Phytochrome activates the plastid-encoded RNA polymerase for chloroplast biogenesis via nucleus-to-plastid signaling
Light initiates chloroplast biogenesis by activating photosynthesis-associated genes encoded by not only the nuclear but also the plastidial genome, but how photoreceptors control plastidial gene expression remains enigmatic. Here we show that the photoactivation of phytochromes triggers the express...
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Published in | Nature communications Vol. 10; no. 1; pp. 2629 - 16 |
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Format | Journal Article |
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14.06.2019
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Abstract | Light initiates chloroplast biogenesis by activating photosynthesis-associated genes encoded by not only the nuclear but also the plastidial genome, but how photoreceptors control plastidial gene expression remains enigmatic. Here we show that the photoactivation of phytochromes triggers the expression of photosynthesis-associated plastid-encoded genes (PhAPGs) by stimulating the assembly of the bacterial-type plastidial RNA polymerase (PEP) into a 1000-kDa complex. Using forward genetic approaches, we identified REGULATOR OF CHLOROPLAST BIOGENESIS (RCB) as a dual-targeted nuclear/plastidial phytochrome signaling component required for PEP assembly. Surprisingly, RCB controls PhAPG expression primarily from the nucleus by interacting with phytochromes and promoting their localization to photobodies for the degradation of the transcriptional regulators PIF1 and PIF3. RCB-dependent PIF degradation in the nucleus signals the plastids for PEP assembly and PhAPG expression. Thus, our findings reveal the framework of a nucleus-to-plastid anterograde signaling pathway by which phytochrome signaling in the nucleus controls plastidial transcription. |
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AbstractList | Light initiates chloroplast biogenesis by controlling gene expression in plastids. Here Yoo et al. show that nuclear phytochrome signaling triggers plastid gene expression via a novel dual-localized protein necessary for nuclear phytochrome signaling and subsequent anterograde signaling to the plastid. Light initiates chloroplast biogenesis by activating photosynthesis-associated genes encoded by not only the nuclear but also the plastidial genome, but how photoreceptors control plastidial gene expression remains enigmatic. Here we show that the photoactivation of phytochromes triggers the expression of photosynthesis-associated plastid-encoded genes ( PhAPG s) by stimulating the assembly of the bacterial-type plastidial RNA polymerase (PEP) into a 1000-kDa complex. Using forward genetic approaches, we identified REGULATOR OF CHLOROPLAST BIOGENESIS (RCB) as a dual-targeted nuclear/plastidial phytochrome signaling component required for PEP assembly. Surprisingly, RCB controls PhAPG expression primarily from the nucleus by interacting with phytochromes and promoting their localization to photobodies for the degradation of the transcriptional regulators PIF1 and PIF3. RCB-dependent PIF degradation in the nucleus signals the plastids for PEP assembly and PhAPG expression. Thus, our findings reveal the framework of a nucleus-to-plastid anterograde signaling pathway by which phytochrome signaling in the nucleus controls plastidial transcription. Light initiates chloroplast biogenesis by controlling gene expression in plastids. Here Yoo et al. show that nuclear phytochrome signaling triggers plastid gene expression via a novel dual-localized protein necessary for nuclear phytochrome signaling and subsequent anterograde signaling to the plastid. Abstract Light initiates chloroplast biogenesis by activating photosynthesis-associated genes encoded by not only the nuclear but also the plastidial genome, but how photoreceptors control plastidial gene expression remains enigmatic. Here we show that the photoactivation of phytochromes triggers the expression of photosynthesis-associated plastid-encoded genes ( PhAPG s) by stimulating the assembly of the bacterial-type plastidial RNA polymerase (PEP) into a 1000-kDa complex. Using forward genetic approaches, we identified REGULATOR OF CHLOROPLAST BIOGENESIS (RCB) as a dual-targeted nuclear/plastidial phytochrome signaling component required for PEP assembly. Surprisingly, RCB controls PhAPG expression primarily from the nucleus by interacting with phytochromes and promoting their localization to photobodies for the degradation of the transcriptional regulators PIF1 and PIF3. RCB-dependent PIF degradation in the nucleus signals the plastids for PEP assembly and PhAPG expression. Thus, our findings reveal the framework of a nucleus-to-plastid anterograde signaling pathway by which phytochrome signaling in the nucleus controls plastidial transcription. Light initiates chloroplast biogenesis by activating photosynthesis-associated genes encoded by not only the nuclear but also the plastidial genome, but how photoreceptors control plastidial gene expression remains enigmatic. Here we show that the photoactivation of phytochromes triggers the expression of photosynthesis-associated plastid-encoded genes (PhAPGs) by stimulating the assembly of the bacterial-type plastidial RNA polymerase (PEP) into a 1000-kDa complex. Using forward genetic approaches, we identified REGULATOR OF CHLOROPLAST BIOGENESIS (RCB) as a dual-targeted nuclear/plastidial phytochrome signaling component required for PEP assembly. Surprisingly, RCB controls PhAPG expression primarily from the nucleus by interacting with phytochromes and promoting their localization to photobodies for the degradation of the transcriptional regulators PIF1 and PIF3. RCB-dependent PIF degradation in the nucleus signals the plastids for PEP assembly and PhAPG expression. Thus, our findings reveal the framework of a nucleus-to-plastid anterograde signaling pathway by which phytochrome signaling in the nucleus controls plastidial transcription. Light initiates chloroplast biogenesis by activating photosynthesis-associated genes encoded by not only the nuclear but also the plastidial genome, but how photoreceptors control plastidial gene expression remains enigmatic. Here we show that the photoactivation of phytochromes triggers the expression of photosynthesis-associated plastid-encoded genes (PhAPGs) by stimulating the assembly of the bacterial-type plastidial RNA polymerase (PEP) into a 1000-kDa complex. Using forward genetic approaches, we identified REGULATOR OF CHLOROPLAST BIOGENESIS (RCB) as a dual-targeted nuclear/plastidial phytochrome signaling component required for PEP assembly. Surprisingly, RCB controls PhAPG expression primarily from the nucleus by interacting with phytochromes and promoting their localization to photobodies for the degradation of the transcriptional regulators PIF1 and PIF3. RCB-dependent PIF degradation in the nucleus signals the plastids for PEP assembly and PhAPG expression. Thus, our findings reveal the framework of a nucleus-to-plastid anterograde signaling pathway by which phytochrome signaling in the nucleus controls plastidial transcription. |
ArticleNumber | 2629 |
Author | Wang, He Pasoreck, Elise K Weigel, Detlef Chen, Meng Yoo, Chan Yul Blaha, Gregor M Cao, Jun |
Author_xml | – sequence: 1 givenname: Chan Yul orcidid: 0000-0001-6159-7443 surname: Yoo fullname: Yoo, Chan Yul organization: Department of Botany and Plant Sciences, Institute for Integrative Genome Biology, University of California, Riverside, CA, 92521, USA – sequence: 2 givenname: Elise K surname: Pasoreck fullname: Pasoreck, Elise K organization: Department of Botany and Plant Sciences, Institute for Integrative Genome Biology, University of California, Riverside, CA, 92521, USA – sequence: 3 givenname: He surname: Wang fullname: Wang, He organization: Department of Botany and Plant Sciences, Institute for Integrative Genome Biology, University of California, Riverside, CA, 92521, USA – sequence: 4 givenname: Jun surname: Cao fullname: Cao, Jun organization: Department of Molecular Biology, Max Planck Institute for Developmental Biology, 72076, Tübingen, Germany – sequence: 5 givenname: Gregor M surname: Blaha fullname: Blaha, Gregor M organization: Department of Biochemistry, University of California, Riverside, CA, 92521, USA – sequence: 6 givenname: Detlef surname: Weigel fullname: Weigel, Detlef organization: Department of Molecular Biology, Max Planck Institute for Developmental Biology, 72076, Tübingen, Germany – sequence: 7 givenname: Meng orcidid: 0000-0003-0351-5897 surname: Chen fullname: Chen, Meng email: meng.chen@ucr.edu organization: Department of Botany and Plant Sciences, Institute for Integrative Genome Biology, University of California, Riverside, CA, 92521, USA. meng.chen@ucr.edu |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31201355$$D View this record in MEDLINE/PubMed |
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Snippet | Light initiates chloroplast biogenesis by activating photosynthesis-associated genes encoded by not only the nuclear but also the plastidial genome, but how... Abstract Light initiates chloroplast biogenesis by activating photosynthesis-associated genes encoded by not only the nuclear but also the plastidial genome,... Light initiates chloroplast biogenesis by controlling gene expression in plastids. Here Yoo et al. show that nuclear phytochrome signaling triggers plastid... |
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SubjectTerms | Arabidopsis - physiology Arabidopsis Proteins - metabolism Assembly Basic Helix-Loop-Helix Transcription Factors - metabolism Biodegradation Biosynthesis Cell Nucleus - metabolism Chloroplasts Chloroplasts - genetics Chloroplasts - metabolism Degradation DNA-directed RNA polymerase DNA-Directed RNA Polymerases - metabolism Gene expression Gene Expression Regulation, Plant - radiation effects Genes Genomes Light Localization Photoactivation Photoreceptors Photosynthesis Photosynthesis - physiology Phytochrome - metabolism Phytochromes Plants, Genetically Modified Plastids Plastids - genetics Plastids - metabolism Proteolysis Regulators Ribonucleic acid RNA RNA polymerase Signal transduction Signal Transduction - physiology Signaling Thioredoxins - metabolism Transcription Transcription, Genetic - physiology Transcription, Genetic - radiation effects |
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Title | Phytochrome activates the plastid-encoded RNA polymerase for chloroplast biogenesis via nucleus-to-plastid signaling |
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