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

ABSTRACT: Haberlea rhodopensis is a resurrection plant with an extremely high desiccation tolerance. Even after long periods of almost full desiccation, its physiological functions are recovered shortly upon re-watering. In order to identify physiological strategies which contribute to its remarkable drought stress tolerance we used near infrared spectroscopy to investigate the state of water in the leaves of this plant and compared it to its relative, non-resurrection plant species Deinostigma eberhardtii. Here we show, using a novel aquaphotomics spectral analysis, that H. rhodopensis performs a dynamic regulation of water molecular structure during dehydration directed at drastic decrease of free water molecules, increase of water molecules with 4 hydrogen bonds, and a massive accumulation of water dimers in the full desiccation stage. Our findings suggest that changes in water structure mirror the changes in major metabolites and antioxidants which together constitute a robust defense system underlying the desiccation tolerance of the resurrection plant, while the water dimer may hold special importance for the "drying without dying" ability.

SUBMITTER: Kuroki S

PROVIDER: S-EPMC6395626 | biostudies-literature | 2019 Feb

REPOSITORIES: biostudies-literature

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

Kuroki Shinichiro S Tsenkova Roumiana R Moyankova Daniela D Muncan Jelena J Morita Hiroyuki H Atanassova Stefka S Djilianov Dimitar D

Scientific reports 20190228 1

Haberlea rhodopensis is a resurrection plant with an extremely high desiccation tolerance. Even after long periods of almost full desiccation, its physiological functions are recovered shortly upon re-watering. In order to identify physiological strategies which contribute to its remarkable drought stress tolerance we used near infrared spectroscopy to investigate the state of water in the leaves of this plant and compared it to its relative, non-resurrection plant species Deinostigma eberhardti ...[more]

PMID: 30816196

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Project description:BackgroundDrought is one of the main consequences of global climate change and this problem is expected to intensify in the future. Resurrection plants evolved the ability to withstand the negative impact of long periods of almost complete desiccation and to recover at rewatering. In this respect, many physiological, transcriptomic, proteomic and genomic investigations have been performed in recent years, however, few epigenetic control studies have been performed on these valuable desiccation-tolerant plants so far.ResultsIn the present study, for the first time for resurrection plants we provide evidences about the differential chromatin accessibility of Haberlea rhodopensis during desiccation stress by ATAC-seq (Assay for Transposase Accessible Chromatin with high-throughput sequencing). Based on gene similarity between species, we used the available genome of the closely related resurrection plant Dorcoceras hygrometricum to identify approximately nine hundred transposase hypersensitive sites (THSs) in H. rhodopensis. The majority of them corresponds to proximal and distal regulatory elements of different genes involved in photosynthesis, carbon metabolism, synthesis of secondary metabolites, cell signalling and transcriptional regulation, cell growth, cell wall, stomata conditioning, chaperons, oxidative stress, autophagy and others. Various types of binding motifs recognized by several families of transcription factors have been enriched from the THSs found in different stages of drought. Further, we used the previously published RNA-seq data from H. rhodopensis to evaluate the expression of transcription factors putatively interacting with the enriched motifs, and the potential correlation between the identified THS and the expression of their corresponding genes.ConclusionsThese results provide a blueprint for investigating the epigenetic regulation of desiccation tolerance in resurrection plant H. rhodopensis and comparative genomics between resurrection and non-resurrection species with available genome information.

Project description:The desiccation tolerance of plants relies on defense mechanisms that enable the protection of macromolecules, biological structures, and metabolism. Although the defense of leaf tissues exposed to solar irradiation is challenging, mechanisms that protect the viability of the roots, yet largely unexplored, are equally important for survival. Although the photosynthetic apparatus in leaves contributes to the generation of oxidative stress under drought stress, we hypothesized that oxidative stress and thus antioxidative defense is also predominant in the roots. Thus, we aimed for a comparative analysis of the protective mechanisms in leaves and roots during the desiccation of Haberlea rhodopensis. Consequently, a high content of non-enzymatic antioxidants and high activity of antioxidant enzymes together with the activation of specific isoenzymes were found in both leaves and roots during the final stages of desiccation of H. rhodopensis. Among others, catalase and glutathione reductase activity showed a similar tendency of changes in roots and leaves, whereas, unlike that in the leaves, superoxide dismutase activity was enhanced under severe but not under medium desiccation in roots. Nitric oxide accumulation in the root tips was found to be sensitive to water restriction but suppressed under severe desiccation. In addition to the antioxidative defense, desiccation induced an enhanced abundance of dehydrins, ELIPs, and sHSP 17.7 in leaves, but this was significantly better in roots. In contrast to leaf cells, starch remained in the cells of the central cylinder of desiccated roots. Taken together, protective compounds and antioxidative defense mechanisms are equally important in protecting the roots to survive desiccation. Since drought-induced damage to the root system fundamentally affects the survival of plants, a better understanding of root desiccation tolerance mechanisms is essential to compensate for the challenges of prolonged dry periods.

Dataset Information

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

Publications

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

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