A Core Module of Nuclear Genes Regulated by Biogenic Retrograde Signals from Plastids

Abstract

Chloroplast biogenesis during seedling development of angiosperms is a rapid and highly dynamic process that parallels the light-dependent photomorphogenic programme. Pre-treatments of dark-grown seedlings with lincomyin or norflurazon prevent chloroplast biogenesis upon illumination yielding albino seedlings. A comparable phenotype was found for the Arabidopsis mutant plastid-encoded polymerase associated protein 7 (pap7) being defective in the prokaryotic-type plastid RNA polymerase. In all three cases the defect in plastid function has a severe impact on the expression of nuclear genes representing the influence of retrograde signaling pathway(s) from the plastid. We performed a meta-analysis of recently published genome-wide expression studies that investigated the impact of the aforementioned chemical and genetic blocking of chloroplast biogenesis on nuclear gene expression profiles. We identified a core module of 152 genes being affected in all three conditions. These genes were classified according to their function and analyzed with respect to their implication in retrograde signaling and chloroplast biogenesis. Our study uncovers novel genes regulated by retrograde biogenic signals and suggests the action of a common signaling pathway that is used by signals originating from plastid transcription, translation and oxidative stress.

Chloroplast development in green plant tissues: the interplay between light, hormone, and transcriptional regulation

“…Signalling from the chloroplast to control nuclear transcription is referred to as retrograde signalling and is controlled by factors such as light, chloroplast gene expression, chloroplast protein import, tetrapyrrole biosynthesis, redox‐state and reactive oxygen species (Yurina & Odintsova, 2019). Biogenic retrograde signalling refers to signals from plastids during early steps of chloroplast biogenesis, to ensure the process is completed safely, whereas operational retrograde signals derive from fully active chloroplasts and adjust operation of the organelle in response to environmental conditions (Pogson et al ., 2008; Grübler et al ., 2021). Several genes which belong to the pentatricopeptide repeat (PRR) family have been shown to impact on retrograde signalling by altering messenger RNA (mRNA) sequence, turnover, processing or translation (Barkan & Small, 2014).…”

Correlated retrograde and developmental regulons implicate multiple retrograde signals as coordinators of chloroplast development in maize

“…The transcriptome remodeling in the four mutants we analyzed presented in two primary patterns or syndromes. The “chlorotic” syndrome is displayed by the Zm- ptac12 and tha1 transcriptomes, whose similarity suggests that Zm-PTAC12 does not directly coordinate nuclear and chloroplast gene expression or mediate phytochrome signaling, as has been proposed for its Arabidopsis ortholog (Chen et al, 2010; Hernandez-Verdeja and Strand, 2018; Tadini et al, 2020; Grübler et al, 2021). The albino syndrome is displayed by the Zm- murE and ppr5 mutants.…”

“…Repression of genes in Cluster 1 (reduced expression in all four mutants) is suggested in the Arabidopsis data. Cluster 1 genes that respond similarly in maize and Arabidopsis include genes encoding the transcription factor GLK1 in Arabidopsis and its co-orthologs in maize, Golden2 and GLK1, which activate PhANGs (Rossini et al, 2001; Waters et al, 2009) and play a central role in retrograde regulation of PhANG expression in Arabidopsis (Leister and Kleine, 2016; Martin et al, 2016; Hernandez-Verdeja and Strand, 2018; Grübler et al, 2021). Our data show, however, that PhANGs and GLK1 are not co-regulated in response to plastid dysfunctions: PhANG expression is minimally affected in maize and Arabidopsis mutants that retain some plastid translation activity, but the expression of GLK1 co-orthologs is reduced in all of these mutants (Supplemental Dataset S5, Figure 3B).…”

“…Genes whose expression increases in response to disrupted chloroplast biogenesis have been reported previously (e.g. Biehl et al, 2005; Woodson et al, 2013; Kleine and Leister, 2016; Grübler et al, 2017; Wang et al, 2020; Grübler et al, 2021), but aside from NEP, whose expression is well known to increase when PEP is compromised (Tadini et al, 2020), they have received little attention with regard to their functions or mechanisms of up-regulation. Roughly half of the genes in our differentially-expressed set were expressed at higher levels in mutants than in the wild-type.…”

“…Supplemental Dataset S8. Arabidopsis Core Retrograde Modules (Glässer et al, 2014;Leister and Kleine, 2016;Grübler et al, 2021) Immunoblots were probed with an antibody that detects cytosolic ribosomal protein S6 (eS6) (upper panels), an antibody specific for its phosphorylated S240P isoform (middle panels) and an antibody specific for its phosphorylated S237P isoform. eS6-S240P is TOR-dependent in Arabidopsis and maize (Dobrenel et al, 2016) (Supplemental Figure S4), whereas eS6-S237P appears not to be (Supplemental Figure S4).…”