Protein Changes in Shade and Sun Haberlea rhodopensis Leaves during Dehydration at Optimal and Low Temperatures

Abstract

Haberlea rhodopensis is a unique resurrection plant of high phenotypic plasticity, colonizing both shady habitats and sun-exposed rock clefts. H. rhodopensis also survives freezing winter temperatures in temperate climates. Although survival in conditions of desiccation and survival in conditions of frost share high morphological and physiological similarities, proteomic changes lying behind these mechanisms are hardly studied. Thus, we aimed to reveal ecotype-level and temperature-dependent variations in the protective mechanisms by applying both targeted and untargeted proteomic approaches. Drought-induced desiccation enhanced superoxide dismutase (SOD) activity, but FeSOD and Cu/ZnSOD-III were significantly better triggered in sun plants. Desiccation resulted in the accumulation of enzymes involved in carbohydrate/phenylpropanoid metabolism (enolase, triosephosphate isomerase, UDP-D-apiose/UDP-D-xylose synthase 2, 81E8-like cytochrome P450 monooxygenase) and protective proteins such as vicinal oxygen chelate metalloenzyme superfamily and early light-induced proteins, dehydrins, and small heat shock proteins, the latter two typically being found in the latest phases of dehydration and being more pronounced in sun plants. Although low temperature and drought stress-induced desiccation trigger similar responses, the natural variation of these responses in shade and sun plants calls for attention to the pre-conditioning/priming effects that have high importance both in the desiccation responses and successful stress recovery.

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

“…In fact, similar proteome changes in roots and fronds during dehydration and rehydration are observed. A significant number of proteins that appear during desiccation in leaves correspond to the alterations in carbohydrate metabolism [58]. These alterations contribute to the removal of the starch granules from chloroplasts and the accumulation of carbohydrates in the secondary vacuoles [59].…”

“…Recently, shotgun proteomics showed the enhanced protein abundance of dehydrins, ELIPs, and HSPs in leaves of H. rhodopensis during desiccation [61]. The increased protein content of dehydrins was monitored during drought-and freezing-induced desiccation of Balkan's resurrection species H. rhodopensis, Ramonda serbica, and Ramonda nathaliae [58,62]. Dehydrins have chaperone-like functions in plant cells related to the protection of proteins and membrane stabilization during stress, but they also act as ROS scavengers [63,64].…”

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

“…Van Buren et al [44] proposed that duplication of ELIP genes in the genomes of resurrection plants is related to the evolution of desiccation tolerance and the protection of chloroplasts from photooxidative damage. ELIP transcripts and proteins are highly expressed in the leaves of H. rhodopensis in response to desiccation and during the early hours after rehydration [10,39,41,[45][46][47]. Recently, we found that rehydration after freezinginduced desiccation enhanced the ELIP transcript abundance more strongly in leaves compared with rehydration after drought [41].…”

Resurrection Plants—A Valuable Source of Natural Bioactive Compounds: From Word-of-Mouth to Scientifically Proven Sustainable Use

“…As could be expected, most of them live under desert or semi-desert conditions. However, there are also species that belong in humid tropical regions in Africa and South America or survive winters with freezing temperatures in Europe [3][4][5][6][7][8][9][10][11]. Their strategies to withstand desiccation are predetermined, constitutive (e.g., in-advance high-abundance of protective compounds, including metabolites), and/or inducible, leading to reprogramming at the transcriptome and metabolome levels upon stress establishment [4,[12][13][14][15][16][17].…”