Acclimation-induced metabolic reprogramming contributes to rapid desiccation tolerance acquisition in Boea hygrometrica

The acquisition of rapid desiccation tolerance for the resurrection plant Boea hygrometrica requires a cycle of drought acclimation. Here, a gas chromatography-mass spectrometry based global untargeted metabolite profiling analysis was conducted on leaves of B. hygrometrica during dehydration and rehydration. Metabolic profiles between non-acclimated and drought acclimated plants were clearly distinguished in principal-component and hierarchical cluster analysis, indicating that drought acclimation response required the process in metabolic reprogramming. Accumulation of numerous metabolites involved in carbon and energy metabolism as well as amino acid and fatty acid biosynthesis was observed to be significantly changed upon drought acclimation and dehydration treatments. Using partial least-squares discriminant analysis, 25 known metabolites and 51 compounds with unknown structures were identified as putative biomarkers contributed to the discrimination between drought acclimated and non-acclimated plants. Remarkably, as revealed by transcriptome data analysis, some up-accumulated metabolites in acclimated plants, such as maltose, glutaric acid, L-tryptophan and alpha-tocopherol, which are in good correlation with the increased desiccation tolerance, and were precisely controlled by the transcript changes in multigene family members of related enzymes. Furthermore, genes positively correlated with the up-accumulated biomarkers in transcription abundances were enriched in multiple biological processes, such as ubiquitin-dependent protein catabolism and abscisic acid-activated signaling pathway. Taken together, our observations indicate that the accumulation of important metabolites correlates with the transcriptional activity of biosynthetic related enzymes and putative regulators involved in ubiquitination and ABA signal transduction during a short period of drought acclimation might contribute to the acquisition of rapid desiccation tolerance in B. hygrometrica.