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Transcriptome reprogramming at late stage of desiccation defines the resurrection behavior of Haberlea rhodopensis

ABSTRACT: Water shortage is a major factor that harms agriculture and ecosystems worldwide. Plants display various levels of tolerance to water deficit, but only resurrection plants can survive full desiccation of their vegetative tissues. Haberlea rhodopensis, an endemic plant of the Balkans, is one of the few resurrection plants found in Europe. We performed transcriptomic analyses of this species under slight, severe and full dehydration and recovery to investigate the dynamics of gene expression and associate them with existing physiological and metabolomics data. De novo assembly yielded a total of 142,479 unigenes with an average sequence length of 1,034 nt. Among them, 18,110 unigenes were differentially expressed. Hierarchical clustering of all differentially expressed genes resulted in seven clusters of dynamic expression patterns. The most significant expression changes, involving more than 15,000 genes, started at severe dehydration (~20% relative water content) and were partially maintained at full desiccation (<10% relative water content). More than a hundred pathways were enriched and functionally organized in a GO/pathway network at the severe dehydration stage. Transcriptomic changes in key pathways were analyzed and discussed in relation to metabolic processes, signal transduction, quality control of protein and DNA repair in this plant during dehydration and rehydration. Reprograming of the transcriptome occurs during severe dehydration, resulting in a profound alteration of metabolism toward alternative energy supply, hormone signal transduction, and prevention of DNA/protein damage under very low cellular water content, underlying the observed physiological and metabolic responses and the resurrection behavior of H. rhodopensis.

ORGANISM(S): Haberlea rhodopensis

PROVIDER: GSE109958 | GEO | 2018/11/20

REPOSITORIES: GEO

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Project description:Sporobolus stapfianus is a desiccation tolerant (DT) grass and a member of the Poaceae family alongside prominent crop and forage species. Despite the worldwide distribution of this family, most of its species are vulnerable to water loss within their vegetative tissues. As a DT species, S. stapfianus, could, therefore, serve as a model species for identifying the molecular changes that enabled such a rare occurrence of the DT phenotype in resurrection grasses and the implications of such a unique adaptation for agriculture. A comprehensive gene expression profiling was performed in plants subjected to a dehydration/rehydration cycle using NimbleGen microarrays hybridization method. Our results showed that most transcripts were high in the hydrated state of S. stapfianus leaf tissues and that minor dehydration (> 60% relative water content; RWC) did not induce most transcripts, but did repress photosynthetic activity, which show the importance of curtailing the production of toxic elements to the DT phenotype. It took a loss of 40% RWC for induction of most transcripts. This shows that this species is pre-equipped to deal with mild dehydration, but requires stress-induced activation mechanisms to prepare for desiccation. In agreement with our transcriptomic data, a global metabolic analysis conducted in this species has shown that most metabolites accumulate to their highest levels below 45% RWC, which suggests the importance of those late stages of dehydration in preparing resurrection grasses for desiccation and for early stages of rehydration. In most cases, a 12-h rehydration was sufficient to reinstate pre-stress expression levels, which shows that only partial damage occurred during drying. Unlike during dehydration, our metabolomic data profiled after rehydration showed that there is no clear correlation between gene expression and metabolic abundance, which suggests that most of the compounds that are produced during rehydration are quickly utilized in active metabolism of restoration. The findings of the paper show that S. stapfianus is primed to respond to mild dehydration, although severe dehydration require inducible response, with 40-30% RWC being the peak of gene expression. As for photosynthesis, this species cease its photosynthetic activity even at high water levels (85% RWC) alleviating the need to activate antioxidants activity during mild dehydration.

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Transcriptome reprogramming at late stage of desiccation defines the resurrection behavior of Haberlea rhodopensis

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