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A multi-omics angle sheds light on the molecular mechanisms underlying desiccation tolerance in Craterostigma plantagineum

ABSTRACT: The resurrection plant Craterostigma plantagineum possesses an extraordinary capacity to survive long-term desiccation. To enhance our understanding of this phenomenon, complementary transcriptome, soluble proteome and primary metabolome analyses were carried out on plant leaves collected from different physiological stages during a dehydration and rehydration cycle. A total of 7348 contigs, 611 proteins and 46 metabolites were differentially regulated across stages. Dynamic changes in transcript, protein and metabolite levels revealed a unique signature characterizing each stage. An overall low correlation between transcript and protein abundance suggests a prominent role for post-transcriptional modification in metabolic reprogramming to prepare plants to desiccation and recovery upon rehydration. The integrative analysis of three -omics datasets was performed with an emphasis on photosynthesis, photorespiration, energy metabolism and amino acid metabolism. The results revealed a set of fine regulations/changes that modulate primary metabolism to confer plasticity to metabolic pathways, thus optimizing plant performance under stress. For example, maintenance of cyclic electron flow and photorespiration and switch from C3 to Crassulacean acid metabolism (CAM) photosynthesis may contribute to partially sustain photosynthesis and minimize oxidative damage during dehydration. transcripts with a delayed translation, ATP-independent bypasses, alternative respiratory pathway and 4-aminobutyric acid (GABA) shunt may play a role in energy management, altogether conferring bioenergetic advantages to meet energy demands for survival during desiccation. This knowledge provides a high-resolution map of the changes occurring in the primary metabolism during dehydration and rehydration and enriches the current understanding of the molecular mechanisms underpinning plant desiccation tolerance. The datasets here provided will ultimately inspire biotechnological strategies for drought tolerance improvement in crops.

ORGANISM(S): Craterostigma plantagineum

PROVIDER: GSE157098 | GEO | 2021/04/30

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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A multi-omics angle sheds light on the molecular mechanisms underlying desiccation tolerance in Craterostigma plantagineum

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