NCP activates chloroplast transcription by controlling phytochrome-dependent dual nuclear and plastidial switches

Abstract

Phytochromes initiate chloroplast biogenesis by activating genes encoding the photosynthetic apparatus, including photosynthesis-associated plastid-encoded genes ( PhAPG s). PhAPG s are transcribed by a bacterial-type RNA polymerase (PEP), but how phytochromes in the nucleus activate chloroplast gene expression remains enigmatic. We report here a forward genetic screen in Arabidopsis that identified NUCLEAR CONTROL OF PEP ACTIVITY (NCP) as a necessary component of phytochrome signaling for PhAPG activation. NCP is dual-targeted to plastids and the nucleus. While nuclear NCP mediates the degradation of two repressors of chloroplast biogenesis, PIF1 and PIF3, NCP in plastids promotes the assembly of the PEP complex for PhAPG transcription. NCP and its paralog RCB are non-catalytic thioredoxin-like proteins that diverged in seed plants to adopt nonredundant functions in phytochrome signaling. These results support a model in which phytochromes control PhAPG expression through light-dependent double nuclear and plastidial switches that are linked by evolutionarily conserved and dual-localized regulatory proteins.

Increasing ambient temperature progressively disassembles Arabidopsis phytochrome B from individual photobodies with distinct thermostabilities

“…In particular, PCH1 and PCHL facilitate the PB localization of phyB [50][51][52] . Molecular genetic studies showed that PB localization of phyB requires a number of signaling components, including HMR (HEMERA) 44,65 , RCB (REGULATOR OF CHLOROPLAST BIOGENESIS) 47 , and NCP (NUCLEAR CONTROL OF PEP ACTIVITY) 48 . Both HMR and RCB interact directly with phyB 47,65 .…”

“…By contrast, shade conditions and dim light, which enhance the conversion to the Pr, lead to the relocalization of phyB-FP from PBs to tens of small foci of 0.1-0.7 μm in diameter and the nucleoplasm 40,45 . Molecular genetic studies on mutants with altered PB patterns indicate that PBs are required for phyB signaling 44,[46][47][48][49][50][51][52][53] .…”

Transcriptional regulatory network of the light signaling pathways

“…Four proteins regulate this process: the nucleus-localized PHOTOPERIODIC CONTROL OF HYPOCOTYL 1 (PCH1) and chloroplast/nuclear dual-localized proteins HEMERA (HMR), NUCLEAR CONTROL OF PEP ACTIVITY (NCP), and REGULATOR OF CHLOROPLAST BIOGENESIS (RCB) (Chen et al, 2010;Enderle et al, 2017;Huang et al, 2019;Yang et al, 2019;Yoo et al, 2019). In response to light, HMR, NCP, and RCB are also involved in the coordinating of photosynthesis-associated gene expression in the nucleus and chloroplast (Chen et al, 2010;Yang et al, 2019;Yoo et al, 2019). Interestingly, PCH1 and PCHL expression is circadian regulated and peaks at dusk, in correlation with the formation of large phyB photobodies (Enderle et al, 2017;Huang et al, 2019).…”

Coordinating light responses between the nucleus and the chloroplast, a role for plant cryptochromes and phytochromes

“…Plastome transcription involves the activity of a nuclear‐encoded RNA polymerase (NEP) and a plastid‐encoded RNA polymerase (PEP) (Del Campo 2009). Photoreceptor links to the modulation of transcriptional processes in the chloroplast are illustrated by the NEP activity repression by CRY2 (Facella et al 2017), and the modulation by phys and crys of several components required for PEP activity, including the transcriptional co‐factors sigma factors and proteins, such as nuclear control of PEP (NCP), PEP‐related development arrested 1 (PRDA1) (Ohgishi et al 2004, Qiao et al 2013, Oh and Montgomery 2014, Yang et al 2019, Yoo et al 2019), and HEMERA (HMR)/plastid transcriptionally active chromosome complex 12 (pTAC12) (Pfalz et al 2006, Chen et al 2010). Yet, plastid‐encoded genes are generally organized into polycistronic operons, and chloroplast transcription rates and steady‐state mRNA levels tend not to be comparable, pointing at a broad impact of post‐transcriptional regulation in modulating the plastome gene expression (Deng et al 1989).…”