Mechanisms of desiccation tolerance in Ramonda serbica Panc.: transcriptomic, proteomic, metabolomic, and photosynthetic aspects

Abstract

Ramonda serbica Panc. is a resurrection plant species that can survive desiccation for a long period and fully resume metabolic functions upon rewatering in a very short period, even within 48 h. The goal of this study was to identify key candidates and pathways involved in desiccation tolerance in R. serbica. To achieve this, systems biology approach combining transcriptomics, proteomics, and analysis of specific metabolites was employed. In addition, FTIR analysis of the cell wall polymers and a detailed analysis of the photosynthetic electron transport (PET) chain were performed. In total, 1192 different protein groups were quantified by TMT-based comparative quantitative proteomics. Among them, 408 protein groups showed a statistically significant difference in abundance between hydrated (HL) and desiccated leaves (DL). Upon desiccation, the majority of proteins related to photosynthetic processes were less abundant, while chlorophyll fluorescence measurements implied shifting from linear photosynthetic transport (PET) to cyclic electron transport (CET). The amounts of H2O2 scavenging enzymes, including ascorbate-glutathione cycle components, catalases, peroxiredoxins, Fe-, and Mn- superoxide dismutase (SOD) were reduced in DL. However, four Cu/ZnSOD isoforms, three polyphenol oxidases, six germin-like proteins (GLPs), and 22 late embryogenesis abundant proteins (LEAPs; mainly LEA4 and dehydrins), were desiccation-inducible. Desiccation-induced cell wall remodelling by changes in cell wall polymer composition might be linked with pectin demethylesterification and GLP-derived H2O2/ HO•. Our study demonstrated that desiccation tolerance in R. serbica is a complex, species-specific process orchestrated by several metabolic pathways and regulatory networks acting at the transcript, protein, metabolite and physiological levels.