GUN1 and Plastid RNA Metabolism: Learning from Genetics.

Luca Tadini,Paolo Pesaresi,Nicolaj Jeran

doi:10.3390/cells9102307

Abstract

GUN1 (genomes uncoupled 1), a chloroplast-localized pentatricopeptide repeat (PPR) protein with a C-terminal small mutS-related (SMR) domain, plays a central role in the retrograde communication of chloroplasts with the nucleus. This flow of information is required for the coordinated expression of plastid and nuclear genes, and it is essential for the correct development and functioning of chloroplasts. Multiple genetic and biochemical findings indicate that GUN1 is important for protein homeostasis in the chloroplast; however, a clear and unified view of GUN1′s role in the chloroplast is still missing. Recently, GUN1 has been reported to modulate the activity of the nucleus-encoded plastid RNA polymerase (NEP) and modulate editing of plastid RNAs upon activation of retrograde communication, revealing a major role of GUN1 in plastid RNA metabolism. In this opinion article, we discuss the recently identified links between plastid RNA metabolism and retrograde signaling by providing a new and extended concept of GUN1 activity, which integrates the multitude of functional genetic interactions reported over the last decade with its primary role in plastid transcription and transcript editing.

Highlights

The GUN1 protein is a pentatricopeptide repeat (PPR)-containing protein that localizes to plastids and relays signals to the nucleus after exposure to either norflurazon (NF) or lincomycin (Lin) treatment [1,2]
Later studies have shown that loss of sigma factor 2 (SIG2) or 6 (SIG6)—each of which is utilized by the plastid-encoded RNA polymerase (PEP) to transcribe specific sets of plastid genes [8,9,10]— activates retrograde signaling [11]
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

Summary

Introduction

The GUN1 (genomes uncoupled 1) protein is a pentatricopeptide repeat (PPR)-containing protein that localizes to plastids and relays signals to the nucleus after exposure to either norflurazon (NF) or lincomycin (Lin) treatment [1,2]. NEP-dependent transcript levels are increased encoded plastid proteins required for PEP activity (SIG6, PAP2, PAP8, PRIN2) or mRNA maturation in plastids, giving rise toHowever, what isgun known as the “∆-rpo phenotype”. Like plastid gene expression, indicating that the drastically reduced accumulation of PEP- and NEPgun seedlings grown on norflurazon-containing medium (gun1 + NF) undergo severe repression dependent transcripts upon NF treatment is a characteristic of the gun genetic background. 5) seedlingsthat in serve the presence of modulate the activities of NEP and PEP enzymes during plastid differentiation and in the course of norflurazon (Col-0 + NF and gun5 + NF) show a wild-type-like plastid gene expression, indicating that responses of mature chloroplasts to environmental cues [27,29,30,31].

GUN1 andfavored

Findings

Conclusions and Open Questions