Water retention and metabolic changes improve desiccation tolerance in Barbacenia graminifolia (Velloziaceae)

Barbacenia graminifolia is a Velloziaceae species endemic to the campos rupestres in Serra do Cipo, Minas Gerais state (Brazil). This biome is characterised by high irradiance and limited water conditions. Unlike other resurrection plants, B. graminifolia can maintain a high hydric status (>80%) after 28 days of water suppression before desiccation. We investigated the physiological and metabolic mechanisms associated with structural changes that allow B. graminifolia to maintain hydration under a prolonged water deficit and to recover after desiccation. After 30 days of water deficit, desiccated plants exhibited chlorophyll degradation, a 178.4% and 193.7% increase in total carotenoids and MDA, respectively, and twice the CAT and APX activity compared to hydrated plants. The metabolite profile showed increased amino acids, carbohydrates, saturated fatty acids and benzoic acids during dehydration, while trichloroacetic acid cycle acids were higher in hydrated and rehydrated plants. Anatomical and ultrastructural data corroborated the physiological and metabolic changes and revealed the presence of mucilaginous cells with high water retention capacity. Our data indicated that combined strategies of assimilatory metabolism shutdown, accumulation of compatible solutes and antioxidant compounds, increase in hydrophilic molecules, changes in the composition of membrane lipids and remodelling of cell organelles conditioned the efficiency of B. graminifolia in delaying water loss, tolerating further desiccation and quickly recovering after rehydration. These attributes evidence that this species is well adapted to cope with adverse environmental conditions, mainly directing the metabolism to an efficient antioxidant response and improving its capacity to retain water during the dry season.