Abstract

BackgroundWater 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.ResultsDe novo assembly yielded a total of 142,479 unigenes with an average sequence length of 1034 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.ConclusionReprograming 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.

Highlights

  • Water shortage is a major factor that harms agriculture and ecosystems worldwide

  • Our de novo analysis supported these results and identified novel genes that extend our understanding of the roles that cyclic electron flow (CEF), carbon turnover, phenylpropanoids, stress hormone signal transduction, protein quality control and DNA repair play in desiccation tolerance

  • We believe that our transcriptomic data contribute to the elucidation of new desiccation tolerance mechanisms in the Balkan endemic plant H. rhodopensis, as we have identified a large number of novel dehydration-responsive genes (Fig. 8)

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Summary

Introduction

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. We have shown that the dynamics of desiccation tolerance can be characterized by numerous changes in various processes at additional important time points during drying: the stages of slight (~ 65–75%) and severe (20–25% RWC) dehydration [8]. Dramatic changes in photosynthetic performance and energy supply, such as ATP and glycolytic intermediates, were observed at this stage of dehydration [9,10,11,12]. This time point appears to be of crucial importance, as non-resurrection plants related to H. rhodopensis tolerated the loss of almost two-thirds of their water content, whereas further drying to 20% RWC was irreversible [11]

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