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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.

Project description:Arabidopsis thaliana plants that have experienced an initial exposure to dehydration stress (“trained plants”) have an increased ability to maintain leaf relative water content (RWC) during subsequent stresses than plants experiencing the stress for the first time and transcription of selected dehydration response genes is altered during successive exposures to dehydration stress. This physiological and transcriptional behavior of trained plants is consistent with a “memory “of an earlier stress. It is unknown whether such memory is present in other Angiosperm lineages and whether it is an evolutionarily conserved response to stress (see E-GEOD-48235). Here, we analyzed the behavior and transcriptomes of maize (Zea mays) plants experiencing multiple dehydration stresses and compare them with responses of the evolutionarily distant A. thaliana. We found structurally related genes in maize that displayed the same memory-type responses as in A. thaliana, providing evidence of the conservation of function and transcriptional memory in the evolution of plants’ dehydration stress response systems. Similar to A. thaliana, trained Z. mays plants retained higher RWC during dehydration stress than untrained plants, due in part to maintaining reduced stomatal conductance, despite full recovery of RWC, after the first stress. Divergent transcriptional memory responses were also expressed, suggesting diversification of function among stress memory genes. Some dehydration stress memory genes were also shared with other stress and hormone responding pathways, indicating complex and dynamic interactions between different plant signaling networks. The results provide new insight into how plants respond to multiple dehydration stresses and provide a platform for studies of the functions of memory genes in adaptive responses to water deficit in monocot and eudicot plants . For each condition (water, S1, and S3) the transcriptome was sequenced for two replicates. The watered condition is considered the control.

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

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