Definition of a core module for the nuclear retrograde response to altered organellar gene expression identifies GLK overexpressors as gun mutants

Abstract

Retrograde signaling can be triggered by changes in organellar gene expression (OGE) induced by inhibitors such as lincomycin (LIN) or mutations that perturb OGE. Thus, an insufficiency of the organelle-targeted prolyl-tRNA synthetase PRORS1 in Arabidopsis thaliana activates retrograde signaling and reduces the expression of nuclear genes for photosynthetic proteins.Recently, we showed that mTERF6, a member of the so-called mitochondrial transcription termination factor (mTERF) family, is involved in the formation of chloroplast (cp) isoleucine-tRNA. To obtain further insights into its functions, co-expression analysis of MTERF6, PRORS1 and two other genes for organellar aminoacyl-tRNA synthetases was conducted. The results suggest a prominent role of mTERF6 in aminoacylation activity, light signaling and seed storage. Analysis of changes in whole-genome transcriptomes in the mterf6-1 mutant showed that levels of nuclear transcripts for cp OGE proteins were particularly affected. Comparison of the mterf6-1 transcriptome with that of prors1-2 showed that reduced aminoacylation of proline (prors1-2) and isoleucine (mterf6-1) tRNAs alters retrograde signaling in similar ways. Database analyses indicate that comparable gene expression changes are provoked by treatment with LIN, norflurazon or high light. A core OGE response module was defined by identifying genes that were differentially expressed under at least four of six conditions relevant to OGE signaling. Based on this module, overexpressors of the Golden2-like transcription factors GLK1 and GLK2 were identified as genomes uncoupled mutants.

Ubiquitin-Proteasome Dependent Regulation of the GOLDEN2-LIKE 1 Transcription Factor in Response to Plastid Signals

“…overexpressing line (Leister and Kleine, 2016), the expression of LHCB1 in these lines (Fig. 5C) were comparable to that in wild-type (line 1) or even higher than that in wild type (line 2).…”

The Characterization of Arabidopsis mterf6 Mutants Reveals a New Role for mTERF6 in Tolerance to Abiotic Stress

“…As a result, this would alter nuclear gene expression, and hence, tolerance to these environmental conditions. Similarly, Leister and Kleine [21] found that levels of the nuclear transcripts, which encode the chloroplast proteins involved in organellar gene expression (OGE), were affected in the weak mterf6-1 mutant. Notwithstanding, while some mTERF proteins (e.g., mTERF5, mTERF9 and mTERF10) would negatively modulate Arabidopsis salt tolerance as their down-regulation diminishes sensitivity to ABA and abiotic stresses, mTERF6 would play the opposite role by promoting such tolerance, at least during germination and seedling establishment.…”

“…Accordingly, Arabidopsis mTERF15 [15] and maize Zm-mTERF4 [16] are involved in intron splicing in mitochondria, Arabidopsis BELAYA SMERT/RUGOSA2 [17,18] is required for intron splicing in plastids, and Chlamydomonas reindhardtii MOC1 promotes the termination of antisense mitochondrial transcription [19]. The Arabidopsis mTERF6 protein, dually targeted to chloroplasts and mitochondria, is involved in the maturation of the chloroplast isoleucine tRNA ( trnI.2 ) gene and the aminoacylation of tRNA for isoleucine [20,21]. …”

Transcriptional Regulation of Tetrapyrrole Biosynthesis in Arabidopsis thaliana

“…Genetic evidence suggests that GUN1 signaling activates ABI4 to downregulate PhANGs in response to chloroplast dysfunction (Koussevitzky et al, 2007), although the significance of ABI4 in this process is controversial (Acevedo-Hernandez et al, 2005; Kakizaki et al, 2009; Kerchev et al, 2011). In addition, GLK1 and GLK2 are under transcriptional control by plastid signaling (Waters et al, 2009; Leister and Kleine, 2016). Furthermore, overexpressors of GLK1 and GLK2 showed a gun phenotype after norflurazon or lincomycin treatment (Leister and Kleine, 2016).…”

“…In addition, GLK1 and GLK2 are under transcriptional control by plastid signaling (Waters et al, 2009; Leister and Kleine, 2016). Furthermore, overexpressors of GLK1 and GLK2 showed a gun phenotype after norflurazon or lincomycin treatment (Leister and Kleine, 2016). GUN1 somehow downregulates GLK1 expression in response to chloroplast dysfunction, which results in the downregulation of GLK targets including key TPB genes independent of ABI4 signaling (Kakizaki et al, 2009; Waters et al, 2009).…”