Function of plastid sigma factors in higher plants: regulation of gene expression or just preservation of constitutive transcription?

Lerbs-Mache, Silva

doi:10.1007/s11103-010-9714-4

Cited by 119 publications

(95 citation statements)

References 104 publications

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“…Genes for PEP core subunits, α, β, β′, and β′′ were retained in plastid genomes as rpoA, rpoB, rpoC1, and rpoC2 during plant evolution, but genes for σ-factors involved in transcription initiation, have been transferred to the nuclear genome (5), which allows the nucleus to control PEP transcription initiation in response to developmental and environmental cues (recently reviewed in ref. 6). PEP is responsible for transcription of photosynthesis genes in chloroplast in response to light.…”

mentioning

confidence: 99%

Eukaryotic-type plastid nucleoid protein pTAC3 is essential for transcription by the bacterial-type plastid RNA polymerase

Yagi

Ishizaki

Nakahira

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

103

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Plastid transcription is mediated by two distinct types of RNA polymerases (RNAPs), bacterial-type RNAP (PEP) and phage-type RNAP (NEP). Recent genomic and proteomic studies revealed that higher plants have lost most prokaryotic transcription regulators and have acquired eukaryotic-type proteins during plant evolution. However, in vivo dynamics of chloroplast RNA polymerases and eukaryotic-type plastid nucleoid proteins have not been directly characterized experimentally. Here, we examine the association of the α-subunit of PEP and eukaryotic-type protein, plastid transcriptionally active chromosome 3 (pTAC3) with transcribed regions in vivo by using chloroplast chromatin immunoprecipitation (cpChIP) assays. PEP α-subunit preferentially associates with PEP promoters of photosynthesis and rRNA genes, but not with NEP promoter regions, suggesting selective and accurate recognition of PEP promoters by PEP. The cpChIP assays further demonstrate that the peak of PEP association occurs at the promoterproximal region and declines gradually along the transcribed region. pTAC3 is a putative DNA-binding protein that is localized to chloroplast nucleoids and is essential for PEP-dependent transcription. Density gradient and immunoprecipitation analyses of PEP revealed that pTAC3 is associated with the PEP complex. Interestingly, pTAC3 associates with the PEP complex not only during transcription initiation, but also during elongation and termination. These results suggest that pTAC3 is an essential component of the chloroplast PEP complex. In addition, we demonstrate that light-dependent chloroplast transcription is mediated by light-induced association of the PEP-pTAC3 complex with promoters. This study illustrates unique dynamics of PEP and its associated protein pTAC3 during light-dependent transcription in chloroplasts.

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mentioning

confidence: 99%

Eukaryotic-type plastid nucleoid protein pTAC3 is essential for transcription by the bacterial-type plastid RNA polymerase

Yagi

Ishizaki

Nakahira

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

103

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“…For instance, chloroplast genes encoding subunits of the ATP synthase (atpB [ATCG00480] and atpE [ATCG00470]) or the cytochrome b 6 /f complex (petB [ATCG00720]) were coregulated with nuclear genes encoding diverse Rubisco small chain subunits (AT1G67090, AT5G38410, AT5G38420, and AT5G38430), Rubisco activase (RCA [AT2G39730]), and several proteins of the lightharvesting complexes of PSI and PSII (Supplemental Table S5H). In higher plants, chloroplast transcription is performed by three different plastid RNA polymerases: a multimeric plastid-encoded plastid (PEP) and two monomeric nucleus-encoded plastid (NEP) RNA polymerases (Lerbs-Mache, 2011;Liere et al, 2011). In principle, most plastid genes can be transcribed by both types of RNA polymerases.…”

Section: Coregulation Between Different Genetic Compartments At the Gmentioning

confidence: 99%

“…Considerable advances have been made in elucidating the role of s factors for specific promoter recognition and selected transcription of some plastid genes (Lerbs-Mache, 2011). However, the unambiguous identification of target genes was hindered for two reasons.…”

Section: Identification Of Tentative Chloroplast Target Genes Of S Famentioning

confidence: 99%

“…(1) One s factor can have both specialized roles (at certain promoters and certain times/tissues) and overlapping redundant functions (at other promoters, times, and situations; Schweer et al, 2010). (2) The promoter of one plastid gene can be the target of multiple s factors (Schweer et al, 2010;Lerbs-Mache, 2011). Our coregulation analysis of chloroplast genes (Supplemental Fig.…”

Section: Identification Of Tentative Chloroplast Target Genes Of S Famentioning

confidence: 99%

“…Moreover, cluster analyses of chloroplast genes conducted on transcriptomes from mutants with severe photosynthetic defects or from plants exposed to stresses suggested that the accumulation of plastid gene transcripts is regulated in response to altered states of the chloroplast (Cho et al, 2009). The importance of transcriptional control in the chloroplast is underpinned by work with s (SIG) factors, which are nucleus encoded and required as chloroplast RNA polymerase transcription factors for chloroplast genes (Schweer et al, 2010;Lerbs-Mache, 2011). Accordingly, the loss of SIG2 and SIG6 delays chloroplast biogenesis (Hanaoka et al, 2003;Ishizaki et al, 2005;Loschelder et al, 2006).…”

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

et al. 2011

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(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.

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Plant Sigma Factors

Cuitun‐Coronado¹,

Dodd²

2020

Encyclopedia of Life Sciences

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Photosynthesis within chloroplasts is crucial for ecosystem function and all agricultural productivity. Chloroplasts are a type of plastid and contain a small circular genome of prokaryotic origin. This genome encodes proteins crucial for chloroplast function and requires correct regulation of gene expression. One cellular mechanism regulating plastid gene transcription involves sigma factors, which in plants are nuclear‐encoded proteins forming part of the chloroplast transcriptional system. These are required for chloroplast gene promoter recognition and transcription initiation, with specific sigma factors thought to recognise specific chloroplast promoters. Plant sigma factors participate in the adjustment of chloroplast transcription in response to environmental fluctuations and during development. They appear to be ancient, originating from photosynthetic bacteria that were chloroplast ancestors, with an increase in sigma factor copy number during plant evolution providing an example of the evolution of cell signalling. We examine the origins, structure, function and environmental signalling by plant sigma factors. Key Concepts Chloroplasts contain a small circular genome that encodes essential components of the photosynthetic apparatus and machinery for plastid transcription/translation. Some higher plant sigma factors participate in the integration of environmental signals that regulate chloroplast gene transcription. Sigma factors are found in bacteria to higher plants. In plants, they are important regulators of chloroplast transcription. Higher plant sigma factors allow the nuclear control of chloroplast transcription, forming a signalling pathway from the nucleus to chloroplasts. Higher plant sigma factors are thought to have evolved from sigma factors of photosynthetic bacteria that were engulfed by eukaryotic cells during the evolution of chloroplasts. During plant evolution, they transferred to the nuclear genome.

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Function of plastid sigma factors in higher plants: regulation of gene expression or just preservation of constitutive transcription?

Cited by 119 publications

References 104 publications

Eukaryotic-type plastid nucleoid protein pTAC3 is essential for transcription by the bacterial-type plastid RNA polymerase

Eukaryotic-type plastid nucleoid protein pTAC3 is essential for transcription by the bacterial-type plastid RNA polymerase

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

Plant Sigma Factors

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