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A translational regulator MHZ9 modulates ethylene signaling in rice.

ABSTRACT: Ethylene plays essential roles in rice growth, development and stress adaptation. Translational control of ethylene signaling remains unclear in rice. Here, through analysis of an ethylene-response mutant mhz9, we identified a glycine-tyrosine-phenylalanine (GYF) domain protein MHZ9, which positively regulates ethylene signaling at translational level in rice. MHZ9 is localized in RNA processing bodies. The C-terminal domain of MHZ9 interacts with OsEIN2, a central regulator of rice ethylene signaling, and the N-terminal domain directly binds to the OsEBF1/2 mRNAs for translational inhibition, allowing accumulation of transcription factor OsEIL1 to activate the downstream signaling. RNA-IP seq and CLIP-seq analyses reveal that MHZ9 associates with hundreds of RNAs. Ribo-seq analysis indicates that MHZ9 is required for the regulation of ~ 90% of genes translationally affected by ethylene. Our study identifies a translational regulator MHZ9, which mediates translational regulation of genes in response to ethylene, facilitating stress adaptation and trait improvement in rice.

SUBMITTER: Huang YH

PROVIDER: S-EPMC10403538 | biostudies-literature | 2023 Aug

REPOSITORIES: biostudies-literature

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A translational regulator MHZ9 modulates ethylene signaling in rice.

Huang Yi-Hua YH Han Jia-Qi JQ Ma Biao B Cao Wu-Qiang WQ Li Xin-Kai XK Xiong Qing Q Zhao He H Zhao Rui R Zhang Xun X Zhou Yang Y Wei Wei W Tao Jian-Jun JJ Zhang Wan-Ke WK Qian Wenfeng W Chen Shou-Yi SY Yang Chao C Yin Cui-Cui CC Zhang Jin-Song JS

Nature communications 20230804 1

Ethylene plays essential roles in rice growth, development and stress adaptation. Translational control of ethylene signaling remains unclear in rice. Here, through analysis of an ethylene-response mutant mhz9, we identified a glycine-tyrosine-phenylalanine (GYF) domain protein MHZ9, which positively regulates ethylene signaling at translational level in rice. MHZ9 is localized in RNA processing bodies. The C-terminal domain of MHZ9 interacts with OsEIN2, a central regulator of rice ethylene sig ...[more]

PMID: 37542048

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Project description:Low temperature stress represents a significant abiotic stress factor affecting rice yields. While the structure and some of the functions of cell cycle protein-dependent protein kinase inhibitor (CKI) family proteins have been the subject of study, their relevance to cold tolerance in rice has been less investigated. In this study, we cloned OsEL2 (LOC_Os03g01740) and constructed anti-expression lines of this gene. The resulting lines exhibited significant cold sensitivity and displayed greater oxidative damage than wild type Nippobare (Nip). However, the activities of antioxidant enzymes, such as catalase (CAT), were significantly elevated in OsEL2-AX plants in comparison to Nip following exposure to 4 °C stress. RNA sequencing revealed the presence of 18,822 differential genes, with the majority of them being expressed with temporal specificity. The Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment analysis revealed that a considerable number of differentially expressed genes (DEGs) are involved in the metabolism of amino acids, lipids, and terpenoids. Weighted gene co-expression network analysis (WGCNA) revealed a close relationship between the genes in the turquoise and light green modules and rice cold tolerance traits. These genes were predominantly enriched in terpene metabolism and the metabolism of various plant secondary metabolites, suggesting that OsEL2 influences rice cold tolerance through the metabolism of these two classes of substances. An analysis of the genes within these two modules using transcription factor (TF) enrichment and KEGG enrichment revealed that they are predominantly regulated by mitogen-activated protein kinase (MAPK) and ethylene signaling pathways. Furthermore, we found that tryptophan metabolism, phenylalanine metabolism, and monoterpene synthesis were enriched in down-regulated pathway enrichment analysis. In addition, we also found that the MAPK signaling pathway was enriched in the KEGG enrichment analysis of AX2 with Nip. The results demonstrate that anti-expression of OsEL2 is associated with a notable decline in rice tolerance to cold stress.

Project description:The inhibition of hypocotyl elongation by ethylene in dark-grown seedlings was the basis of elegant screens that identified ethylene-insensitive Arabidopsis mutants, which remained tall even when treated with high concentrations of ethylene. This simple approach proved invaluable for identification and molecular characterization of major players in the ethylene signaling and response pathway, including receptors and downstream signaling proteins, as well as transcription factors that mediate the extensive transcriptional remodeling observed in response to elevated ethylene. However, the dark-adapted early developmental stage used in these experiments represents only a small segment of a plant's life cycle. After a seedling's emergence from the soil, light signaling pathways elicit a switch in developmental programming and the hormonal circuitry that controls it. Accordingly, ethylene levels and responses diverge under these different environmental conditions. In this review, we compare and contrast ethylene synthesis, perception, and response in light and dark contexts, including the molecular mechanisms linking light responses to ethylene biology. One powerful method to identify similarities and differences in these important regulatory processes is through comparison of transcriptomic datasets resulting from manipulation of ethylene levels or signaling under varying light conditions. We performed a meta-analysis of multiple transcriptomic datasets to uncover transcriptional responses to ethylene that are both light-dependent and light-independent. We identified a core set of 139 transcripts with robust and consistent responses to elevated ethylene across three root-specific datasets. This "gold standard" group of ethylene-regulated transcripts includes mRNAs encoding numerous proteins that function in ethylene signaling and synthesis, but also reveals a number of previously uncharacterized gene products that may contribute to ethylene response phenotypes. Understanding these light-dependent differences in ethylene signaling and synthesis will provide greater insight into the roles of ethylene in growth and development across the entire plant life cycle.

Project description:The phytohormone ethylene is a key signaling molecule that regulates a variety of developmental processes and stress responses in plants. Transcriptional modulation is a pivotal process controlling ethylene synthesis, which further triggers the expression of stress-related genes and plant adaptation to stresses; however, it is unclear how this process is transcriptionally modulated in rice. In the present research, we report the transcriptional regulation of a novel rice ethylene response factor (ERF) in ethylene synthesis and drought tolerance. Through analysis of transcriptional data, one of the drought-responsive ERF genes, OsDERF1, was identified for its activation in response to drought, ethylene and abscisic acid. Transgenic plants overexpressing OsDERF1 (OE) led to reduced tolerance to drought stress in rice at seedling stage, while knockdown of OsDERF1 (RI) expression conferred enhanced tolerance at seedling and tillering stages. This regulation was supported by negative modulation in osmotic adjustment response. To elucidate the molecular basis of drought tolerance, we identified the target genes of OsDERF1 using the Affymetrix GeneChip, including the activation of cluster stress-related negative regulators such as ERF repressors. Biochemical and molecular approaches showed that OsDERF1 at least directly interacted with the GCC box in the promoters of ERF repressors OsERF3 and OsAP2-39. Further investigations showed that OE seedlings had reduced expression (while RI lines showed enhanced expression) of ethylene synthesis genes, thereby resulting in changes in ethylene production. Moreover, overexpression of OsERF3/OsAP2-39 suppressed ethylene synthesis. In addition, application of ACC recovered the drought-sensitive phenotype in the lines overexpressing OsERF3, showing that ethylene production contributed to drought response in rice. Thus our data reveal that a novel ERF transcriptional cascade modulates drought response through controlling the ethylene synthesis, deepening our understanding of the regulation of ERF proteins in ethylene related drought response.

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A translational regulator MHZ9 modulates ethylene signaling in rice.

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A translational regulator MHZ9 modulates ethylene signaling in rice.

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