Evolutionary aspects of plastid proteins involved in transcription: The transcription of a tiny genome is mediated by a complicated machinery

Yagi, Yusuke; Shiina, Takashi

doi:10.4161/trns.21810

Cited by 12 publications

(7 citation statements)

References 28 publications

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“…PRIN2 is absent from the genomes of green algae and cyanobacteria, indicating that this protein appeared during evolution of the plant lineage and suggesting that it might perform a regulatory function 22 . Analysis of the PRIN2 protein sequences from different plant species showed that the protein lacked putative kinase or phosphatase domains, but revealed the presence of two conserved cysteine residues within the mature protein, Cys68, and Cys115 (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…The PEP-associated proteins are plant-specific proteins, suggesting that those proteins evolved relatively late compared with the eubacterial core subunits of the PEP complex. Proteins that evolved late in the plant lineage can be linked to regulatory functions coordinating different processes in the cell 22 and could potentially improve the redox regulatory system inherited from cyanobacteria 23 .…”

Section: Introductionmentioning

confidence: 99%

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Redox regulation of PEP activity during seedling establishment in Arabidopsis thaliana

et al. 2018

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Activation of the plastid-encoded RNA polymerase is tightly controlled and involves a network of phosphorylation and, as yet unidentified, thiol-mediated events. Here, we characterize PLASTID REDOX INSENSITIVE2, a redox-regulated protein required for full PEP-driven transcription. PRIN2 dimers can be reduced into the active monomeric form by thioredoxins through reduction of a disulfide bond. Exposure to light increases the ratio between the monomeric and dimeric forms of PRIN2. Complementation of prin2-2 with different PRIN2 protein variants demonstrates that the monomer is required for light-activated PEP-dependent transcription and that expression of the nuclear-encoded photosynthesis genes is linked to the activity of PEP. Activation of PEP during chloroplast development likely is the source of a retrograde signal that promotes nuclear LHCB expression. Thus, regulation of PRIN2 is the thiol-mediated mechanism required for full PEP activity, with PRIN2 monomerization via reduction by TRXs providing a mechanistic link between photosynthetic electron transport and activation of photosynthetic gene expression.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Redox regulation of PEP activity during seedling establishment in Arabidopsis thaliana

et al. 2018

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“…Chloroplasts have recruited significant number of eukaryotic proteins from host cells. Thus, chloroplasts possess unique prokaryotic-eukaryotic hybrid systems in several cellular processes, including transcription (Baumgartner et al, 1993 ; Yagi and Shiina, 2011 ), translation and metabolic pathways (Martin and Schnarrenberger, 1997 ; Reyes-Prieto and Bhattacharya, 2007 ; Reyes-Prieto and Moustafa, 2012 ). In total, more than 600 non-cyanobacterial-host-derived proteins contribute to the chloroplast proteome, which includes ~3000 proteins (Abdallah et al, 2000 ).…”

Section: Discussionmentioning

confidence: 99%

Evidence for lateral gene transfer (LGT) in the evolution of eubacteria-derived small GTPases in plant organelles

et al. 2014

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The genomes of free-living bacteria frequently exchange genes via lateral gene transfer (LGT), which has played a major role in bacterial evolution. LGT also played a significant role in the acquisition of genes from non-cyanobacterial bacteria to the lineage of “primary” algae and land plants. Small GTPases are widely distributed among prokaryotes and eukaryotes. In this study, we inferred the evolutionary history of organelle-targeted small GTPases in plants. Arabidopsis thaliana contains at least one ortholog in seven subfamilies of OBG-HflX-like and TrmE-Era-EngA-YihA-Septin-like GTPase superfamilies (together referred to as Era-like GTPases). Subcellular localization analysis of all Era-like GTPases in Arabidopsis revealed that all 30 eubacteria-related GTPases are localized to chloroplasts and/or mitochondria, whereas archaea-related DRG and NOG1 are localized to the cytoplasm and nucleus, respectively, suggesting that chloroplast- and mitochondrion-localized GTPases are derived from the ancestral cyanobacterium and α-proteobacterium, respectively, through endosymbiotic gene transfer (EGT). However, phylogenetic analyses revealed that plant organelle GTPase evolution is rather complex. Among the eubacterium-related GTPases, only four localized to chloroplasts (including one dual targeting GTPase) and two localized to mitochondria were derived from cyanobacteria and α-proteobacteria, respectively. Three other chloroplast-targeted GTPases were related to α-proteobacterial proteins, rather than to cyanobacterial GTPases. Furthermore, we found that four other GTPases showed neither cyanobacterial nor α-proteobacterial affiliation. Instead, these GTPases were closely related to clades from other eubacteria, such as Bacteroides (Era1, EngB-1, and EngB-2) and green non-sulfur bacteria (HflX). This study thus provides novel evidence that LGT significantly contributed to the evolution of organelle-targeted Era-like GTPases in plants.

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“…B). Silenced NtEMB2738 blocked chloroplast development in tobacco, and the expression pattern of plastid genes in the silenced tobacco showed a similar pattern to those in PEP‐deficient mutants, such as Δrpos (Hess et al , Allison et al , De Santis‐MacIossek et al , Krause et al , Legen et al ) and ptac mutants (Pfalz et al , , Garcia et al , Myouga et al , Arsova et al , Gao et al , Yagi et al , Yu et al ). These results suggested that EMB2738 was probably involved in the expression of plastid gene in higher plants.…”

Section: Discussionmentioning

confidence: 85%

EMB2738, which encodes a putative plastid‐targeted GTP‐binding protein, is essential for embryogenesis and chloroplast development in higher plants

Zhang

Pan

et al. 2017

Physiologia Plantarum

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In higher plants, chloroplasts carry out many important functions, and normal chloroplast development is required for embryogenesis. Numerous chloroplast-targeted proteins involved in embryogenesis have been identified. Nevertheless, their functions remain unclear. In this study, a chloroplast-localized protein, EMB2738, was reported to be involved in Arabidopsis embryogenesis. EMB2738 knockout led to defective embryos, and the embryo development in emb2738 was interrupted after the globular stage. Complementation experiments identified the AT3G12080 locus as EMB2738. Cellular observation indicated that severely impaired chloroplast development was observed in these aborted embryos. Quantitative reverse transcription-polymerase chain reaction (qRT-PCR) analysis showed that chloroplast-encoded photosynthetic genes, which are transcribed by plastid-encoded RNA polymerase (PEP), are predominantly decreased in defective embryogenesis, compared with those in the wild-type. In contrast, genes encoding PEP core subunits, which are transcribed by nucleus-encoded RNA polymerase (NEP), were increased. These results suggested that the knockout of EMB2738 strongly blocked chloroplast-encoded photosynthesis gene expression in embryos. Silencing of the EMB2738 orthologue in tobacco through a virus-induced genome silencing technique resulted in an albinism phenotype, vacuolated chloroplasts and decreased PEP-dependent plastid transcription. These results suggested that NtEMB2738 might be involved in plastid gene expression. Nevertheless, genetic analysis showed that the NtEMB2738 coding sequence could not fully rescue the defective embryogenesis of the emb2738 mutant, which suggested functional divergence between NtEMB2738 and EMB2738 in embryogenesis. Taken together, these results indicated that both EMB2738 and NtEMB2738 are involved in the expression of plastid genes in higher plants, and there is a functional divergence between NtEMB2738 and EMB2738 in embryogenesis.

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Evolutionary aspects of plastid proteins involved in transcription: The transcription of a tiny genome is mediated by a complicated machinery

Cited by 12 publications

References 28 publications

Redox regulation of PEP activity during seedling establishment in Arabidopsis thaliana

Redox regulation of PEP activity during seedling establishment in Arabidopsis thaliana

Evidence for lateral gene transfer (LGT) in the evolution of eubacteria-derived small GTPases in plant organelles

EMB2738, which encodes a putative plastid‐targeted GTP‐binding protein, is essential for embryogenesis and chloroplast development in higher plants

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