Alterations in the sugar metabolism and in the vacuolar system of mesophyll cells contribute to the desiccation tolerance of Haberlea rhodopensis ecotypes

Abstract

Haberlea rhodopensis belongs to the small group of resurrection plants having the unique ability to survive desiccation to air dry state retaining most of its chlorophyll content and then resume normal function upon rehydration. It prefers the shady valleys and northward facing slopes of limestone ridges in mountain zones with high average humidity. Nevertheless, it can be found rarely on rocks directly exposed to the sunlight, without the coverage of the canopy. In the present study, we follow the alterations in the subcellular organization of mesophyll cells and sugar metabolism upon desiccation of shade and sun H. rhodopensis plants. Composition and content of soluble carbohydrates during desiccation and rehydration were different in plants grown below the trees or on the sunny rocks. Sucrose, however, was dominating in both ecotypes. The amount of starch grains in chloroplasts was inversely related to that of sugars. Concomitantly with these changes, the number of vacuoles was multiplied in the cells. This can be explained by the development of small (secondary) vacuoles peripherally in the cytoplasm, rather than by the fragmentation of the single vacuole, proposed earlier in the literature. Accordingly, the centripetal movement of chloroplasts and other organelles may be a result of the dynamic changes in the vacuolar system. Upon rehydration, the inner vacuoles enlarged and the organelles returned to their normal position.

Water molecular structure underpins extreme desiccation tolerance of the resurrection plant Haberlea rhodopensis

“…rhodopensis increased the number of hydrogen bonded species – notably those with 4 hydrogen bonds, and of water dimers S 1 in especially large quantities. Organizing water in hydrogen bonded conformations is consistent with the shrinkage in size during drying, the accumulation of sugars 51,52 , subdivision of the vacuoles 52 and cell wall folding 4,53 – major changes which result in the decrease of cell volume and logically to the increase of hydrogen bonded water. The accumulation of sucrose and raffinose was already reported in H .…”

Transcriptome reprogramming during severe dehydration contributes to physiological and metabolic changes in the resurrection plant Haberlea rhodopensis

“…Glutathione is involved in plant desiccation tolerance as an antioxidant [11, 37, 38]. DEGs related to glutathione metabolism have been reported previously in H. rhodopensis [5] and another resurrection plant species from the same family Gesneriaceae, Boea hygrometrica [3].…”

Light sensitivity of Haberlea rhodopensis shade adapted phenotype under drought stress

“…As the prominent component of these lipid droplets is the antioxidant tocopherol (Vidi et al 2006;Piller et al 2014), their large increase in number could be connected with the higher ROS production caused by the concomitant desiccation and rehydration under light stress. Although both shade and sun adapted thylakoids contain ample protective luminal substance (DLS) during a dehydration-rehydration cycle (Sárvári et al 2014;Georgieva et al 2015), ML thylakoids run out of this (probably phenolic) substance (visible at high resolution) during desiccation (Georgieva et al 2010). The non-eliminated ROS species may damage not only the thylakoid membrane components (PSII RCs), but also inhibit starch re-synthesis during rehydration (Fig.…”

“…The reason may be either the lack of ATP synthesis caused by inhibition of photosynthetic electron transport, or the impaired starch synthase activity, or inhibited triose transport across the plastid envelope. In such a way there is no sink for the water-replacing sugars filling the numerous small vacuoles in the desiccated state (Georgieva et al 2015). Since water can not be taken up by the cells under rewatering, the desiccation proved to be lethal to ML plants.…”