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.
Highlights
Light initiates chloroplast biogenesis by activating photosynthesis-associated genes encoded by the nuclear and the plastidial genome, but how photoreceptors control plastidial gene expression remains enigmatic
We have elucidated the framework of a nucleus-to-plastid or anterograde light signaling pathway that is initiated by PHYs in the nucleus to activate photosynthesis-associated plastid-encoded genes (PhAPGs) in the plastids for chloroplast biogenesis (Fig. 7f)
Our results demonstrate that REGULATOR OF CHLOROPLAST BIOGENESIS (RCB)-dependent photobody biogenesis and degradation of nuclear repressors of chloroplast biogenesis, PIF1 and PIF3, trigger anterograde signaling to the plastids for the assembly and activation of the plastid-encoded RNA polymerase (PEP) for PhAPG expression (Fig. 7f)
Summary
Light initiates chloroplast biogenesis by activating photosynthesis-associated genes encoded by the nuclear and the plastidial genome, but how photoreceptors control plastidial gene expression remains enigmatic. As an environmental signal, light reprograms hundreds of genes in the nucleus to initiate the developmental transition from heterotrophic growth supported by seed-stored energy to autotrophic growth, which relies on photosynthesis[7,9]. In dicotyledonous plants, such as Arabidopsis thaliana, young seedlings that germinate underground adopt a dark-grown developmental program called skotomorphogenesis or etiolation, which inhibits leaf development and promotes elongation of the embryonic stem (hypocotyl), allowing seedlings to emerge quickly from the soil into the light. Light is first perceived by a suite of photoreceptors, including the red (R)-
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