Abstract
BackgroundThe variation of growth and cold tolerance of two natural Arabidopsis accessions, Cvi (cold sensitive) and Rschew (cold tolerant), was analysed on a proteomic, phosphoproteomic and metabolomic level to derive characteristic information about genotypically distinct strategies of metabolic reprogramming and growth maintenance during cold acclimation.ResultsGrowth regulation before and after a cold acclimation period was monitored by recording fresh weight of leaf rosettes. Significant differences in the shoot fresh weight of Cvi and Rschew were detected both before and after acclimation to low temperature. During cold acclimation, starch levels were found to accumulate to a significantly higher level in Cvi compared to Rschew. Concomitantly, statistical analysis revealed a cold-induced decrease of beta-amylase 3 (BAM3; AT4G17090) in Cvi but not in Rschew. Further, only in Rschew we observed an increase of the protein level of the debranching enzyme isoamylase 3 (ISA3; AT4G09020). Additionally, the cold response of both accessions was observed to severely affect ribosomal complexes, but only Rschew showed a pronounced accumulation of carbon and nitrogen compounds. The abundance of the Cold Regulated (COR) protein COR78 (AT5G52310) as well as its phosphorylation was observed to be positively correlated with the acclimation state of both accessions. In addition, transcription factors being involved in growth and developmental regulation were found to characteristically separate the cold sensitive from the cold tolerant accession. Predicted protein-protein interaction networks (PPIN) of significantly changed proteins during cold acclimation allowed for a differentiation between both accessions. The PPIN revealed the central role of carbon/nitrogen allocation and ribosomal complex formation to establish a new cold-induced metabolic homeostasis as also observed on the level of the metabolome and proteome.ConclusionOur results provide evidence for a comprehensive multi-functional molecular interaction network orchestrating growth regulation and cold acclimation in two natural accessions of Arabidopsis thaliana. The differential abundance of beta-amylase 3 and isoamylase 3 indicates a central role of transitory starch degradation in the coordination of growth regulation and the development of stress tolerance. Finally, our study indicates naturally occurring differential patterns of C/N balance and protein synthesis during cold acclimation.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-015-0668-1) contains supplementary material, which is available to authorized users.
Highlights
The variation of growth and cold tolerance of two natural Arabidopsis accessions, Cvi and Rschew, was analysed on a proteomic, phosphoproteomic and metabolomic level to derive characteristic information about genotypically distinct strategies of metabolic reprogramming and growth maintenance during cold acclimation
Differential growth of Cvi and Rsch during cold acclimation Growth behaviour of both accessions was characterized by recording the total fresh weight of leaf rosettes from 15 independently grown plants for each acclimation state, i.e. the non-acclimated and acclimated state (Fig. 1a)
Analysis of variance (ANOVA) revealed a significantly higher fresh weight of Rsch plants before and after cold acclimation compared to Cvi (Fig. 1b)
Summary
The variation of growth and cold tolerance of two natural Arabidopsis accessions, Cvi (cold sensitive) and Rschew (cold tolerant), was analysed on a proteomic, phosphoproteomic and metabolomic level to derive characteristic information about genotypically distinct strategies of metabolic reprogramming and growth maintenance during cold acclimation. Reprogramming of primary metabolism plays a crucial role during cold acclimation leading to a changed photosynthetic activity and the accumulation of soluble sugars, amino acids and polyamines. On a whole plant level, it remains elusive whether sugar accumulation may result from reduced sink activity, because growth retardation at low temperatures is stronger than the reduction of photosynthetic activity [21]. It is not clear whether sugars function as cryoprotective substances or because they are substrates for the cryoprotectant synthesis [19]
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