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Phytochrome activates the plastid-encoded RNA polymerase for chloroplast biogenesis via nucleus-to-plastid signaling

Author

Listed:
  • Chan Yul Yoo

    (University of California)

  • Elise K. Pasoreck

    (University of California)

  • He Wang

    (University of California)

  • Jun Cao

    (Max Planck Institute for Developmental Biology)

  • Gregor M. Blaha

    (University of California)

  • Detlef Weigel

    (Max Planck Institute for Developmental Biology)

  • Meng Chen

    (University of California)

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.

Suggested Citation

  • Chan Yul Yoo & Elise K. Pasoreck & He Wang & Jun Cao & Gregor M. Blaha & Detlef Weigel & Meng Chen, 2019. "Phytochrome activates the plastid-encoded RNA polymerase for chloroplast biogenesis via nucleus-to-plastid signaling," Nature Communications, Nature, vol. 10(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-10518-0
    DOI: 10.1038/s41467-019-10518-0
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    Cited by:

    1. Chanhee Kim & Yongmin Kwon & Jaehoon Jeong & Minji Kang & Ga Seul Lee & Jeong Hee Moon & Hyo-Jun Lee & Youn-Il Park & Giltsu Choi, 2023. "Phytochrome B photobodies are comprised of phytochrome B and its primary and secondary interacting proteins," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    2. Youra Hwang & Soeun Han & Chan Yul Yoo & Liu Hong & Chenjiang You & Brandon H. Le & Hui Shi & Shangwei Zhong & Ute Hoecker & Xuemei Chen & Meng Chen, 2022. "Anterograde signaling controls plastid transcription via sigma factors separately from nuclear photosynthesis genes," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    3. Ruth Jean Ae Kim & De Fan & Jiangman He & Keunhwa Kim & Juan Du & Meng Chen, 2024. "Photobody formation spatially segregates two opposing phytochrome B signaling actions of PIF5 degradation and stabilization," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    4. Juan Du & Keunhwa Kim & Meng Chen, 2024. "Distinguishing individual photobodies using Oligopaints reveals thermo-sensitive and -insensitive phytochrome B condensation at distinct subnuclear locations," Nature Communications, Nature, vol. 15(1), pages 1-12, December.

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