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

Nat Commun. 2019 Jun 14;10(1):2630. 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.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Arabidopsis / physiology
  • Arabidopsis Proteins / metabolism*
  • Basic Helix-Loop-Helix Transcription Factors / metabolism
  • Cell Nucleus / genetics
  • Cell Nucleus / metabolism
  • Chloroplasts / genetics
  • Chloroplasts / metabolism*
  • DNA-Directed RNA Polymerases / metabolism
  • Gene Expression Regulation, Plant / radiation effects
  • Light
  • Molecular Chaperones / metabolism*
  • Photosynthesis / physiology
  • Phytochrome / metabolism*
  • Plants, Genetically Modified
  • Plastids / genetics
  • Plastids / metabolism
  • Signal Transduction / physiology
  • Transcription, Genetic / physiology*
  • Transcription, Genetic / radiation effects

Substances

  • Arabidopsis Proteins
  • At2g31840 protein, Arabidopsis
  • Basic Helix-Loop-Helix Transcription Factors
  • Molecular Chaperones
  • PIF1 protein, Arabidopsis
  • PIF3 protein, Arabidopsis
  • Phytochrome
  • DNA-Directed RNA Polymerases