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Transcriptional regulatory network triggered by oxidative signals configures the early response mechanisms of japonica rice to chilling stress.

ABSTRACT: BACKGROUND: The transcriptional regulatory network involved in low temperature response leading to acclimation has been established in Arabidopsis. In japonica rice, which can only withstand transient exposure to milder cold stress (10 degrees C), an oxidative-mediated network has been proposed to play a key role in configuring early responses and short-term defenses. The components, hierarchical organization and physiological consequences of this network were further dissected by a systems-level approach. RESULTS: Regulatory clusters responding directly to oxidative signals were prominent during the initial 6 to 12 hours at 10 degrees C. Early events mirrored a typical oxidative response based on striking similarities of the transcriptome to disease, elicitor and wounding induced processes. Targets of oxidative-mediated mechanisms are likely regulated by several classes of bZIP factors acting on as1/ocs/TGA-like element enriched clusters, ERF factors acting on GCC-box/JAre-like element enriched clusters and R2R3-MYB factors acting on MYB2-like element enriched clusters.Temporal induction of several H2O2-induced bZIP, ERF and MYB genes coincided with the transient H2O2 spikes within the initial 6 to 12 hours. Oxidative-independent responses involve DREB/CBF, RAP2 and RAV1 factors acting on DRE/CRT/rav1-like enriched clusters and bZIP factors acting on ABRE-like enriched clusters. Oxidative-mediated clusters were activated earlier than ABA-mediated clusters. CONCLUSION: Genome-wide, physiological and whole-plant level analyses established a holistic view of chilling stress response mechanism of japonica rice. Early response regulatory network triggered by oxidative signals is critical for prolonged survival under sub-optimal temperature. Integration of stress and developmental responses leads to modulated growth and vigor maintenance contributing to a delay of plastic injuries.

SUBMITTER: Yun KY

PROVIDER: S-EPMC2826336 | biostudies-literature | 2010

REPOSITORIES: biostudies-literature

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Transcriptional regulatory network triggered by oxidative signals configures the early response mechanisms of japonica rice to chilling stress.

Yun Kil-Young KY Park Myoung Ryoul MR Mohanty Bijayalaxmi B Herath Venura V Xu Fuyu F Mauleon Ramil R Wijaya Edward E Bajic Vladimir B VB Bruskiewich Richard R de Los Reyes Benildo G BG

BMC plant biology 20100125

<h4>Background</h4>The transcriptional regulatory network involved in low temperature response leading to acclimation has been established in Arabidopsis. In japonica rice, which can only withstand transient exposure to milder cold stress (10 degrees C), an oxidative-mediated network has been proposed to play a key role in configuring early responses and short-term defenses. The components, hierarchical organization and physiological consequences of this network were further dissected by a syste ...[more]

PMID: 20100339

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Project description:The central role of transcriptional regulation in integrating various low temperature response mechanisms has been established in Arabidopsis, where the CBF/DREB regulon plays a prominent role during acclimation. Rice is sensitive to chilling but many japonica cultivars can survive continuous exposure to as low as 10oC for up to 7 days during the most critical stage of seedling establishment better than most indica cultivars. The transcriptional regulatory networks that define this variation have not been studied in detail as cold acclimation has been scrutinized in Arabidopsis. Towards the comparison of the compositional complexity of low temperature response regulons of rice and Arabidopsis, we used the cultivar Nipponbare for genome-wide survey of regulatory clusters by integrative analysis of promoter architectures and temporal expression profiles during exposure to 10oC at narrow time intervals. Temporal profiles revealed major clusters of genes that were induced within the initial 24 hours. These clusters were further defined by common features of having either CRT/DRE-like elements, as1/ocs-like elements or both in their promoters. Genes containing as1/ocs-like elements with or without CRT/DRE, but not those containing only CRT/DRE-like elements were induced by exogenous H2O2 but not by ABA at ambient temperature, suggesting that they belong to a potential regulon (ROS-bZIP – as1/ocs module) that responds to elevated levels of reactive oxygen species (ROS) during the initial stages of stress. Parallel analysis of transcription factors during the initial 12 hours revealed candidate regulator(s) of this putative early response regulon. Cultivar-specific expression signatures of selected members of this regulatory cluster were also positively correlated with genotypic variation in chilling tolerance. We hypothesized that the ROS-bZIP – as1/ocs cluster has important roles in configuring the transcriptome of rice seedlings during the early stages of chilling stress and it appears to be independent of ABA and functions in parallel to the CBF/DREB regulon. Keywords: time course (response to low temperature) This experiment describes the analysis of the temporal changes in gene expression in response to chilling temperature in Nipponbare rice. A total of 10 stress time points, i.e., 0.5, 2, 4, 6, 12, 18, 24, 36, 48, and 96 hrs after exposure to 10C in a growth chamber and one recovery time point, i.e., 96 hrs at 10C and then 24 hrs (24R) at ambient or control temperature (29C), were profiled with reference to a corresponding control, which was exposed to ambient temperature (29C) for the same length of time under cold stress (each stress time point has a corresponding control sample). Control and cold stress samples were labeled with Cy5 and Cy3, respectively. No dye swap replicate was performed in this experiment. The microarray platform used in this study was the 45K oligonucleotide microarray (www.ricearray.org) which comes in pairs of slides A and B (each containing about 50% of the total number of features). The data described in this series include all hybridizations with slide A and with slide B. All experiments were performed with two independent biological replicates (R1 and R2) for each time point.

Project description:BackgroundPlants respond to low temperature through an intricately coordinated transcriptional network. The CBF/DREB-regulated network of genes has been shown to play a prominent role in freeze-tolerance of Arabidopsis through the process of cold acclimation (CA). Recent evidence also showed that the CBF/DREB regulon is not unique to CA but evolutionarily conserved between chilling-insensitive (temperate) and chilling-sensitive (warm-season) plants. In this study, the wide contrast in chilling sensitivity between indica and japonica rice was used as model to identify other regulatory clusters by integrative analysis of promoter architecture (ab initio) and gene expression profiles.ResultsTranscriptome analysis in chilling tolerant japonica rice identified a subset of 121 'early response' genes that were upregulated during the initial 24 hours at 10 degrees C. Among this group were four transcription factors including ROS-bZIP1 and another larger sub-group with a common feature of having as1/ocs-like elements in their promoters. Cold-induction of ROS-bZIP1 preceded the induction of as1/ocs-like element-containing genes and they were also induced by exogenous H2O2 at ambient temperature. Coordinated expression patterns and similar promoter architectures among the 'early response' genes suggest that they belong to a potential regulon (ROS-bZIP-as1/ocs regulatory module) that responds to elevated levels of ROS during chilling stress. Cultivar-specific expression signatures of the candidate genes indicate a positive correlation between the activity of the putative regulon and genotypic variation in chilling tolerance.ConclusionA hypothetical model of an ROS-mediated regulon (ROS-bZIP-as1/ocs) triggered by chilling stress was assembled in rice. Based on the current results, it appears that this regulon is independent of ABA and CBF/DREB, and that its activation has an important contribution in configuring the rapid responses of rice seedlings to chilling stress.

Project description:Regulation of gene expression by reactive oxygen species (ROS) is an important component of abiotic stress signal transduction mechanisms. Previous genome-wide analysis of chilling-induced changes in gene expression suggested a potential role of H2O2 and other ROS as key signals in the induction of early response genes in japonica rice (cv. Nipponbare). Candidate regulators including bZIP-, Myb- or WRKY-types of transcription factors that were responsive to both chilling (10oC) and exogenous H2O2, and their probable target clusters (as1/ocs/TGA1-like, MybR-like element containing genes) were inferred by integrative analysis of qPCR expression profiles and ab initio promoter motif data. In an effort to define the composition and hierarchical organization of the ROS-mediated chilling response regulatory networks, we examined the effect of exogenous H2O2 (6 hours in 4mM H2O2 at 28oC and then 6 hours of recovery in water at 28oC) on the transcriptome of Nipponbare in a genome-wide scale and compared them with the chilling stress transcriptome. Results of this study were consistent with our earlier model that a ROSbZIP-as1/ocs/TGA1 regulatory module is a direct consequence of chilling-induced elevation of intracellular ROS during the initial 24 hours. Keywords: time course (response to exogenous H2O2) This experiment describes the analysis of the temporal changes in gene expression in response to exogenous H2O2 in Nipponbare rice. A total of 5 treatment regimes were examined (1, 3, and 6 hours at 4 mM H2O2 and then 3 and 6 hours of recovery in water after 6 hours of exposure to H2O2). The microarray platform used in this study was the 45K oligonucleotide microarray (www.ricearray.org) which comes in pairs of slides A and B (each containing about 50% of the total number of features). The data described in this series include all hybridizations with slide A and with slide B. All experiments were performed with two independent biological replicates (R1 and R2) for each time point.

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Transcriptional regulatory network triggered by oxidative signals configures the early response mechanisms of japonica rice to chilling stress.

Publications

Transcriptional regulatory network triggered by oxidative signals configures the early response mechanisms of japonica rice to chilling stress.

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