Abstract
Haberlea rhodopensis is a resurrection species with extreme resistance to drought stress and desiccation but also with ability to withstand low temperatures and freezing stress. In order to identify biochemical strategies which contribute to Haberlea's remarkable stress tolerance, the metabolic reconfiguration of H. rhodopensis during low temperature (4°C) and subsequent return to optimal temperatures (21°C) was investigated and compared with that of the stress tolerant Thellungiella halophyla and the stress sensitive Arabidopsis thaliana. Metabolic analysis by GC-MS revealed intrinsic differences in the metabolite levels of the three species even at 21°C. H. rhodopensis had significantly more raffinose, melibiose, trehalose, rhamnose, myo-inositol, sorbitol, galactinol, erythronate, threonate, 2-oxoglutarate, citrate, and glycerol than the other two species. A. thaliana had the highest levels of putrescine and fumarate, while T. halophila had much higher levels of several amino acids, including alanine, asparagine, beta-alanine, histidine, isoleucine, phenylalanine, serine, threonine, and valine. In addition, the three species responded differently to the low temperature treatment and the subsequent recovery, especially with regard to the sugar metabolism. Chilling induced accumulation of maltose in H. rhodopensis and raffinose in A. thaliana but the raffinose levels in low temperature exposed Arabidopsis were still much lower than these in unstressed Haberlea. While all species accumulated sucrose during chilling, that accumulation was transient in H. rhodopensis and A. thaliana but sustained in T. halophila after the return to optimal temperature. Thus, Haberlea's metabolome appeared primed for chilling stress but the low temperature acclimation induced additional stress-protective mechanisms. A diverse array of sugars, organic acids, and polyols constitute Haberlea's main metabolic defence mechanisms against chilling, while accumulation of amino acids and amino acid derivatives contribute to the low temperature acclimation in Arabidopsis and Thellungiella. Collectively, these results show inherent differences in the metabolomes under the ambient temperature and the strategies to respond to low temperature in the three species.
Highlights
The small but diverse group of resurrection plants exhibit a remarkable adaptation to extreme drought stress
CHARACTERIZATION OF THE PHYSIOLOGICAL RESPONSES OF H. rhodopensis, T. halophyla, AND A. thaliana TO CHILLING TREATMENT AND SUBSEQUENT RECOVERY To evaluate the influence of low temperatures on the three species, plants were inspected for any visible damage and a number of physiological parameters were measured: malondialdehyde levels, which are indicators of lipid peroxidation and oxidative stress; chlorophyll pigments, which normally decrease during severe stress; reduced and oxidized glutathione, which increase as a result of various stresses and their ratio indicates the redox status of the cell
Despite the numerous studies on resurrection species in the past decade, there is no detailed information on the response of resurrection species to other types of abiotic stresses except drought
Summary
The small but diverse group of resurrection plants exhibit a remarkable adaptation to extreme drought stress. Haberlea rhodopensis is a desiccation-tolerant species, perennial herbaceous plant endemic to several mountains in the Balkan Peninsula in South-Eastern Europe (Gechev et al, 2013a). Earlier studies on resurrection plants indicated that complex and diverse mechanisms can contribute to their desiccation tolerance These include alterations of sugar metabolism, reconfiguration of the cell wall, inhibition of growth and photosynthesis, rapid induction of late embryogenesis abundant (LEA) and small heat shock proteins, accumulation of phenolic antioxidants, upregulation of antioxidant enzymes, aldehyde dehydrogenases, and other protective enzymes
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