Born to revive: molecular and physiological mechanisms of double tolerance in a paleotropical and resurrection plant

Abstract

Resurrection plants recover physiological functions after complete desiccation. Almost all of them are native to tropical warm environments. However, the Gesneriaceae include four genera, remnant of the past palaeotropical flora, which inhabit temperate mountains. One of these species is additionally freezing-tolerant: Ramonda myconi. We hypothesise that this species has been able to persist in a colder climate thanks to some resurrection-linked traits. To disentangle the physiological mechanisms underpinning multistress tolerance to desiccation and freezing, we conducted an exhaustive seasonal assessment of photosynthesis (gas exchange, limitations to partitioning, photochemistry and galactolipids) and primary metabolism (through metabolomics) in two natural populations at different elevations. R. myconi displayed low rates of photosynthesis, largely due to mesophyll limitation. However, plants were photosynthetically active throughout the year, excluding a reversible desiccation period. Common responses to desiccation and low temperature involved chloroplast protection: enhanced thermal energy dissipation, higher carotenoid to Chl ratio and de-epoxidation of the xanthophyll cycle. As specific responses, antioxidants and secondary metabolic routes rose upon desiccation, while putrescine, proline and a variety of sugars rose in winter. The data suggest conserved mechanisms to cope with photo-oxidation during desiccation and cold events, while additional metabolic mechanisms may have evolved as specific adaptations to cold during recent glaciations.