidopsis Col-0 was grown at 20°C and transferred to 17, 14, 12, 10 or 8°C for 6 and 78 h, before harvesting the rosette and profiling >22 000 transcripts, >20 enzyme activities and >80 metabolites. Most parameters showed a qualitatively similar response across the entire temperature range, with the amplitude increasing as the temperature decreased. Transcripts typically showed large changes after 6 h, which were often damped by 78 h. Genes were induced for sucrose, proline, raffinose, tocopherol and polyamine synthesis, phenylpropanoid and flavonoid metabolism, fermentation, non-phosphorylating mitochondrial electron transport, RNA processing, and protein synthesis, targeting and folding. Genes were repressed for carbonic anhydrases, vacuolar invertase, and ethylene and jasmonic acid signalling. While some enzyme activities and metabolites changed rapidly, most changed slowly. After 6 h, there was an accumulation of phosphorylated intermediates, a shift of partitioning towards sucrose, and a perturbation of glycine decarboxylation and nitrogen metabolism. By 78 h, there was an increase of the overall protein content and many enzyme activities, a general increase of carbohydrates, organic and amino acids, and an increase of many stress-responsive metabolites including raffinose, proline, tocopherol and polyamines. When the responses of transcripts and metabolism were compared, there was little agreement after 6 h, but considerable agreement after 78 h. Comparison with the published studies indicated that much, but not all, of the response was orchestrated by the CBF programme. Overall, our results showed that transcription and metabolism responded in a continuous manner across a wide range of temperatures.The general increase of enzyme activities and metabolites emphasized the positive and compensatory nature of this response.

Regulation of Leaf Starch Degradation by Abscisic Acid Is Important for Osmotic Stress Tolerance in Plants

“…In response to acute temperature shock, plants mobilize starch at time when biosynthesis would be expected (e.g., in the middle of the light period), resulting in the accumulation of maltose, the major starch catabolite, and of its deriving sugars (Usadel et al, 2008a;Purdy et al, 2013;Guy, 2005, 2004;Sitnicka and Orzechowski, 2014;Yano et al, 2005;Kaplan et al, 2007). Similar rearrangements of starch metabolism are observed when plants are subject to short periods of oxidative or osmotic stress (Scarpeci and Valle, 2008;Zanella et al, 2016;Valerio et al, 2011;Geigenberger et al, 1997).…”

Advances in detection of stress tolerance in plants through metabolomics approaches

“…Plant system responses to salt stress are finetuned to the increasing stress by linear, plateau-and threshold-like dose-dependent molecular and metabolic changes (Sanchez et al, 2008). Similar responses were also detected during acclimation to both cold and drought in Arabidopsis thaliana (Wilin et al, 2007;Usadel et al, 2008;Tähtiharju, and Palva, 2001).…”

“…For example, levels of sugar alcohols, sugars, and amino acids usually amplify with response to diverse stresses. Proline is mostly accumulated on drought, salinity and cold stress but declines during heat stress (Usadel et al, 2008;Urano et al, 2009;Lugan et al, 2010). In most of the studies, amount of TCA-cycle intermediates and organic acids become deteriorated in glycophytes after salinity stress (Gong et al, 2005), but improved upon drought or temperature stress (Kaplan et al, 2004;Usadel et al, 2008;Urano et al, 2009).…”

The art of growing plants for experimental purposes: a practical guide for the plant biologist

“…The first example combines data from two independent experiments where genome-wide mRNA expression was measured in Arabidopsis thaliana (L.) Heynh. plants that were pre-grown at 20À22 C and subsequently switched to low temperatures (4À8 C; Vogel et al 2005;Usadel et al 2008). In both experiments,~800-900 of the 25 000 genes were found to be significantly up-or downregulated, which, therefore, seems a reproducible result.…”

“…Laboratories Total leaf area (%) Vogel et al (2005) 549 Usadel et al (2008) 674 242 Vogel et al (2005) and Usadel et al (2008). (b) Leaf area of Arabidopsis thaliana Col. plants grown with the same protocol, the same seed stock and the same soil in growth rooms of nine different laboratories.…”