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

Tai-Ping Sun,Emily J Yang,Jiangxin Liu,Detlef Weigel,Meng Chen,Fay-Wei Li,Pei Zhou,Kathleen M Pryer,Jun Cao,Chan Yul Yoo,He Wang

doi:10.1038/s41467-019-10517-1

Abstract

Phytochromes initiate chloroplast biogenesis by activating genes encoding the photosynthetic apparatus, including photosynthesis-associated plastid-encoded genes (PhAPGs). PhAPGs 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.

Highlights

Phytochromes initiate chloroplast biogenesis by activating genes encoding the photosynthetic apparatus, including photosynthesis-associated plastid-encoded genes (PhAPGs)
We focused on one of the mutants, which we named ncp-1 (Fig. 1a, b)
NUCLEAR CONTROL OF plastidencoded RNA polymerase (PEP) ACTIVITY (NCP)-HA-His in vivo was significantly smaller than the in vitro translated full-length NCPHA-His and similar to NCPΔ48-HA-His (Fig. 3b). These results indicate that NCP is dual-targeted to plastids and the nucleus and imply that NCP might localize to the plastids first and translocate to the nucleus similar to HMR41

Summary

Introduction

Phytochromes initiate chloroplast biogenesis by activating genes encoding the photosynthetic apparatus, including photosynthesis-associated plastid-encoded genes (PhAPGs). 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. The regulation of plastid-encoded photosynthesis-associated genes is pivotal for plants to establish photosynthetically active chloroplasts and is essential for plant survival. Most PIFs accumulate to high levels in dark-grown seedlings to promote hypocotyl elongation and inhibit chloroplast biogenesis by activating growth-relevant genes and repressing nuclearencoded photosynthesis-associated genes, respectively[15,16]. PHY-mediated PIF degradation is a central mechanism for inducing chloroplast biogenesis through the activation of photosynthesis-associated nuclear-encoded genes (PhANGs)[14]. The localization of PHYs to photobodies is closely associated with PIF3 degradation[12,13,17,19,20]

Methods

Results

Conclusion