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

Ramonda serbica Panc. is a resurrection plant species that can survive desiccation for a longperiod and fully resume metabolic functions upon rewatering in a very short period, even within48 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 thecell wall polymers and a detailed analysis of the photosynthetic electron transport (PET) chainwere performed. In total, 1192 different protein groups were quantified by TMT-based comparative quantitative proteomics. Among them, 408 protein groups showed a statistically significantdifference in abundance between hydrated (HL) and desiccated leaves (DL). Upon desiccation, themajority of proteins related to photosynthetic processes were less abundant, while chlorophyllfluorescence measurements implied shifting from linear photosynthetic transport (PET) to cyclicelectron transport (CET). The amounts of H2O2 scavenging enzymes, including ascorbate-glutathione cycle components, catalases, peroxiredoxins, Fe-, and Mn- superoxide dismutase (SOD) werereduced 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 wallpolymer 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