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Dehydration stress activates Arabidopsis MPK6 to signal DCP1 phosphorylation.

ABSTRACT: Eukaryotic mRNA decapping proteins are essential for normal turnover of mRNA. Yet, the mechanism of bulk mRNA turnover during stress responses and its importance to stress tolerance are poorly understood. Here, we showed that dehydration stress activated MPK6 to phosphorylate serine 237 of Arabidopsis DCP1 and phospho-DCP1 preferentially associated with DCP5 to promote mRNA decapping in vivo. This process was essential for stress adaption as dcp5-1 and DCP1-S237A plants were hypersensitive to stress compared with wild-type (WT) plants. Microarray analysis revealed that dehydration-induced expression of many stress responsive genes was compromised in dcp5-1, whereas a subset of transcripts was over-represented in this mutant. Further analysis revealed that this subset of transcripts was likely the direct targets of stress-triggered mRNA decapping in WT. Our results suggest that mRNA decapping through MPK6-DCP1-DCP5 pathway serves as a rapid response to dehydration stress in Arabidopsis.

SUBMITTER: Xu J

PROVIDER: S-EPMC3343339 | biostudies-literature | 2012 Apr

REPOSITORIES: biostudies-literature

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Dehydration stress activates Arabidopsis MPK6 to signal DCP1 phosphorylation.

Xu Jun J Chua Nam-Hai NH

The EMBO journal 20120309 8

Eukaryotic mRNA decapping proteins are essential for normal turnover of mRNA. Yet, the mechanism of bulk mRNA turnover during stress responses and its importance to stress tolerance are poorly understood. Here, we showed that dehydration stress activated MPK6 to phosphorylate serine 237 of Arabidopsis DCP1 and phospho-DCP1 preferentially associated with DCP5 to promote mRNA decapping in vivo. This process was essential for stress adaption as dcp5-1 and DCP1-S237A plants were hypersensitive to st ...[more]

PMID: 22407295

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Project description:BACKGROUND: Pre-exposing plants to diverse abiotic stresses may alter their physiological and transcriptional responses to a subsequent stress, suggesting a form of "stress memory". Arabidopsis thaliana plants that have experienced multiple exposures to dehydration stress display transcriptional behavior suggesting "memory" from an earlier stress. Genes that respond to a first stress by up-regulating or down-regulating their transcription but in a subsequent stress provide a significantly different response define the 'memory genes' category. Genes responding similarly to each stress form the 'non-memory' category. It is unknown whether such memory responses exists in other Angiosperm lineages and whether memory is an evolutionarily conserved response to repeated dehydration stresses. RESULTS: Here, we determine the transcriptional responses of maize (Zea mays L.) plants that have experienced repeated exposures to dehydration stress in comparison with plants encountering the stress for the first time. Four distinct transcription memory response patterns similar to those displayed by A. thaliana were revealed. The most important contribution is the evidence that monocot and eudicot plants, two lineages that have diverged 140 to 200 M years ago, display similar abilities to 'remember' a dehydration stress and to modify their transcriptional responses, accordingly. The highly sensitive RNA-Seq analyses allowed to identify genes that function similarly in the two lineages, as well as genes that function in species-specific ways. Memory transcription patterns indicate that the transcriptional behavior of responding genes under repeated stresses is different from the behavior during an initial dehydration stress, suggesting that stress memory is a complex phenotype resulting from coordinated responses of multiple signaling pathways. CONCLUSIONS: Structurally related genes displaying the same memory responses in the two species would suggest conservation of the genes' memory during the evolution of plants' dehydration stress response systems. On the other hand, divergent transcription memory responses by genes encoding similar functions would suggest occurrence of species-specific memory responses. The results provide novel insights into our current knowledge of how plants respond to multiple dehydration stresses, as compared to a single exposure, and may serve as a reference platform to study the functions of memory genes in adaptive responses to water deficit in monocot and eudicot plants.

Project description:BackgroundHow plants respond to dehydration stress has been extensively researched. However, how plants respond to multiple consecutive stresses is virtually unknown. Pre-exposure to various abiotic stresses (including dehydration) may alter plants' subsequent responses by improving resistance to future exposures. These observations have led to the concept of 'stress memory' implying that during subsequent exposures plants provide responses that are different from those during their first encounter with the stress. Genes that provide altered responses in a subsequent stress define the 'memory genes' category; genes responding similarly to each stress form the 'non-memory' category.ResultsUsing a genome-wide RNA-Seq approach we determine the transcriptional responses of Arabidopsis plants that have experienced multiple exposures to dehydration stress and compare them with the transcriptional behavior of plants encountering the stress for the first time. The major contribution of this study is the revealed existence of four distinct, previously unknown, transcription memory response patterns of dehydration stress genes in A.thaliana. The biological relevance for each of the four memory types is considered in the context of four overlapping strategies employed by a plant to improve its stress tolerance and/or survival: 1) increased synthesis of protective, damage-repairing, and detoxifying functions; 2) coordinating photosynthesis and growth under repetitive stress; 3) re-adjusting osmotic and ionic equilibrium to maintain homeostasis; and 4) re-adjusting interactions between dehydration and other stress/hormone regulated pathways.ConclusionsThe results reveal the unknown, hitherto, existence of four distinct transcription memory response types in a plant and provide genome-wide characterization of memory and non-memory dehydration stress response genes in A.thaliana. The transcriptional responses during repeated exposures to stress are different from known responses occurring during a single exposure. GO analyses of encoded proteins suggested implications for the cellular/organismal protective, adaptive, and survival functions encoded by the memory genes. The results add a new dimension to our understanding of plants' responses to dehydration stress and to current models for interactions between different signaling systems when adjusting to repeated spells of water deficits.

Dataset Information

Dehydration stress activates Arabidopsis MPK6 to signal DCP1 phosphorylation.

Publications

Dehydration stress activates Arabidopsis MPK6 to signal DCP1 phosphorylation.

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