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Anterograde signaling controls plastid transcription via sigma factors separately from nuclear photosynthesis genes

Author

Listed:
  • Youra Hwang

    (University of California)

  • Soeun Han

    (University of California
    University of California, San Diego)

  • Chan Yul Yoo

    (University of California
    University of Utah)

  • Liu Hong

    (University of California)

  • Chenjiang You

    (University of California
    Fudan University)

  • Brandon H. Le

    (University of California)

  • Hui Shi

    (Capital Normal University)

  • Shangwei Zhong

    (Peking University)

  • Ute Hoecker

    (University of Cologne)

  • Xuemei Chen

    (University of California)

  • Meng Chen

    (University of California)

Abstract

Light initiates chloroplast biogenesis in Arabidopsis by eliminating PHYTOCHROME-INTERACTING transcription FACTORs (PIFs), which in turn de-represses nuclear photosynthesis genes, and synchronously, generates a nucleus-to-plastid (anterograde) signal that activates the plastid-encoded bacterial-type RNA polymerase (PEP) to transcribe plastid photosynthesis genes. However, the identity of the anterograde signal remains frustratingly elusive. The main challenge has been the difficulty to distinguish regulators from the plethora of necessary components for plastid transcription and other essential chloroplast functions, such as photosynthesis. Here, we show that the genome-wide induction of nuclear photosynthesis genes is insufficient to activate the PEP. PEP inhibition is imposed redundantly by multiple PIFs and requires PIF3’s activator activity. Among the nuclear-encoded components of the PEP holoenzyme, we identify four light-inducible, PIF-repressed sigma factors as anterograde signals. Together, our results elucidate that light-dependent inhibition of PIFs activates plastid photosynthesis genes via sigma factors as anterograde signals in parallel with the induction of nuclear photosynthesis genes.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-35080-0
    DOI: 10.1038/s41467-022-35080-0
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    References listed on IDEAS

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    1. Weimin Ni & Shou-Ling Xu & Eduardo González-Grandío & Robert J. Chalkley & Andreas F. R. Huhmer & Alma L. Burlingame & Zhi-Yong Wang & Peter H. Quail, 2017. "PPKs mediate direct signal transfer from phytochrome photoreceptors to transcription factor PIF3," Nature Communications, Nature, vol. 8(1), pages 1-11, August.
    2. 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.
    3. Hak Soo Seo & Jun-Yi Yang & Masaki Ishikawa & Cordelia Bolle & Maria L. Ballesteros & Nam-Hai Chua, 2003. "LAF1 ubiquitination by COP1 controls photomorphogenesis and is stimulated by SPA1," Nature, Nature, vol. 423(6943), pages 995-999, June.
    4. Emily J. Yang & Chan Yul Yoo & Jiangxin Liu & He Wang & Jun Cao & Fay-Wei Li & Kathleen M. Pryer & Tai-ping Sun & Detlef Weigel & Pei Zhou & Meng Chen, 2019. "NCP activates chloroplast transcription by controlling phytochrome-dependent dual nuclear and plastidial switches," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
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    Cited by:

    1. Runlai Hang & Hao Li & Wenjing Liu & Runyu Wang & Hao Hu & Meng Chen & Chenjiang You & Xuemei Chen, 2024. "HOT3/eIF5B1 confers Kozak motif-dependent translational control of photosynthesis-associated nuclear genes for chloroplast biogenesis," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

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