Intracompartmental and Intercompartmental Transcriptional Networks Coordinate the Expression of Genes for Organellar Functions  

Abstract

(X.W., G.H., K.F.X.M.)Genes for mitochondrial and chloroplast proteins are distributed between the nuclear and organellar genomes. Organelle biogenesis and metabolism, therefore, require appropriate coordination of gene expression in the different compartments to ensure efficient synthesis of essential multiprotein complexes of mixed genetic origin. Whereas organelle-to-nucleus signaling influences nuclear gene expression at the transcriptional level, organellar gene expression (OGE) is thought to be primarily regulated posttranscriptionally. Here, we show that intracompartmental and intercompartmental transcriptional networks coordinate the expression of genes for organellar functions. Nearly 1,300 ATH1 microarray-based transcriptional profiles of nuclear and organellar genes for mitochondrial and chloroplast proteins in the model plant Arabidopsis (Arabidopsis thaliana) were analyzed. The activity of genes involved in organellar energy production (OEP) or OGE in each of the organelles and in the nucleus is highly coordinated. Intracompartmental networks that link the OEP and OGE gene sets serve to synchronize the expression of nucleus-and organelle-encoded proteins. At a higher regulatory level, coexpression of organellar and nuclear OEP/OGE genes typically modulates chloroplast functions but affects mitochondria only when chloroplast functions are perturbed. Under conditions that induce energy shortage, the intercompartmental coregulation of photosynthesis genes can even override intracompartmental networks. We conclude that dynamic intracompartmental and intercompartmental transcriptional networks for OEP and OGE genes adjust the activity of organelles in response to the cellular energy state and environmental stresses, and we identify candidate cis-elements involved in the transcriptional coregulation of nuclear genes. Regarding the transcriptional regulation of chloroplast genes, novel tentative target genes of s factors are identified.

Mitochondrial and Chloroplast Stress Responses Are Modulated in Distinct Touch and Chemical Inhibition Phases

“…Accordingly, the promoter of AtOM66 was previously demonstrated to be directly bound by AtWRKY15 and AtWRKY40 (Van Aken et al, 2013). The presence of WRKY binding sites in stressresponsive genes encoding energy organelle proteins has been described previously Leister et al, 2011;Van Aken and Whelan, 2012). However, not all these genes exhibit touch-responsive expression patterns (e.g.…”

“…As mitochondria and chloroplasts are tightly involved in cellular metabolism, they are in a prime position to sense cellular dysfunction and are therefore thought to be one of the initial sites of stress recognition and can contribute to programmed cell death execution (Vanlerberghe, 2013). A significant body of evidence supports a crucial role for mitochondria and chloroplasts in perceiving and responding to biotic and abiotic stress conditions (Skirycz et al, 2010;Leister et al, 2011;Nomura et al, 2012;Zhang et al, 2014;Stael et al, 2015). This is further supported by several studies demonstrating that the transcriptomic response to mitochondrial or chloroplast dysfunction by chemical or genetic disruption appears to be part of broad biotic and abiotic stress responses (Schwarzländer et al, 2012;Van Aken and Whelan, 2012).…”

Widespread dual targeting of proteins in land plants: When, where, how and why

“…21,22 The replication and expression of these genomes are therefore coordinated during development. 23,24 It has also been observed that these genes that encode dual targeted mitochondrial and plastid proteins involved in genome maintenance and expression are physically clustered within the genome and thus more likely to be coinherited. 25 However a more widespread analysis of the clustering of nuclear genes encoding organelle proteins did not find statistical evidence for clustering of any genes encoding organelle proteins.…”

Analysis of Arabidopsisglucose insensitive growthMutants Reveals the Involvement of the Plastidial Copper Transporter PAA1 in Glucose-Induced Intracellular Signaling

“…Such mutants showed loss of intercompartmental communication, including aberrant control of the expression of nucleusencoded plastid genes at the transcriptional level (Nott et al, 2006;Koussevitzky et al, 2007;Pogson et al, 2008). Interestingly, the ABA signaling pathway is also implicated in retrograde signaling (Penfield et al, 2006;Shen et al, 2006;Koussevitzky et al, 2007;Kim et al, 2009;Priest et al, 2009;Jung and Chory, 2010;Leister et al, 2011). Indeed, Koussevitzky et al (2007) demonstrated that ABI4, an AP2-type transcription factor, serves as a point of convergence and regulates nuclear gene expression in retrograde signaling.…”