Coordination of gene expression between organellar and nuclear genomes

Abstract

Following the acquisition of chloroplasts and mitochondria by eukaryotic cells during endosymbiotic evolution, most of the genes in these organelles were either lost or transferred to the nucleus. Encoding organelle-destined proteins in the nucleus allows for host control of the organelle. In return, organelles send signals to the nucleus to coordinate nuclear and organellar activities. In photosynthetic eukaryotes, additional interactions exist between mitochondria and chloroplasts. Here we review recent advances in elucidating the intracellular signalling pathways that coordinate gene expression between organelles and the nucleus, with a focus on photosynthetic plants.

Figure 1. An overview of genome co-ordination between the nucleus and intracellular organelles

The diagram depicts communication between the nucleus, chloroplast and mitochondrion. Details of anterograde signalling and retrograde signalling between the nucleus and the organelles, and of chloroplast–mitochondrion cross-talk are discussed in the main text. Environmental signals such as stress, oxygen or nutrient availability, light intensity or quality, developmental cues, and hormones affect the expression of nuclear genes that encode organellar proteins. This process will, in turn, affect organelle function and gene expression through anterograde mechanisms. Chloroplasts and mitochondria are also able to sense certain environmental conditions and stimuli that can affect their functional activities, for example, light intensity or quality (chloroplasts) and O₂ availability (mitochondria). Using retrograde signals, organelles communicate these received stimuli and their functional status to the nucleus, which leads to nuclear gene regulation.

Figure 2. Nuclear anterograde control of organelle gene expression

A generalized model of the coordination of organelle gene expression through nuclear anterograde control in eukaryotes. Several processes are highlighted. a | In flowering plants, restorers of fertility (Rf) proteins reverse the cytoplasmic male sterility (CMS) phenotype by reducing the expression of the aberrant mitochondrial gene using post-transcriptional mechanisms, b | Post-translational control of mitochondrial gene expression using nuclear-encoded proteases and assembly proteins, c | Post-transcriptional control of chloroplast gene expression using nuclear-encoded regulators of organelle gene expression (ROGE) proteins that target specific RNA transcripts, d | Control by epistasy of synthesis (CES) is an autoregulatory process in which unassembled organelle proteins repress their own translation. The autoregulation of the petA gene encoding the cytochrome f subunit (Cyt f) of the cytochrome b₆f complex in Chlamydomonas reinhardtii is used as an example of the CES process. In scenario 1, unassembled Cyt f binds the ROGE protein translation factor TCA1, and translation of the petA mRNA is inhibited. In scenario 2, the presence of cognate protein subunits cytochrome b₆ (Cyt b₆) and cytochrome subunit IV (SUIV) assemble with Cyt f. TCA1 is now able to bind petA mRNA and activate its translation. A discussion of which proteins are organelle encoded can be found in BOX 1. A more complete model of retrograde signalling than that highlighted in panel a can be viewed in FIG. 3. Proteins and protein complexes are designated as ovals. PPR pentatricopeptide repeat; TPR, tetratricopeptide repeat.

Figure 3. Retrograde signalling pathways and chloroplast-mitochondrion cross-talk in higher plant cells

This figure depicts chloroplast-to-nucleus and mitochondrion-to-nucleus retrograde signalling pathways in the higher plant cell (and in yeast and animals where noted). Seven different pathways are highlighted, a | The use of chloroplast-generated reactive oxygen species (ROS) to induce nuclear gene transcription, b | Control of nuclear gene regulation by the redox state of the photosynthetic electron transport chain (PET), c | Chloroplast Mg–protoporphyrin IX (Mg–proto) accumulation, d | Inhibition of plastid gene expression (PGE). c and d lead to the repression of nuclear-encoded chloroplast protein genes. Signals from inhibited mitochondrial gene expression act synergistically with the PGE pathway. Two putative Mg–proto signalling pathways are depicted: in pathway 1, GENOMES UNCOUPLED 1 (GUN1) or a putative GUN1-dependent chloroplast protein (GDCP) facilitate the export of Mg–proto from the chloroplast where it interacts with cytoplasmic signalling factors; in pathway 2, GUN1 or GDCP sense Mg–proto accumulation and other retrograde signals within the chloroplast and send an unidentified signal to the nucleus to control transcription of chloroplast protein-encoding genes, e | Mitochondrial electron transport chain (mtETC) dysfunction leads to transcriptional changes in the nucleus in several phyla, f | An aberrant mitochondrial protein leads to cytoplasmic male sterility (CMS) by affecting nuclear gene expression, g | Mitochondrial haem synthesis as a cellular sensor for O₂ availability in yeast. Proteins that are known to be involved in these pathways are designated as ovals. ABI4, abscisic acid insensitive 4; AOX, gene encoding the mitochondrial alternative oxidase; HAP1, haem activation protein; LHCB, gene encoding photosystem II chlorophyll a/b-binding protein; PQ, plastoquinone; PSI, photosystem I; ROX1, repressor of hypoxic genes; STN7, a thylakoid protein kinase.