Resurrection plants of the genus Ramonda: prospective survival strategies – unlock further capacity of adaptation, or embark on the path of evolution?

Abstract

Paleoendemic species of the monophyletic genus Ramonda (R. myconi, R. serbica and R.~nathaliae) are the remnants of the Tertiary tropical and subtropical flora in Europe. They are the rare resurrection plants of Northern Hemisphere temperate zone. Ramonda serbica and R. nathaliae are chorologically differentiated in the Balkan Peninsula and occupy similar habitats in calcareous, northward slopes in canyons and mountainsides. They remain well-hydrated during spring, late autumn and even in winter. In summer and early autumn when plants are subjected to drought and thermal stress, their desiccation tolerance comes into operation and they fall into anabiosis. Investigations revealed the permanent presence of ubiquitine and its conjugates, high amounts of oxalic acid and proline. Both species are homoiochlorophyllous. It enables them to rapidly resume photosynthesis upon rehydration, but also makes them susceptible to reactive oxygen species formation. Dehydration induces activation of antioxidative enzymes (ascorbate peroxidase, glutathione reductase, polyphenol oxidase), increase in amounts of AsA and GSH, phenolic acids, dehydrins, sucrose, and inorganic ions. Plasma membranes, characterized by high amount of cholesterol, are subjected to decrease in membrane fluidity mostly on account of increased level of lipid saturation. Cytogenetic analysis revealed that R. nathaliae is a diploid (2n = 48) and probably evolutionary older species, while R. serbica is a hexaploid (2n = 144). Two species live together in only two localities forming hybrid individuals (2n = 96). Polyploidization is the major evolutionary mechanism in the genus Ramonda that together with hybridization ability indicates that these relict species which have preserved an ancient survival strategy are not the evolutionary “dead end.”The species of the genus Ramonda are promising sources of data important for understanding the complex strategy of resurrection plants’ survival, appraised through a prism of their evolutionary and adaptive potential for multiple environmental stresses.

First evidence of freezing tolerance in a resurrection plant: insights into molecular mobility and zeaxanthin synthesis in the dark

“…de‐epoxidation of V to A + Z by VDE) took place below the freezing temperature range and above the alpha‐relaxation temperature, in which the cellular content had a considerably high viscosity but with molecular mobility still possible to some extent. These findings could be interpreted in agreement with the hypothesis proposed by Rakić et al (), which suggests that desiccation tolerance mechanisms of R. myconi may have provided the basis of its resistance to frost allowing this (and maybe its close Balkan relatives) to remain as the relict tertiary tropical species that survived the glacial era in the European continent.…”

“…(Picó and Riba ). While most resurrection plants described so far have their native habitats in tropical areas of the southern hemisphere (Porembski and Barthlott ), R. myconi is one of the few resurrection angiosperms in Europe (Rakić et al ). There are five European resurrection plant species, which represent preglacial endemo‐relict examples of the tropical–subtropical family Gesneriaceae.…”

“…There are five European resurrection plant species, which represent preglacial endemo‐relict examples of the tropical–subtropical family Gesneriaceae. R. myconi is the only one growing in the Iberian Peninsula (it is endemic to the Pyrenees) while the other four: Ramonda serbica , Ramonda nathaliae , Haberlea rhodopensis and Jankaea heldreichii grow in the Balkan Peninsula (Rakić et al ). Surprisingly, most of the research conducted with R. myconi has dealt with molecular aspects related to its polyploidy, phylogeny and biogeography, or focused on the development of protocols for its in vitro culturing and transformation (Tóth et al , , Dubreuil et al , Siljak‐Yakovlev et al ).…”

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

“…Three species belonging to this genus can be found currently in Europe, two in the Balkans and one in the Pyrenees ( R. myconi ). The three Ramonda species now inhabit sheltered locations, usually growing at the base of north‐facing limestone cliffs and gorges (Rakić et al , 2014). A very similar ecological niche is occupied in Asia by different resurrection species of the genus Boea within the same family Gesneriaceae (Wang et al , 2018).…”

“…Physiological studies with R. myconi , are scarce (but see Kappen, 1966 and Schwab et al , 1989) because the majority of research effort has been focused towards understanding its population genetics (Picó et al , 2002; Siljak‐Yakovlev et al , 2008), in vitro growth (Tóth et al , 2004, 2006), biomechanics (Kampowski et al , 2018) and certain aspects of its ecology (Picó & Riba, 2002). An exhaustive evaluation of physiological performance has been conducted in its close European relatives R. nathaliae , R. serbica and Haberlea rhodopensis (Rakić et al , 2014) and in Boea species, its Asian relatives (Mitra et al , 2013; Tan et al , 2017). Nevertheless, all these studies were conducted with potted plants in gardens and/or under laboratory conditions.…”