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

Youra Hwang, Soeun Han, Chan Yul Yoo, Liu Hong, Chenjiang You, Brandon H. Le, Hui Shi, Shangwei Zhong, Ute Hoecker, Xuemei Chen and Meng Chen ()
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Youra Hwang: University of California
Soeun Han: University of California
Chan Yul Yoo: University of California
Liu Hong: University of California
Chenjiang You: University of California
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

Nature Communications, 2022, vol. 13, issue 1, 1-16

Abstract: 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.

Date: 2022
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DOI: 10.1038/s41467-022-35080-0

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