Light-regulated dual-targeting of NUCLEAR CONTROL OF PEP ACTIVITY establishes photomorphogenesis via interorganellar communication

Abstract

Interorganellar communication is essential for maintaining cellular and organellar functions and adapting to dynamic environmental changes in eukaryotic cells. In angiosperms, light initiates photomorphogenesis, a developmental program characterized by chloroplast biogenesis and inhibition of hypocotyl elongation, through photoreceptors such as the red/far-red-sensing phytochromes and their downstream signaling pathways. However, the mechanisms underlying nucleus-chloroplast crosstalk during photomorphogenesis remain elusive. Here, we show that light-regulated dual-targeting of NUCLEAR CONTROL OF PEP ACTIVITY (NCP) mediates bidirectional communication between the nucleus and chloroplasts via alternative promoter selection and retrograde translocation. Light promotes transcription from an upstream canonical transcription start site, producing a long NCP isoform (NCP-L) containing an N-terminal chloroplast transit peptide that directs chloroplast localization. In contrast, darkness or low red-light conditions favor transcription from a downstream alternative start site, producing a shorter cytoplasmic isoform (NCP-S) that is rapidly degraded via the 26S proteasome. This light-regulated alternative transcription initiation depends on PHYTOCHROME-INTERACTING FACTORS (PIFs), key repressors of photomorphogenesis. Upon chloroplast import, NCP-L is processed into its mature form (NCPm), which promotes assembly and nucleoid localization of the PEP complex to initiate chloroplast biogenesis. Notably, NCP's nuclear function requires its prior localization to chloroplasts, supporting a model in which NCP mediates chloroplast-to-nucleus retrograde signaling. Consistent with this, NCP promotes stromule formation in Arabidopsis (Arabidopsis thaliana) hypocotyls, linking chloroplast dynamics to phytochrome-dependent nuclear pathways that restrict hypocotyl elongation. Our findings uncover an interorganellar communication mechanism in which light-dependent alternative promoter usage and retrotranslocation regulate photomorphogenesis, integrating nuclear and plastid signals to coordinate organ-specific developmental programs.