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OsTGAP1, a bZIP transcription factor, coordinately regulates the inductive production of diterpenoid phytoalexins in rice.

ABSTRACT: Production of major diterpenoid phytoalexins, momilactones and phytocassanes, is induced in rice upon recognition of pathogenic invasion as plant defense-related compounds. We recently showed that biosynthetic genes for momilactones are clustered on rice chromosome 4 and co-expressed after elicitation, mimicking pathogen attack. Because genes for most metabolic pathways in plants are not organized in gene clusters, examination of the mechanism(s) regulating the expression of such clustered genes is needed. Here, we report a chitin oligosaccharide elicitor-inducible basic leucine zipper transcription factor, OsTGAP1, which is essential for momilactone biosynthesis and regulates the expression of the five genes in the cluster. The knock-out mutant for OsTGAP1 had almost no expression of the five clustered genes (OsCPS4, OsKSL4, CYP99A2, CYP99A3, and OsMAS) or production of momilactones upon elicitor treatment. Inductive expression of OsKSL7 for phytocassane biosynthesis was also largely affected in the ostgap1 mutant, although phytocassane accumulation still occurred. Conversely, OsTGAP1-overexpressing lines exhibited enhanced expression of the clustered genes and hyperaccumulation of momilactones in response to the elicitor. Furthermore, enhanced expression of OsKSL7 and hyperaccumulation of phytocassanes was also observed. We also found that OsTGAP1 overexpression can influence transcriptional up-regulation of OsDXS3 in the methylerythritol phosphate pathway, eventually leading to inductive production of diterpenoid phytoalexins. These results indicate that OsTGAP1 functions as a key regulator of the coordinated transcription of genes involved in inductive diterpenoid phytoalexin production in rice and mainly exerts an essential role on expression of the clustered genes for momilactone biosynthesis.

SUBMITTER: Okada A

PROVIDER: S-EPMC2785339 | biostudies-literature | 2009 Sep

REPOSITORIES: biostudies-literature

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OsTGAP1, a bZIP transcription factor, coordinately regulates the inductive production of diterpenoid phytoalexins in rice.

Okada Atsushi A Okada Kazunori K Miyamoto Koji K Koga Jinichiro J Shibuya Naoto N Nojiri Hideaki H Yamane Hisakazu H

The Journal of biological chemistry 20090727 39

Production of major diterpenoid phytoalexins, momilactones and phytocassanes, is induced in rice upon recognition of pathogenic invasion as plant defense-related compounds. We recently showed that biosynthetic genes for momilactones are clustered on rice chromosome 4 and co-expressed after elicitation, mimicking pathogen attack. Because genes for most metabolic pathways in plants are not organized in gene clusters, examination of the mechanism(s) regulating the expression of such clustered genes ...[more]

PMID: 19635799

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Project description:Phytoalexins are specialised antimicrobial metabolites that are produced by plants in response to pathogen attack. Momilactones and phytocassanes are the major diterpenoid phytoalexins in rice and are synthesised from geranylgeranyl diphosphate, which is derived from the methylerythritol phosphate (MEP) pathway. The hyperaccumulation of momilactones and phytocassanes due to the hyperinductive expression of the relevant biosynthetic genes and the MEP pathway gene OsDXS3 in OsTGAP1-overexpressing (OsTGAP1ox) rice cells has previously been shown to be stimulated by the chitin oligosaccharide elicitor. In this study, to clarify the mechanisms of the elicitor-stimulated coordinated hyperinduction of these phytoalexin biosynthetic genes in OsTGAP1ox cells, transcriptome analysis and chromatin immunoprecipitation with next-generation sequencing were performed, resulting in the identification of 122 OsTGAP1 target genes. Transcriptome analysis revealed that nearly all of the momilactone and phytocassane biosynthetic genes, which are clustered on chromosomes 4 and 2, respectively, and the MEP pathway genes were hyperinductively expressed in the elicitor-stimulated OsTGAP1ox cells. Unexpectedly, none of the clustered genes was included among the OsTGAP1 target genes, suggesting that OsTGAP1 did not directly regulate the expression of these biosynthetic genes through binding to each promoter region. Interestingly, however, several OsTGAP1-binding regions were found in the intergenic regions among and near the cluster regions. Concerning the MEP pathway genes, only OsDXS3, which encodes a key enzyme of the MEP pathway, possessed an OsTGAP1-binding region in its upstream region. A subsequent transactivation assay further confirmed the direct regulation of OsDXS3 expression by OsTGAP1, but other MEP pathway genes were not included among the OsTGAP1 target genes. Collectively, these results suggest that OsTGAP1 participates in the enhanced accumulation of diterpenoid phytoalexins, primarily through mechanisms other than the direct transcriptional regulation of the genes involved in the biosynthetic pathway of these phytoalexins.

Project description:BackgroundRice productivity is adversely affected by environmental stresses. Transcription factors (TFs), as the regulators of gene expression, are the key players contributing to stress tolerance and crop yield. Histone gene binding protein-1b (OsHBP1b) is a TF localized within the Saltol QTL in rice. Recently, we have reported the characterization of OsHBP1b in relation to salinity and drought tolerance in a model system tobacco. In the present study, we over-express the full-length gene encoding OsHBP1b in the homologous system (rice) to assess its contribution towards multiple stress tolerance and grain yield.ResultsWe provide evidence to show that transgenic rice plants over-expressing OsHBP1b exhibit better survival and favourable osmotic parameters under salinity stress than the wild type counterparts. These transgenic plants restricted reactive oxygen species accumulation by exhibiting high antioxidant enzyme activity (ascorbate peroxidase and superoxide dismutase), under salinity conditions. Additionally, these transgenic plants maintained the chlorophyll concentration, organellar structure, photosynthesis and expression of photosynthesis and stress-related genes even when subjected to salinity stress. Experiments conducted for other abiotic stresses such as drought and high temperature revealed improved tolerance in these transgenic plants with better root and shoot growth, better photosynthetic parameters, and enhanced antioxidant enzyme activity, in comparison with WT. Further, the roots of transgenic lines showed large cortical cells and accumulated a good amount of callose, unlike the WT roots, thus enabling them to penetrate hard soil and prevent the entry of harmful ions in the cell.ConclusionCollectively, our results show that rice HBP1b gene contributes to multiple abiotic stress tolerance through several molecular and physiological pathways and hence, may serve as an important gene for providing multiple stress tolerance and improving crop yield in rice.

Dataset Information

OsTGAP1, a bZIP transcription factor, coordinately regulates the inductive production of diterpenoid phytoalexins in rice.

Publications

OsTGAP1, a bZIP transcription factor, coordinately regulates the inductive production of diterpenoid phytoalexins in rice.

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