Recruitment of a Ribosomal Release Factor for Light- and Stress-Dependent Regulation of <i>petB</i> Transcript Stability in <i>Arabidopsis</i> Chloroplasts

Stoppel, Rhea; Lezhneva, Lina; Schwenkert, Serena; Torabi, Salar; Felder, Susanne; Meierhoff, Karin; Westhoff, Peter; Meurer, Jörg

doi:10.1105/tpc.111.085324

Cited by 48 publications

(71 citation statements)

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“…CP43, PsbH, and PsaA antisera were obtained from Agrisera. Other antibodies used in this study were described elsewhere (Umate et al, 2008;Stoppel et al, 2011). Loading was estimated by staining with Coomassie Brilliant Blue prior to immunohybridization.…”

Section: Protein Analysismentioning

confidence: 99%

PsbN Is Required for Assembly of the Photosystem II Reaction Center in Nicotiana tabacum

et al. 2014

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ORCID ID: 0000-0003-2973-9514 (J.M.)The chloroplast-encoded low molecular weight protein PsbN is annotated as a photosystem II (PSII) subunit. To elucidate the localization and function of PsbN, encoded on the opposite strand to the psbB gene cluster, we raised antibodies and inserted a resistance cassette into PsbN in both directions. Both homoplastomic tobacco (Nicotiana tabacum) mutants ΔpsbN-F and ΔpsbN-R show essentially the same PSII deficiencies. The mutants are extremely light sensitive and failed to recover from photoinhibition. Although synthesis of PSII proteins was not altered significantly, both mutants accumulated only ;25% of PSII proteins compared with the wild type. Assembly of PSII precomplexes occurred at normal rates, but heterodimeric PSII reaction centers (RCs) and higher order PSII assemblies were not formed efficiently in the mutants. The ΔpsbN-R mutant was complemented by allotopic expression of the PsbN gene fused to the sequence of a chloroplast transit peptide in the nuclear genome. PsbN represents a bitopic trans-membrane peptide localized in stroma lamellae with its highly conserved C terminus exposed to the stroma. Significant amounts of PsbN were already present in dark-grown seedling. Our data prove that PsbN is not a constituent subunit of PSII but is required for repair from photoinhibition and efficient assembly of the PSII RC.

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Section: Protein Analysismentioning

confidence: 99%

PsbN Is Required for Assembly of the Photosystem II Reaction Center in Nicotiana tabacum

et al. 2014

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“…Homologs of only few factors for chloroplast RNA metabolism are also found in cyanobacteria. However, they significantly diversified by recruiting novel domains and/or extensions and changed their functions, as was found for CHLOROPLAST RNA SPLICING2 (Jenkins and Barkan, 2001), HCF109 (Meurer et al, 2002), CHLOROPLAST RNA SPLICING AND RIBOSOME MATURATION (Barkan et al, 2007), PrfB3 (Stoppel et al, 2011), and RNase E (Mudd et al, 2008;Schein et al, 2008;.…”

Section: Introductionmentioning

confidence: 99%

“…Little is known about factors that authentically regulate plastid mRNA stability and even less about how metabolic processes as well as endogenous and external stimuli are involved in this regulation. This regulation is, for instance, essential to cope with photosystem II (PSII) excitation pressure and plastidic redox stress induced by changes in temperature and light intensity (Stoppel et al, 2011;Kupsch et al, 2012). In summary, divergence of plastid UTRs and appearance of phylogenetically novel RNA processing sites provide new platforms at the RNA extremities for RNA binding factors to implement molecular processes in response to environmental stimuli, emphasizing the importance of RNA metabolism and translation in adjusting chloroplast homeostasis (Stern et al, 2010;Stoppel and Meurer, 2013).…”

Section: Introductionmentioning

confidence: 99%

“…In several cases, processing within intergenic regions is required for subsequent translation of the 59 processed product (Germain et al, 2013) and regulation of stability of individual mRNAs at both ends (Barkan, 2011;Zhelyazkova et al, 2012). The 39 processing has been hypothesized to be a prerequisite also for efficient translation of plastid transcripts (Stoppel et al, 2011). Degradation of plastid RNAs is often initiated by endonucleolytic processing and by the subsequent action of unspecific 59 → 39 and 39 → 59 exonucleases (Germain et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

“…Examples are PALE CRESS, ACCUMULATION OF PHOTOSYSTEM ONE1 (APO1) to APO4, PEPTIDE CHAIN RELEASE FACTOR B3 (PrfB3), RHO-N domain protein (RHON1), PLANT ORGANELLE RNA RECOGNITION domains, and many chloroplast PENTATRICOPEPTIDEREPEAT (PPR) proteins (Meurer et al, 1998;Kroeger et al, 2009;Stoppel et al, 2011Watkins et al, 2011;Shikanai and Fujii, 2013;Barkan and Small, 2014). Recruitment of novel factors for the management and regulation of the plastid and mitochondrial RNA metabolism was presumably driven by the acquisition of introns, massive endonucleolytic cleavage of precursor transcripts, numerous editing sites, and the fast divergence of noncoding sequences in the intergenic as well as the 59 and 39 UTRs in the genome of the endosymbiont (Barkan, 2011;Manavski et al, 2012a).…”

Section: Introductionmentioning

confidence: 99%

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HIGH CHLOROPHYLL FLUORESCENCE145 Binds to and Stabilizes the psaA 5′ UTR via a Newly Defined Repeat Motif in Embryophyta

et al. 2015

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ORCID IDs: 0000-0003-2740-5991 (N.M.); 0000-0003-2973-9514 (J.M.)The seedling-lethal Arabidopsis thaliana high chlorophyll fluorescence145 (hcf145) mutation leads to reduced stability of the plastid tricistronic psaA-psaB-rps14 mRNA and photosystem I (PSI) deficiency. Here, we genetically mapped the HCF145 gene, which encodes a plant-specific, chloroplast-localized, modular protein containing two homologous domains related to the polyketide cyclase family comprising 37 annotated Arabidopsis proteins of unknown function. Two further highly conserved and previously uncharacterized tandem repeat motifs at the C terminus, herein designated the transcript binding motif repeat (TMR) domains, confer sequence-specific RNA binding capability to HCF145. Homologous TMR motifs are often found as multiple repeats in quite diverse proteins of green and red algae and in the cyanobacterium Microcoleus sp PCC 7113 with unknown function. HCF145 represents the only TMR protein found in vascular plants. Detailed analysis of hcf145 mutants in Arabidopsis and Physcomitrella patens as well as in vivo and in vitro RNA binding assays indicate that HCF145 has been recruited in embryophyta for the stabilization of the psaA-psaB-rps14 mRNA via specific binding to its 59 untranslated region. The polyketide cyclase-related motifs support association of the TMRs to the psaA RNA, presumably pointing to a regulatory role in adjusting PSI levels according to the requirements of the plant cell.

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Chloroplast Gene Expression—RNA Synthesis and Processing

Börner¹,

Zhelyazkova²,

Legen³

et al. 2014

Plastid Biology

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Both transcription and transcript processing are more complex in chloroplasts than in bacteria. Plastid genes are transcribed by a plastid-encoded RNA polymerase (PEP) and one (monocots) or two (dicots) nuclear-encoded RNA polymerase(s) (NEP). PEP is a bacterial-type multisubunit enzyme composed of core subunits (coded for by the plastid rpoA, B, C1 and C2 genes) and additional protein factors encoded in the nuclear genome. The nuclear genome of Arabidopsis contains six genes for sigma factors required by PEP for promoter recognition. NEP activity is represented by phage-type RNA polymerases. Factors supporting NEP activity have not been identified yet. NEP and PEP use different promoters. Both types of RNA polymerase are active in proplastids and all stages of chloroplast development. PEP is the dominating transcriptase in chloroplasts.Chloroplast RNA processing consists of hundreds of mostly independent events. In recent years, much progress has been made in identifying factors behind RNA splicing and RNA editing. Namely, pentatricopeptide repeat (PPR) proteins have come into focus as RNA binding proteins conferring specificity to individual processing events. Also, studies on chloroplast RNases have helped considerably to understand chloroplast RNA turnover. Such mechanistic insights are set in contrast to how little we know about the regulatory role of RNA processing in chloroplasts.Keywords Chloroplast transcription · Chloroplast RNA polymerase · Chloroplast promoter · Chloroplast RNA processing · Chloroplast RNA-binding proteins · PPR proteins · Chloroplast splicing · Chloroplast editing · Chloroplast RNA degradation · Chloroplast nucleases Abbreviations CRS2 Chloroplast RNA splicing 2 protein IR Inverted repeat NEP Nuclear-encoded plastid RNA polymerase

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Recruitment of a Ribosomal Release Factor for Light- and Stress-Dependent Regulation of petB Transcript Stability in Arabidopsis Chloroplasts

Cited by 48 publications

References 71 publications

PsbN Is Required for Assembly of the Photosystem II Reaction Center in Nicotiana tabacum

PsbN Is Required for Assembly of the Photosystem II Reaction Center in Nicotiana tabacum

HIGH CHLOROPHYLL FLUORESCENCE145 Binds to and Stabilizes the psaA 5′ UTR via a Newly Defined Repeat Motif in Embryophyta

Chloroplast Gene Expression—RNA Synthesis and Processing

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