RAP, the Sole Octotricopeptide Repeat Protein in <i>Arabidopsis</i>, Is Required for Chloroplast <i>16S</i> rRNA Maturation

Kleinknecht, Laura; Wang, Fei; Stübe, Roland; Philippar, Katrin; Nickelsen, Jörg; Bohne, Alexandra‐Viola

doi:10.1105/tpc.114.122853

Cited by 68 publications

(76 citation statements)

References 58 publications

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“…Fully consistent with the results reported here, depletion of FASTKD2 by RNAi was just found in to cause misassembly of the mitochondrial ribosome and impaired mitochondrial protein synthesis in human immortalized fibroblasts (Antonicka and Shoubridge 2015). Our observations for FASTKD2 also complement a recent report implicating RAP, a protein of Arabidopsis thaliana that shares the RAP domain with FASTKD2, in precursor processing of the small ribosomal subunit RNA in chloroplasts (Kleinknecht et al 2014). Despite this surprising similarity, our data suggest that FASTKD2 may function somewhat differently, as we did not observe the accumulation of ribosomal precursor transcripts upon depletion of FASTKD2.…”

Section: Depletion Of Fastkd2 Affects the Levels Of Several Of Its Tasupporting

confidence: 81%

FASTKD2 is an RNA-binding protein required for mitochondrial RNA processing and translation

Popow

Alleaume

Curk

et al. 2015

RNA

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Mitochondrial RNA processing is an essential step for the synthesis of the components of the electron transport chain in all eukaryotic organisms, yet several aspects of mitochondrial RNA biogenesis and regulation are not sufficiently understood. RNA interactome capture identified several disease-relevant RNA-binding proteins (RBPs) with noncanonical RNAbinding architectures, including all six members of the FASTK (FAS-activated serine/threonine kinase) family of proteins. A mutation within one of these newly assigned FASTK RBPs, FASTKD2, causes a rare form of Mendelian mitochondrial encephalomyopathy. To investigate whether RNA binding of FASTKD2 contributes to the disease phenotype, we identified the RNA targets of FASTKD2 by iCLIP. FASTKD2 interacts with a defined set of mitochondrial transcripts including 16S ribosomal RNA (RNR2) and NADH dehydrogenase subunit 6 (ND6) messenger RNA. CRISPR-mediated deletion of FASTKD2 leads to aberrant processing and expression of RNR2 and ND6 mRNA that encodes a subunit of the respiratory complex I. Metabolic phenotyping of FASTKD2-deficient cells reveals impaired cellular respiration with reduced activities of all respiratory complexes. This work identifies key aspects of the molecular network of a previously uncharacterized, disease-relevant RNAbinding protein, FASTKD2, by a combination of genomic, molecular, and metabolic analyses.

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Section: Depletion Of Fastkd2 Affects the Levels Of Several Of Its Tasupporting

confidence: 81%

FASTKD2 is an RNA-binding protein required for mitochondrial RNA processing and translation

Popow

Alleaume

Curk

et al. 2015

RNA

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“…Structural and biochemical analyses suggest that these newly identified helical repeat proteins, termed octotricopeptide repeat (OPR) proteins, like PPR proteins, are postulated to form a-helical RNA-binding domains (RAP domains) responsible for RNA stabilization/processing and translation (Eberhard et al, 2011;Rahire et al, 2012). Interestingly, in contrast to the large numbers of PPR proteins, only a single OPR gene exists in most of the higher plants (Kleinknecht et al, 2014). RAP encodes the sole OPR protein in Arabidopsis (Arabidopsis thaliana).…”

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confidence: 99%

“…RAP encodes the sole OPR protein in Arabidopsis (Arabidopsis thaliana). Depletion of RAP caused a severe defect in the processing of chloroplast 16S ribosomal RNA (rRNA), eventually leading to impaired chloroplast translation and photosynthesis (Kleinknecht et al, 2014). However, further investigation of the molecular mechanism of OPR protein in regulating chloroplast development is still needed.…”

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confidence: 99%

“…Recently, a novel class of helical repeat proteins was identified that also participate in chloroplast development (Eberhard et al, 2011;Rahire et al, 2012;Kleinknecht et al, 2014). Structural and biochemical analyses suggest that these newly identified helical repeat proteins, termed octotricopeptide repeat (OPR) proteins, like PPR proteins, are postulated to form a-helical RNA-binding domains (RAP domains) responsible for RNA stabilization/processing and translation (Eberhard et al, 2011;Rahire et al, 2012).…”

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confidence: 99%

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Albino Leaf 1 that Encodes the Sole Octotricopeptide Repeat Protein Is Responsible for Chloroplast Development in Rice

et al. 2016

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Chloroplast, the photosynthetic organelle in plants, plays a crucial role in plant development and growth through manipulating the capacity of photosynthesis. However, the regulatory mechanism of chloroplast development still remains elusive. Here, we characterized a mutant with defective chloroplasts in rice (Oryza sativa), termed albino leaf1 (al1), which exhibits a distinct albino phenotype in leaves, eventually leading to al1 seedling lethality. Electronic microscopy observation demonstrated that the number of thylakoids was reduced and the structure of thylakoids was disrupted in the al1 mutant during rice development, which eventually led to the breakdown of chloroplast. Molecular cloning revealed that AL1 encodes the sole octotricopeptide repeat protein (RAP) in rice. Genetic complementation of Arabidopsis (Arabidopsis thaliana) rap mutants indicated that the AL1 protein is a functional RAP. Further analysis illustrated that three transcript variants were present in the AL1 gene, and the altered splices occurred at the 39 untranslated region of the AL1 transcript. In addition, our results also indicate that disruption of the AL1 gene results in an altered expression of chloroplast-associated genes. Consistently, proteomic analysis demonstrated that the abundance of photosynthesis-associated proteins is altered significantly, as is that of a group of metabolism-associated proteins. More specifically, we found that the loss of AL1 resulted in altered abundances of ribosomal proteins, suggesting that RAP likely also regulates the homeostasis of ribosomal proteins in rice in addition to the ribosomal RNA. Taken together, we propose that AL1, particularly the AL1a and AL1c isoforms, plays an essential role in chloroplast development in rice.

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“…This includes the psaA mRNA splicing factors Raa1, Rat2, and Raa8 (18,21,31,32). In most land plants, the genomes encode only a single OPR gene (33). However, interestingly, they exhibit tetratricopeptide repeat, pentatricopeptide repeat, and mTERF proteins, which also belong to the helical repeat superfamily and are involved in RNA processing (16,34,35), thereby demonstrating that despite the independent origin of group II introns in green algae and land plants, a co-evolution of helical repeat superfamily proteins as splicing factors has occurred.…”

Section: Discussionmentioning

confidence: 99%

A Ribonucleoprotein Supercomplex Involved in trans-Splicing of Organelle Group II Introns

Reifschneider¹,

Marx²,

Jacobs³

et al. 2016

Journal of Biological Chemistry

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In the chloroplast of the green alga Chlamydomonas reinhardtii, two discontinuous group II introns, psaA-i1 and psaAi2, splice in trans, and thus their excision process resembles the nuclear spliceosomal splicing pathway. Here, we address the question whether fragmentation of trans-acting RNAs is accompanied by the formation of a chloroplast spliceosome-like machinery. Using a combination of liquid chromatographymass spectrometry (LC-MS), size exclusion chromatography, and quantitative RT-PCR, we provide the first characterization of a high molecular weight ribonucleoprotein apparatus participating in psaA mRNA splicing. This supercomplex contains two subcomplexes (I and II) that are responsible for trans-splicing of either psaA-i1 or psaA-i2. We further demonstrate that both subcomplexes are associated with intron RNA, which is a prerequisite for the correct assembly of subcomplex I. This study contributes further to our view of how the eukaryotic nuclear spliceosome evolved after bacterial endosymbiosis through fragmentation of self-splicing group II introns into a dynamic, protein-rich RNP machinery.The spliceosome is a dynamic RNP machinery that participates in the excision of mRNA introns in eukaryotes. This machinery consists of five small nuclear RNAs (snRNAs; U1, U2, U4, U5, and U6) and a large number of spliceosomal proteins (1, 2). It is generally accepted that spliceosomal snRNAs were derived from ancient group II introns, which were introduced into the eukaryotic cell after endosymbiosis (3, 4). Group II introns occur frequently in bacteria and organelles of fungi, algae, and higher plants but are rare in archaea and absent from nuclear genomes. Comparable with spliceosomal introns, the splicing reaction includes two transesterification reactions, yielding spliced exons and an excised intron lariat RNA.Despite the lack of significant sequence similarities, group II introns share a common secondary structure with six helical domains (D1-D6) surrounding a central wheel. During intron excision, these domains take over specific functions, and remarkably, they show plenty of functional and structural similarities to spliceosomal snRNAs (5-7). These similarities led to the assumption that during evolution of the nuclear splicing apparatus, group II introns fragmented and degenerated to spliceosomal snRNAs (3,8,9).In contrast to bacterial group II introns, most organelle group II introns display variant forms of degeneration and fragmentation (9). For example, many of the plant group II introns have mispaired domain structures (10, 11). Moreover, group II introns are able to split into autonomous fragments due to rearrangements of organelle genomes (12, 13). Consequently, they are transcribed independently, and association of precursor RNAs by base pairing generates a catalytically active group II intron structure that is finally processed by trans-splicing. Such degenerated and fragmented group II introns along with the interplay of discrete RNAs during the splicing reaction serve to demonstrate how snRNAs...

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RAP, the Sole Octotricopeptide Repeat Protein in Arabidopsis, Is Required for Chloroplast 16S rRNA Maturation

Cited by 68 publications

References 58 publications

FASTKD2 is an RNA-binding protein required for mitochondrial RNA processing and translation

FASTKD2 is an RNA-binding protein required for mitochondrial RNA processing and translation

Albino Leaf 1 that Encodes the Sole Octotricopeptide Repeat Protein Is Responsible for Chloroplast Development in Rice

A Ribonucleoprotein Supercomplex Involved in trans-Splicing of Organelle Group II Introns

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