TY - JOUR

T1 - Nucleo-plastidic PAP8/pTAC6 couples chloroplast formation with photomorphogenesis

AU - Liebers, Monique

AU - Gillet, François-Xavier

AU - Israel, Abir

AU - Pounot, Kevin

AU - Chambon, Louise

AU - Chieb, Maha

AU - Chevalier, Fabien

AU - Ruedas, Rémi

AU - Favier, Adrien

AU - Gans, Pierre

AU - Boeri Erba, Elisabetta

AU - Cobessi, David

AU - Pfannschmidt, Thomas

AU - Blanvillain, Robert

N1 - Funding Information: We acknowledge the platforms of the Grenoble Instruct‐ERIC Centre (ISBG; UMS 3518 CNRS‐CEA‐UGA‐EMBL) within the Grenoble Partnership for Structural Biology (PSB). Platform access was supported by FRISBI (ANR‐10‐INBS‐05‐02) and GRAL, a project of the University Grenoble Alpes Graduate School (Ecoles Universitaires de Recherche) CBH‐EUR‐GS (ANR‐17‐EURE‐0003). IBS acknowledges integration into the Interdisciplinary Research Institute of Grenoble (IRIG, CEA). The work was supported by the (grant PepRegulChloro3D), the to T.P. (PF323‐5) and the AGIR programme of (UGA) to R.B. The project received further support by institutional grants to the by Labex Grenoble Alliance of Integrated Structural Biology (GRAL) and ANR‐17‐EURE‐0003. We thank F Barneche for the ChIP‐seq analysis at the PAP8 locus; E Monte and G Toledo‐Ortiz for seeds; A Guerrero‐Criado, R Toutain and S Coveley for their help at the bench. We thank E Thevenon in the Parcy Lab for advice on fluorescent labelling EMSA. We thank S Lerbs‐Mache for critical reading. We express our gratitude in memory of D Grunwald for his help on confocal imaging. Agence National de la Recherche Deutsche Forschungsgemeinschaft Université Grenoble‐Alpes Laboratoire de Physiologie Cellulaire et Végétale pifq

PY - 2020/11/16

Y1 - 2020/11/16

N2 - The initial greening of angiosperms involves light activation of photoreceptors that trigger photomorphogenesis, followed by the development of chloroplasts. In these semi-autonomous organelles, construction of the photosynthetic apparatus depends on the coordination of nuclear and plastid gene expression. Here, we show that the expression of PAP8, an essential subunit of the plastid-encoded RNA polymerase (PEP) in Arabidopsis thaliana, is under the control of a regulatory element recognized by the photomorphogenic factor HY5. PAP8 protein is localized and active in both plastids and the nucleus, and particularly required for the formation of late photobodies. In the pap8 albino mutant, phytochrome-mediated signalling is altered, degradation of the chloroplast development repressors PIF1/PIF3 is disrupted, HY5 is not stabilized, and the expression of the photomorphogenesis regulator GLK1 is impaired. PAP8 translocates into plastids via its targeting pre-sequence, interacts with the PEP and eventually reaches the nucleus, where it can interact with another PEP subunit pTAC12/HMR/PAP5. Since PAP8 is required for the phytochrome B-mediated signalling cascade and the reshaping of the PEP activity, it may coordinate nuclear gene expression with PEP-driven chloroplastic gene expression during chloroplast biogenesis.

AB - The initial greening of angiosperms involves light activation of photoreceptors that trigger photomorphogenesis, followed by the development of chloroplasts. In these semi-autonomous organelles, construction of the photosynthetic apparatus depends on the coordination of nuclear and plastid gene expression. Here, we show that the expression of PAP8, an essential subunit of the plastid-encoded RNA polymerase (PEP) in Arabidopsis thaliana, is under the control of a regulatory element recognized by the photomorphogenic factor HY5. PAP8 protein is localized and active in both plastids and the nucleus, and particularly required for the formation of late photobodies. In the pap8 albino mutant, phytochrome-mediated signalling is altered, degradation of the chloroplast development repressors PIF1/PIF3 is disrupted, HY5 is not stabilized, and the expression of the photomorphogenesis regulator GLK1 is impaired. PAP8 translocates into plastids via its targeting pre-sequence, interacts with the PEP and eventually reaches the nucleus, where it can interact with another PEP subunit pTAC12/HMR/PAP5. Since PAP8 is required for the phytochrome B-mediated signalling cascade and the reshaping of the PEP activity, it may coordinate nuclear gene expression with PEP-driven chloroplastic gene expression during chloroplast biogenesis.

KW - Acid Phosphatase/genetics

KW - Arabidopsis/genetics

KW - Arabidopsis Proteins/genetics

KW - Cell Nucleus/metabolism

KW - Chloroplasts/genetics

KW - DNA-Directed RNA Polymerases/metabolism

KW - Gene Expression Regulation, Plant

KW - Light

KW - Morphogenesis/physiology

KW - Organelle Biogenesis

KW - Phytochrome/metabolism

KW - Plants, Genetically Modified

KW - Plastids/genetics

KW - Signal Transduction

KW - Transcription Factors

KW - Transcription, Genetic

KW - photobodies

KW - Arabidopsis PEP/PAPs

KW - biogenesis

KW - photomorphogenesis

KW - chloroplast

UR - http://www.scopus.com/inward/record.url?scp=85091725380&partnerID=8YFLogxK

U2 - 10.15252/embj.2020104941

DO - 10.15252/embj.2020104941

M3 - Article

C2 - 33001465

VL - 39

JO - The EMBO journal

JF - The EMBO journal

SN - 0261-4189

IS - 22

M1 - e104941

ER -