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      Temporal profiling of primary metabolites under chilling stress and its association with seedling chilling tolerance of rice (Oryza sativa L.)

      Rice
      Springer
      primary metabolites, seedling chilling tolerance, transcriptomic responses, rice

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          Abstract

          Background Chilling stress is a major factor limiting rice production. Rice genotypes differ greatly in their seedling chilling tolerance (CT), which is known to involve differential expression of large numbers of genes and proteins. To further understand the metabolomic responses of rice to chilling stress, profiles of the 106 primary metabolites of a CT japonica variety, Lijiangxintuanhegu (LTH) and a chilling sensitive indica line, IR29, were investigated under a time-series of chilling stress and non-stress control conditions at the seedling stage. Results We identified 106 primary metabolites that were temporally and genotype-dependently regulated in LTH and IR29 under the time-series chilling stress and subsequent recovery. Three major groups of primary metabolites, amino acids (AAs), organic acids (OAs) and sugars, showed distinct change patterns in both genotypes in response to the chilling stress: a more general accumulation of most AAs, more dramatic decreased levels of most OAs, and greatly reduced levels for most sugars at early time points of stress but increased levels of specific sugars at the later time points of stress. Compared to IR29, LTH had more metabolites showing chilling induced changes, greater levels of these metabolomic changes and a greater ability to recover after stress, implying that LTH used a positive energy-saving strategy against chilling stress. During subsequent recovery, more metabolites were significantly and exclusively up-regulated in LTH, indicating their positive role in chilling tolerance. A comparative analysis of these metabolites data and differentially expressed genes data allowed identification of 7 AAs and related genes that were both chilling responsive and contributed greatly to the CT of LTH. Conclusions The metabolomic responses of rice to chilling stress at the seedling stage were dynamic and involved large numbers of the metabolites. The chilling induced changes of three major groups of metabolites, AAs, OAs and sugars, in rice were well coordinated. The high level seedling CT of LTH was apparently attributed to its increased levels of most AAs and reduced energy consumption that resulted in increased glycolysis and strong resilience on recovery. The results of this study extend our understanding of molecular mechanisms of chilling stress tolerance in rice. Electronic supplementary material The online version of this article (doi:10.1186/1939-8433-6-23) contains supplementary material, which is available to authorized users.

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          Most cited references68

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          DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression.

          DRE/CRT is a cis-acting element that is involved in gene expression responsive to drought and low-temperature stress in higher plants. DREB1A/CBF3 and DREB2A are transcription factors that specifically bind to DRE/CRT in Arabidopsis. We precisely analyzed the DNA-binding specificity of DREBs. Both DREBs specifically bound to six nucleotides (A/GCCGAC) of DRE. However, these proteins had different binding specificities to the second or third nucleotides of DRE. Gel mobility shift assay using mutant DREB proteins showed that the two amino acids, valine and glutamic acid conserved in the ERF/AP2 domains, especially valine, have important roles in DNA-binding specificity. In the Arabidopsis genome, 145 DREB/ERF-related proteins are encoded. These proteins were classified into five groups-AP-2 subfamily, RAV subfamily, DREB subfamily, ERF subfamily, and others. The DREB subfamily included three novel DREB1A- and six DREB2A-related proteins. We analyzed expression of novel genes for these proteins and discuss their roles in stress-responsive gene expression.
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            Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress.

            To identify genes of potential importance to cold, salt, and drought tolerance, global expression profiling was performed on Arabidopsis plants subjected to stress treatments of 4 degrees C, 100 mM NaCl, or 200 mM mannitol, respectively. RNA samples were collected separately from leaves and roots after 3- and 27-h stress treatments. Profiling was conducted with a GeneChip microarray with probe sets for approximately 8,100 genes. Combined results from all three stresses identified 2,409 genes with a greater than 2-fold change over control. This suggests that about 30% of the transcriptome is sensitive to regulation by common stress conditions. The majority of changes were stimulus specific. At the 3-h time point, less than 5% (118 genes) of the changes were observed as shared by all three stress responses. By 27 h, the number of shared responses was reduced more than 10-fold (< 0.5%), consistent with a progression toward more stimulus-specific responses. Roots and leaves displayed very different changes. For example, less than 14% of the cold-specific changes were shared between root and leaves at both 3 and 27 h. The gene with the largest induction under all three stress treatments was At5g52310 (LTI/COR78), with induction levels in roots greater than 250-fold for cold, 40-fold for mannitol, and 57-fold for NaCl. A stress response was observed for 306 (68%) of the known circadian controlled genes, supporting the hypothesis that an important function of the circadian clock is to "anticipate" predictable stresses such as cold nights. Although these results identify hundreds of potentially important transcriptome changes, the biochemical functions of many stress-regulated genes remain unknown.
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              Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway.

              Many plants, including Arabidopsis, increase in freezing tolerance in response to low, nonfreezing temperatures, a phenomenon known as cold acclimation. Previous studies established that cold acclimation involves rapid expression of the CBF transcriptional activators (also known as DREB1 proteins) in response to low temperature followed by induction of the CBF regulon (CBF-targeted genes), which contributes to an increase in freezing tolerance. Here, we present the results of transcriptome-profiling experiments indicating the existence of multiple low-temperature regulatory pathways in addition to the CBF cold response pathway. The transcript levels of approximately 8000 genes were determined at multiple times after plants were transferred from warm to cold temperature and in warm-grown plants that constitutively expressed CBF1, CBF2, or CBF3. A total of 306 genes were identified as being cold responsive, with transcripts for 218 genes increasing and those for 88 genes decreasing threefold or more at one or more time points during the 7-day experiment. These results indicate that extensive downregulation of gene expression occurs during cold acclimation. Of the cold-responsive genes, 48 encode known or putative transcription factors. Two of these, RAP2.1 and RAP2.6, were activated by CBF expression and thus presumably control subregulons of the CBF regulon. Transcriptome comparisons indicated that only 12% of the cold-responsive genes are certain members of the CBF regulon. Moreover, at least 28% of the cold-responsive genes were not regulated by the CBF transcription factors, including 15 encoding known or putative transcription factors, indicating that these cold-responsive genes are members of different low-temperature regulons. Significantly, CBF expression at warm temperatures repressed the expression of eight genes that also were downregulated by low temperature, indicating that in addition to gene induction, gene repression is likely to play an integral role in cold acclimation.
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                Author and article information

                Journal
                24280004
                4883686
                10.1186/1939-8433-6-23
                http://creativecommons.org/licenses/by/2.0

                Agriculture
                primary metabolites,seedling chilling tolerance,transcriptomic responses,rice
                Agriculture
                primary metabolites, seedling chilling tolerance, transcriptomic responses, rice

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