Mechanism of nucleus-chloroplast communication by alternative promoter usage and stromules to establish photomorphogenesis in Arabidopsis

Abstract

Interorganellar communication is essential for maintaining cellular and organellar functions and adapting to dynamic environmental changes in eukaryotic cells. In plants, light triggers photomorphogenic development, including chloroplast biogenesis and the inhibition of hypocotyl elongation, through photoreceptors such as the red/far-red-sensing phytochromes and their downstream signaling pathways. However, the mechanism of interorganellar crosstalk underlying photomorphogenesis remains elusive. Here, we investigate the role of light-regulated alternative promoter usage in NUCLEAR CONTROL OF PEP ACTIVITY (NCP), a gene encoding a phytochrome signaling component that is dual-localized to the nucleus and chloroplasts. The long transcript variant (NCP-L) is upregulated under high red light, while the short variant (NCP-S) predominates in dark or low red light conditions. This light-regulated alternative transcription initiation of NCP is dependent on PHYTOCHROME-INTERACTING FACTORS (PIFs). The NCP-L isoform primarily localizes to chloroplasts, whereas the NCP-S isoform is found in the cytoplasm and nucleus. Notably, chloroplast-localized NCP-L translocates to the nucleus via stromules. Consequently, NCP-L, present in both chloroplasts and the nucleus, initiates chloroplast biogenesis and inhibits hypocotyl growth during photomorphogenesis, whereas NCP-S is nonfunctional and degraded by the 26S proteasome. Taken together, our findings elucidate the mechanisms by which light-regulated NCP alternative promoter usage and NCP retrotranslocation via stromules control photomorphogenesis in Arabidopsis. These mechanisms provide insights into interorganellar communication, orchestrating organ-specific developmental processes in response to fluctuating light environments.