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Four distinct types of dehydration stress memory genes in Arabidopsis thaliana

ABSTRACT: Arabidopsis plants that have experienced stress from water withdrawal show an improved ability to tolerate subsequent exposures as a ‘memory’ from the previous stress. This physiological stress memory is associated with ‘transcriptional memory’ illustrated by a subset of dehydrations stress responding genes that produce significantly different transcript amounts during repeated dehydration stresses relative to their response in the first. Here we report the genome-wide representation of dehydration stress transcriptional memory genes in A. thaliana. We identify four novel transcription patterns in response to repeated dehydration stress treatments. The nature of the proteins encoded by genes from each type of memory-response pattern is analyzed and the consequences of the genes’ memory behavior are considered in the context of possible biological relevance. The memory behavior of genes co-regulated by the dehydration/ABA and other abiotic stress and hormone responding pathways suggested that the crosstalk at the transcriptional level between them was affected as well. The intensity and the nature of specific biochemical, membrane, chloroplast, and stress response-related interactions during multiple exposures to dehydration stress are different from the responses to a single dehydration stress. The results reveal additional, hitherto unknown, levels of complexity of the plants’ transcriptional behavior when adjusting and adapting to recurring water deficits.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE48235 | GEO | 2014/01/01

SECONDARY ACCESSION(S): PRJNA209324

REPOSITORIES: GEO

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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.

Project description:Pre-exposure of plants to various abiotic conditions confers improved tolerance to subsequent stress. Mild drought acclimation induces acquired rapid desiccation tolerance (RDT) in the resurrection plant Boea hygrometrica, but the mechanisms underlying the priming and memory processes remain unclear. In this study, we demonstrated that drought acclimationinduced RDT can be maintained for at least four weeks but was completely erased after 18 weeks based on a combination of the phenotypic and physiological parameters. Global transcriptome analysis identified several RDT-specific rapid dehydration-responsive genes related to cytokinin and phospholipid biosynthesis, nitrogen and carbon metabolism, and epidermal morphogenesis, most of which were pre-induced by drought acclimation. Comparison of whole-genome DNA methylation revealed dehydration stress-responsive hypomethylation in the CG, CHG, and CHH contexts and acclimation-induced hypermethylation in the CHH context of the B. hygrometrica genome, consistent with the transcriptional changes in methylation pathway genes. As expected, the global promoter and gene body methylation levels were negatively correlated with gene expression levels in both acclimated and dehydrated plants but showed no association with transcriptional divergence during the procedure. Nevertheless, the promoter methylation variations in the CG and CHG contexts were significantly associated with the differential expression of genes required for fundamental genetic processes of DNA conformation, RNA splicing, translation, and post-translational protein modification during acclimation, growth, and rapid dehydration stress response. It was also associated with the dehydration stress-induced upregulation of memory genes, including pre-mRNA-splicing factor 38A, vacuolar amino acid transporter 1-like, and UDP-sugar pyrophosphorylase, which may contribute directly or indirectly to the improvement of dehydration tolerance in B. hygrometrica plants. Altogether, our findings demonstrate the potential implications of DNA methylation in dehydration stress memory and, therefore, provide a molecular basis for enhanced dehydration tolerance in plants induced by drought acclimation.

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Four distinct types of dehydration stress memory genes in Arabidopsis thaliana

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