Chloroplast Redox Control of Nuclear Gene Expression—A New Class of Plastid Signals in Interorganellar Communication

Institute of General Botany, Department of Plant Physiology, University of Jena, Jena, Germany.
Antioxidants and Redox Signaling (Impact Factor: 7.41). 03/2003; 5(1):95-101. DOI: 10.1089/152308603321223586
Source: PubMed


Chloroplasts are genetically semiautonomous organelles that contain their own subset of 100-120 genes coding for chloroplast proteins, tRNAs, and rRNAs. However, the great majority of the chloroplast proteins are encoded in the nucleus and must be imported into the organelle after their translation in the cytosol. This arrangement requires a high degree of coordination between the gene expression machineries in chloroplasts and nucleus, which is achieved by a permanent exchange of information between both compartments. The existence of such coordinating signals has long been known; however, the underlying molecular mechanisms and signaling routes are not understood. The present data indicate that the expression of nuclear-encoded chloroplast proteins is coupled to the functional state of the chloroplasts. Photosynthesis, which is the major function of chloroplasts, plays a crucial role in this context. Changes in the reduction/oxidation (redox) state of components of the photosynthetic machinery act as signals, which regulate the expression of chloroplast proteins in both chloroplasts and nucleus and help to coordinate the expression both in compartments. Recent advances in understanding chloroplast redox regulation of nuclear gene expression are summarized, and the importance for intracellular signaling is discussed.

Download full-text


Available from: Thomas Pfannschmidt
  • Source
    • "In fully matured chloroplasts, a functional regulation that depends on environmental cues such as light variations becomes more dominant. This functional regulation is mediated mainly by the chloroplast itself, for instance by redox signals from photosynthesis (Pfannschmidt et al., 2003). The orchestration of the different transcription machineries, thus, Fig. 1. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Chloroplasts are the sunlight-collecting organelles of photosynthetic eukaryotes that energetically drive the biosphere of our planet. They are the base for all major food webs by providing essential photosynthates to all heterotrophic organisms including humans. Recent research has focused largely on an understanding of the function of these organelles, but knowledge about the biogenesis of chloroplasts is rather limited. It is known that chloroplasts develop from undifferentiated precursor plastids, the proplastids, in meristematic cells. This review focuses on the activation and action of plastid RNA polymerases, which play a key role in the development of new chloroplasts from proplastids. Evolutionarily, plastids emerged from the endosymbiosis of a cyanobacterium-like ancestor into a heterotrophic eukaryote. As an evolutionary remnant of this process, they possess their own genome, which is expressed by two types of plastid RNA polymerase, phage-type and prokaryotic-type RNA polymerase. The protein subunits of these polymerases are encoded in both the nuclear and plastid genomes. Their activation and action therefore require a highly sophisticated regulation that controls and coordinates the expression of the components encoded in the plastid and nucleus. Stoichiometric expression and correct assembly of RNA polymerase complexes is achieved by a combination of developmental and environmentally induced programmes. This review highlights the current knowledge about the functional coordination between the different types of plastid RNA polymerases and provides working models of their sequential expression and function for future investigations.
    Full-text · Article · Sep 2015 · Journal of Experimental Botany
  • Source
    • "Molecular mechanisms of redox-sensitive regulation of protein have also been explained for plants and other living organisms (Cvetkovska et al., 2005; Foyer and Noctor, 2005). ROS mediated signaling involves hetero-trimeric G-proteins and MAP kinase regulated protein phosphorylation and protein Tyr phosphatases (Pfannschmidt et al., 2003; Foyer and Noctor, 2005; Kiffin et al., 2006). Mitogen-activated protein kinase (MAPK) cascades are mainly engaged by eukaryotes which have got much concentration for research since long years. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Plant cells are often exposed to oxidative cellular environments which result in the generation of toxic reactive oxygen species (ROS). In order to detoxify the harmful ROS, plants have evolved various strategies including their scavenging and antioxidant machinery. Plant cellscontain many enzymatic and non-enzymatic antioxidants which aid in removing the toxic oxygen molecules. Various antioxidant molecules localized within different cellular compartments play crucial role(s) during this process, which includes both redox-signalling and redox-homeostasis. The present review gives an overview of cellular oxidativeenvironment, redox signalling operative within a cell and contributions of major cellular organelles towards maintaining the redox homeostasis. Additionally, the importance of various antioxidant enzymes working in an orchestrated and coordinated manner within acell, to protect it from stress injury has been presented. We also present the state-of-the-art where transgenic approach has been used to improve stress tolerance in model and crop species by engineering one or more than one of these components of the ROS scavenging machinery.
    Full-text · Article · Dec 2014
    • "It was demonstrated that the gun4 mutation affects the composition of the PSI core complex, which leads to imbalanced excitation pressure between two photosystems (Formighieri et al., 2012). Changes in the redox state of plastid electron transfer chain (ETC) components were shown to be involved in the retrograde signalling (Pfannschmidt et al., 2003; Brautigam et al., 2009; Lemeille and Rochaix, 2010). Thus, hypothetically, the deregulated gene expression in the strain lacking GUN4 might be the effect of retrograde signals originating from the changes in redox state of the photosynthetic ETC; however, as observed in gun4, a general upregulation of tetrapyrrole biosynthesis and PhAN genes would not be expected in response to an over-reduction of ETC components. "
    [Show abstract] [Hide abstract]
    ABSTRACT: The GUN4 (GENOMES UNCOUPLED 4) protein is found only in aerobic photosynthetic organisms. We investigated the role of GUN4 in metabolic activities of the Mg branch of the tetrapyrrole biosynthesis pathway and the plastid signal-mediated changes of nuclear gene expression in Chlamydomonas reinhardtii. In light gun4 accumulates only 40% of the wild-type chlorophyll level. Light or dark-grown gun4 accumulates high amounts of protoporphyrin IX (Proto) and displays increased sensitivity to moderate light intensities. Despite the photooxidative stress, gun4 fails to down-regulate mRNA levels of the tetrapyrrole biosynthesis and the photosynthesis-associated nuclear genes (PhANGs). In contrast, upon illumination the Proto-accumulating and light-sensitive chlD-1 mutant displays expected down-regulation of the same nuclear genes. Although chlD-1 and wild type have similar GUN4 transcript levels, the GUN4 protein in chlD-1 is hardly detectable. Overexpression of GUN4 in chlD-1 modifies down-regulation of the nuclear gene expression, but also increases light tolerance. Therefore, GUN4 is proposed to function in shielding Proto, and most likely MgProto, by reducing reactivity with O2. Furthermore, GUN4 seems to be involved in sensing the elevated levels of these photoreactive tetrapyrrole intermediates and contributing to 1O2-mediated retrograde signalling, originating from chlorophyll biosynthesis.This article is protected by copyright. All rights reserved.
    No preview · Article · May 2014 · The Plant Journal
Show more