Freezing tolerance of photosynthetic apparatus in the homoiochlorophyllous resurrection plant Haberlea rhodopensis

Haberlea rhodopensis is unique among homoiochlorophyllous resurrection plants with its ability to tolerate also low temperatures at temperate climate. This study was carried out to elucidate the response and acclimation ability of photosynthetic apparatus to cold and the capacity to tolerate freezing temperatures. Cold acclimated plants experienced short-term freezing conditions under controlled-environment in climatic chamber and also long-term subzero winter temperatures in an ex-situ natural environment. Our results indicated strong freezing tolerance after cold acclimation. In fact, fresh leaves were exposed to and survived freezing stress under both controlled and ex-situ conditions, thus confirming their appropriate cold acclimation. Freezing temperatures induced desiccation of leaves and the corresponding ultrastructural changes in mesophyll cells under ex situ environmental conditions. However, while the complete rearrangement in the cells commenced at 20 % RWC under drought stress, this process started already at 60 % RWC under freezing conditions. The presence of epidermal channels on both leaf sides was observed and their role for the fast water loss is proposed. It was found that freezing-induced desiccation, reversible downregulation of photosynthesis, readjustments in the abundance/organization of the pigment protein complexes and the main photosynthetic proteins together with increased thermal energy dissipation during chilling and freezing temperatures enable plants to survive harsh winter conditions and their fast recovery with the onset of spring. Low temperature responses are discussed in comparison to desiccation-induced changes to point out both common and specific features.