Protective Strategies of Haberlea rhodopensis for Acquisition of Freezing Tolerance: Interaction between Dehydration and Low Temperature

Abstract

Resurrection plants are able to deal with complete dehydration of their leaves and then recover normal metabolic activity after rehydration. Only a few resurrection species are exposed to freezing temperatures in their natural environments, making them interesting models to study the key metabolic adjustments of freezing tolerances. Here, we investigate the effect of cold and freezing temperatures on physiological and biochemical changes in the leaves of Haberlea rhodopensis under natural and controlled environmental conditions. Our data shows that leaf water content affects its thermodynamical properties during vitrification under low temperatures. The changes in membrane lipid composition, accumulation of sugars, and synthesis of stress-induced proteins were significantly activated during the adaptation of H. rhodopensis to both cold and freezing temperatures. In particular, the freezing tolerance of H. rhodopensis relies on a sucrose/hexoses ratio in favor of hexoses during cold acclimation, while there is a shift in favor of sucrose upon exposure to freezing temperatures, especially evident when leaf desiccation is relevant. This pattern was paralleled by an elevated ratio of unsaturated/saturated fatty acids and significant quantitative and compositional changes in stress-induced proteins, namely dehydrins and early light-induced proteins (ELIPs). Taken together, our data indicate that common responses of H. rhodopensis plants to low temperature and desiccation involve the accumulation of sugars and upregulation of dehydrins/ELIP protein expression. Further studies on the molecular mechanisms underlying freezing tolerance (genes and genetic regulatory mechanisms) may help breeders to improve the resistance of crop plants.

Antioxidative Defense, Suppressed Nitric Oxide Accumulation, and Synthesis of Protective Proteins in Roots and Leaves Contribute to the Desiccation Tolerance of the Resurrection Plant Haberlea rhodopensis

“…ELIPs had significantly lower expression in root tissues under desiccation and they were still highly expressed 48 h post-rehydration, suggesting their protective role during the recovery of photosynthetic apparatus. ELIPs were also detected in leaves in H. rhodopensis during freezing-induced desiccation, as well after the rehydration of dried plants [66,67].…”

Overexpression of soybean GmDHN9 gene enhances drought resistance of transgenic Arabidopsis

“… 22 Depending on the presence, deletion, and number of repetitions of these fragments, different combinations of structural domains can be formed, 23 resulting in different taxa, classifying into six subclasses, namely: YnSKn, FnSKn, YnKn, SKn, Kn, and KnS. 24 …”

Acquisition of Freezing Tolerance of Resurrection Species from Gesneriaceae, a Comparative Study

“…In addition to their desiccation tolerance, two of the European resurrection gesneriads, Haberlea rhodopensis and Ramonda myconi, are also freezing-tolerant species, as they survive subzero temperatures during winter [7,8]. Both plants share the protective strategies used for acquiring desiccation and/or freezing tolerance [9][10][11]. Subzero temperatures are associated with additional complications for plant metabolism-the formation of ice crystals in the apoplast and subsequent disruption of the cell wall and plasma membrane [12].…”

“…The protective strategies used by H. rhodopensis and R. myconi in response to cold acclimation and freezing-induced desiccation include cell ultrastructural changes (chloroplast remodeling, appearance of epidermal channels), downregulation of photosynthesis, enhanced de-epoxidation of the xanthophyll cycle, changes in the abundance of photosynthetic proteins and rearrangement of chlorophyll protein complexes, elevated ratio of unsaturated/saturated fatty acids of membranes, lowered glass transition temperatures, accumulation of different sugars and upregulation of dehydrins and early light-induced protein (ELIP) abundance, upregulation of antioxidant system (phenolics, anthocyanins, enzymatic and nonenzymatic antioxidants, etc. ), and elevated levels of polyamines [7,8,10,13,14]. The accumulation of protective substances during dehydration and/or in response to drought or freezing temperatures ensures the successful recovery of resurrection species after rehydration [5,10,15].…”

“…), and elevated levels of polyamines [7,8,10,13,14]. The accumulation of protective substances during dehydration and/or in response to drought or freezing temperatures ensures the successful recovery of resurrection species after rehydration [5,10,15].…”