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Phytochrome controls alternative splicing to mediate light responses in Arabidopsis.

ABSTRACT: Plants monitor the ambient light conditions using several informational photoreceptors, including red/far-red light absorbing phytochrome. Phytochrome is widely believed to regulate the transcription of light-responsive genes by modulating the activity of several transcription factors. Here we provide evidence that phytochrome significantly changes alternative splicing (AS) profiles at the genomic level in Arabidopsis, to approximately the same degree as it affects steady-state transcript levels. mRNA sequencing analysis revealed that 1,505 and 1,678 genes underwent changes in their AS and steady-state transcript level profiles, respectively, within 1 h of red light exposure in a phytochrome-dependent manner. Furthermore, we show that splicing factor genes were the main early targets of AS control by phytochrome, whereas transcription factor genes were the primary direct targets of phytochrome-mediated transcriptional regulation. We experimentally validated phytochrome-induced changes in the AS of genes that are involved in RNA splicing, phytochrome signaling, the circadian clock, and photosynthesis. Moreover, we show that phytochrome-induced AS changes of SPA1-RELATED 3, the negative regulator of light signaling, physiologically contributed to promoting photomorphogenesis. Finally, photophysiological experiments demonstrated that phytochrome transduces the signal from its photosensory domain to induce light-dependent AS alterations in the nucleus. Taking these data together, we show that phytochrome directly induces AS cascades in parallel with transcriptional cascades to mediate light responses in Arabidopsis.

SUBMITTER: Shikata H

PROVIDER: S-EPMC4284612 | biostudies-literature | 2014 Dec

REPOSITORIES: biostudies-literature

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Phytochrome controls alternative splicing to mediate light responses in Arabidopsis.

Shikata Hiromasa H Hanada Kousuke K Ushijima Tomokazu T Nakashima Moeko M Suzuki Yutaka Y Matsushita Tomonao T

Proceedings of the National Academy of Sciences of the United States of America 20141215 52

Plants monitor the ambient light conditions using several informational photoreceptors, including red/far-red light absorbing phytochrome. Phytochrome is widely believed to regulate the transcription of light-responsive genes by modulating the activity of several transcription factors. Here we provide evidence that phytochrome significantly changes alternative splicing (AS) profiles at the genomic level in Arabidopsis, to approximately the same degree as it affects steady-state transcript levels ...[more]

PMID: 25512548

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Project description:Jasmonate is an essential phytohormone regulating plant growth, development, and defense. Alternative splicing (AS) in jasmonate ZIM-domain (JAZ) repressors is well-characterized and plays an important role in jasmonate signaling regulation. However, it is unknown whether other genes in the jasmonate signaling pathway are regulated by AS. We explore the potential for AS regulation in three Arabidopsis genotypes (WT, jaz2, jaz7) in response to methyl jasmonate (MeJA) treatment with respect to: (a) differential AS, (b) differential miRNA targeted AS, and (c) AS isoforms with novel functions. AS events identified from transcriptomic data were validated with proteomic data. Protein interaction networks identified two genes, SKIP and ALY4 whose products have both DNA- and RNA-binding affinities, as potential key regulators mediating jasmonate signaling and AS regulation. We observed cases where AS alone, or AS and transcriptional regulation together, can influence gene expression in response to MeJA. Twenty-one genes contain predicted miRNA target sites subjected to AS, which implies that AS is coupled to miRNA regulation. We identified 30 cases where alternatively spliced isoforms may have novel functions. For example, AS of bHLH160 generates an isoform without a basic domain, which may convert it from an activator to a repressor. Our study identified potential key regulators in AS regulation of jasmonate signaling pathway. These findings highlight the importance of AS regulation in the jasmonate signaling pathway, both alone and in collaboration with other regulators. Significance statement:By exploring alternative splicing, we demonstrate its regulation in the jasmonate signaling pathway alone or in collaboration with other posttranscriptional regulations such as nonsense and microRNA-mediated decay. A signal transduction network model for alternative splicing in jasmonate signaling pathway was generated, contributing to our understanding for this important, prevalent, but relatively unexplored regulatory mechanism in plants.

Dataset Information

Phytochrome controls alternative splicing to mediate light responses in Arabidopsis.

Publications

Phytochrome controls alternative splicing to mediate light responses in Arabidopsis.

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