Plasticity of the primary metabolome in 241 cold grown Arabidopsis thaliana accessions and its relation to natural habitat temperature

Abstract

In the present study, 241 natural accessions of Arabidopsis thaliana were grown under two different temperature regimes, 16 °C and 6 °C, and growth parameters were recorded together with metabolite profiles to investigate the natural variation in metabolic responses and growth rates. Primary metabolism and growth rates of accessions significantly differed between accessions and both growth conditions. Relative growth rates showed high correlations to specific metabolite pools. Metabolic distances based on whole metabolite profiles were built from principal component centroids between both growth setups. Genomic prediction using ridge-regression best linear unbiased prediction (rrBLUP) revealed a significant prediction accuracy of metabolite profiles in both conditions and metabolic distances, which suggests a tight relationship between genome and primary metabolome. GWAS analysis revealed significantly associated SNPs for a number of metabolites, especially for fumarate metabolism at low temperature. A highly significant correlation was observed between metabolic distances and maximum temperature in the original growth habitat between January and March. Inverse data-driven modelling revealed that metabolic pathway regulation and metabolic reaction elasticities distinguish accessions originating from warm and cold growth habitats.

Locally adaptive temperature response of vegetative growth in Arabidopsis thaliana

“…In agreement with the variation in growth rates, metabolite measurements taken at the final day of our experiment showed clear differences between accessions from cold and warm regions, and many of these differences involved metabolites with a known role in cold acclimation (21). Since the transcriptomic component of cold acclimation is well studied, we analyzed the expression profiles of 251 known cold acclimation genes in 8 accessions chosen to be representative in terms of their growth and metabolome profiles (Figure S4).…”

“…Even though this is based on a limited set of 8 accessions, metabolome measurements in all 249 accessions lead to the same conclusion. Metabolites involved in cold acclimation such as raffinose, sucrose and proline were found in higher concentrations in accessions from colder climates (29). We believe that accessions from colder environments are relocating more energy and resources from growth towards preparations for upcoming freezing temperatures, which is a clear example of active plasticity (13, 14).…”

“…Samples for metabolome measurements were taken from the same experiments described in this study and, just like the transcriptome samples, were taken at 25 days after stratification. Results and detailed methodology are described in (29).…”

Evolutionary footprints of a cold relic in a rapidly warming world

“…However, despite covering a broad phylogenetic and taxonomic diversity and clustering taxa according to bioclimatically defined clusters, low temperature response did not differentiate among those, as it has been demonstrated e.g. for Arabidopsis thaliana across a gradient from the Mediterranean towards Scandinavia (Weiszmann et al 2020).…”

“…Herein the metabolome is primarily used as a complex phenotype, which might characterize potentially different bioclimatically defined biomes or species distribution ranges. However, since it has been shown for A. thaliana that the cold metabolome can reflect continental-scale biogeographically defined clines along temperature gradients ( Pritchard et al, 2000 ; Weiszmann et al, 2020 ), it can be assumed that on evolutionary scales past footprints of diversification might be detectable, and that in principle genomic analyses (e.g., GWAS) may allow to identify candidate genes involved in pathway regulation and metabolic reaction plasticity. Our phylogenetic and cytogenetic analysis uncovers a recurrent boosting of speciation by glaciation cycles in this cytotypically very diverse genus and indicates that, despite clear challenges brought by global warming, the genus survives evolutionarily while, we speculate, rescuing its species diversity with reticulate and polyploid evolution.…”