The plastid transcription machinery and its coordination with the expression of nuclear genome: Plastid-Encoded Polymerase, Nuclear-Encoded Polymerase and the Genomes Uncoupled 1-mediated retrograde communication

Abstract

Plastid genes in higher plants are transcribed by at least two different RNA polymerases, the plastid-encoded RNA polymerase (PEP), a bacteria-like core enzyme whose subunits are encoded by plastid genes ( rpoA , rpoB , rpoC1 and rpoC2 ), and the nuclear-encoded plastid RNA polymerase (NEP), a monomeric bacteriophage-type RNA polymerase. Both PEP and NEP enzymes are active in non-green plastids and in chloroplasts at all developmental stages. Their transcriptional activity is affected by endogenous and exogenous factors and requires a strict coordination within the plastid and with the nuclear gene expression machinery. This review focuses on the different molecular mechanisms underlying chloroplast transcription regulation and its coordination with the photosynthesis-associated nuclear genes ( PhANGs ) expression. Particular attention is given to the link between NEP and PEP activity and the GUN1- (Genomes Uncoupled 1) mediated chloroplast-to-nucleus retrograde communication with respect to the Δrpo adaptive response, i.e. the increased accumulation of NEP-dependent transcripts upon depletion of PEP activity, and the editing-level changes observed in NEP-dependent transcripts, including rpoB and rpoC1 , in gun1 cotyledons after norflurazon or lincomycin treatment. The role of cytosolic preproteins and HSP90 chaperone as components of the GUN1-retrograde signalling pathway, when chloroplast biogenesis is inhibited in Arabidopsis cotyledons, is also discussed. This article is part of the theme issue ‘Retrograde signalling from endosymbiotic organelles’.

Origins and Molecular Evolution of the NusG Paralog RfaH

“…Multiple Spt5 KOW domains play analogous functions in eukaryotes, coupling RNA synthesis to splicing, polyadenylation, and other cotranscriptional processes ( 3 ). Transcription of chloroplast genomes by PEP depends on its binding to several accessory proteins ( 68 ), including NusG ( 45 ). We speculate that the NusG-KOW domain acts as a hub for PEP complex assembly.…”

GUN1 and Plastid RNA Metabolism: Learning from Genetics

“…Over the past decade, several labs worldwide have collected important pieces of genetic and molecular information concerning the role of GUN1 during the early stages of chloroplast biogenesis. The very recent data on the involvement of GUN1 in plastid RNA metabolism obtained in our lab, almost concomitantly with the labs of Joanne Chory and Enrique Lopez-Juez, allow us to integrate all the information now available into a unified model, which is schematically depicted in Figure 2 [ 12 , 13 , 14 , 15 , 16 ]. As yet, little can be said about how GUN1 is recruited to modulate transcript accumulation and editing under conditions that trigger retrograde communication.…”

“…GUN1 does not appear to bind directly to RNAs [ 17 ], unlike typical PPR proteins [ 17 ]. But it is targeted to an organelle, the chloroplast, and has recently been reported by two independent laboratories to influence plastid transcript accumulation [ 13 , 14 , 15 ]. In particular, following perturbation of PEP activity, a peculiar pattern of plastid transcription, designated as the “ Δ-rpo phenotype”, is typically observed in different plant species [ 14 , 18 , 19 , 20 ].…”

“…The recent findings that point to a primary and direct role of GUN1 in plastid RNA metabolism imply that the protein stimulates NEP activity and alters editing levels of a few NEP-dependent transcripts [ 12 , 13 , 14 , 15 , 16 ] and offer a novel perspective on GUN1 activity. In particular, the decreased accumulation of NEP-dependent transcripts, i.e., transcripts encoding mainly rRNA, tRNA, and housekeeping proteins, and the reduced editing levels of some of them observed in gun1 seedlings upon either NF or Lin treatments, straightforwardly explain the additive effects observed in gun1 -containing double mutants with defects in (i) plastid transcription, (ii) plastid transcript maturation and editing, and (iii) plastid translation.…”

“…Here, we propose a new model for GUN1 function in plastids and GUN1-mediated retrograde communication, which integrates the interactions observed between GUN1 and the machinery that controls plastid protein homeostasis with the recently discovered role of GUN1 in plastid RNA metabolism [ 12 , 13 , 14 , 15 , 16 ]. The many additive phenotypic effects and the very few suppressor phenotypes observed in higher-order (compound) mutants containing gun1 together with mutations affecting various aspects of plastid protein homeostasis, sugar sensing, and plastid osmosis can all be interpreted as pleiotropic phenotypic effects of a primary alteration in plastid transcription and plastid transcript editing attributable to the lack of the GUN1 protein under conditions that would otherwise trigger plastid-to-nucleus retrograde communication.…”