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The Pentatricopeptide Repeat Protein MTSF2 Stabilizes a Nad1 Precursor

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The Pentatricopeptide Repeat Protein MTSF2 Stabilizes a Nad1 Precursor The pentatricopeptide repeat protein MTSF2 stabilizes a nad1 precursor transcript and defines the 3 end of its 5-half intron Chuande Wang, Fabien Aubé, Noelya Planchard, Martine Quadrado, Céline Dargel-Graffin, Fabien Nogué, Hakim Mireau To cite this version: Chuande Wang, Fabien Aubé, Noelya Planchard, Martine Quadrado, Céline Dargel-Graffin, et al.. The pentatricopeptide repeat protein MTSF2 stabilizes a nad1 precursor transcript and defines the 3 end of its 5-half intron. Nucleic Acids Research, Oxford University Press, 2017, 45 (10), pp.6119-6134. 10.1093/nar/gkx162. hal-01602528 HAL Id: hal-01602528 https://hal.archives-ouvertes.fr/hal-01602528 Submitted on 26 May 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution - NonCommercial| 4.0 International License Published online 8 March 2017 Nucleic Acids Research, 2017, Vol. 45, No. 10 6119–6134 doi: 10.1093/nar/gkx162 The pentatricopeptide repeat protein MTSF2 stabilizes a nad1 precursor transcript and defines the 3 end of its 5-half intron Chuande Wang1,2,†, Fabien Aube´ 1,†, Noelya Planchard1,2,†, Martine Quadrado1, Celine´ Dargel-Graffin1, Fabien Nogue´ 1 and Hakim Mireau1,* 1Institut Jean-Pierre Bourgin, INRA, AgroParisTech, CNRS, Universite´ Paris-Saclay, RD10, 78026 Versailles Cedex, France and 2Paris-Sud University, Universite´ Paris-Saclay, 91405 Orsay Cedex, France Received January 11, 2017; Revised February 22, 2017; Editorial Decision February 24, 2017; Accepted February 28, 2017 ABSTRACT ancient bacteria and contain their own genome that is sep- arate from the nuclear chromatin (1,2). Modern mitochon- RNA expression in plant mitochondria implies a large dria encode around 50 genes in most eukaryotes. Despite number of post-transcriptional events in which tran- this conserved and limited coding capacity, the structure script processing and stabilization are essential. In of mitochondrial genomes is highly variable among organ- this study, we analyzed the function of the Arabidop- isms, going from very small and compact genomes in an- sis mitochondrial stability factor 2 gene (MTSF2)and imals to huge and likely multi-circular structures in higher show that the encoded pentatricopeptide repeat pro- plants (3). The size increase of plant mitochondrial genomes tein is essential for the accumulation of stable nad1 results mostly from the presence of extended intergenic re- mRNA. The production of mature nad1 requires the gions that are rich in repeated sequences (4,5). The high assembly of three independent RNA precursors via recombinogenic activity of plant mitochondrial DNA re- two trans-splicing reactions. Genetic analyses re- sults in genomic organizations involving complex arrays of inter-convertible linear and circular DNA molecules. Sub- vealed that the lack of nad1 in mtsf2 mutants results sequently, mitochondrial gene order is poorly conserved from the specific destabilization of the nad1 exons 2– among plant species and examples of gene fragmentations 3 precursor transcript. We further demonstrated that are frequent (5–10). In response, complex RNA expres- MTSF2 binds to its 3 extremity with high affinity, sug- sion processes involving a considerable number of post- gesting a protective action by blocking exoribonucle- transcriptional events have evolved to maintain proper ex- ase progression. By defining the 3 end of nad1 exons pression of mitochondrial genes and generate mature mR- 2–3 precursor, MTSF2 concomitantly determines the NAs. These steps include over 400 C-to-U RNA editing 3 extremity of the first half of the trans-intron found events, cis and trans-intron splicing, 5 and 3 RNA process- at the end of the transcript. Therefore, binding of the ing as well as mRNA stabilization. The underlying mech- MTSF2 protein to nad1 exons 2–3 precursor evolved anisms are still poorly understood at the molecular level both to stabilize the transcript and to define a 3 ex- and the vast majority of the involved protein factors have not been identified. However, in the last years, the pentatri- tremity compatible with the trans-splicing reaction copeptide repeat (PPR) protein family has shown to figure needed to reconstitute mature nad1. We thus reveal prominently in these processes (11,12). Nuclear genomes of that the range of transcripts stabilized by association higher plant encode over 450 PPR genes, and the vast ma- with protective protein on their 3 end concerns also jority encode proteins that are predicted to target mitochon- mitochondrial precursor transcripts. dria or chloroplasts (11,13). PPR proteins are almost exclu- sively composed of tandem repeats of a highly degenerate 35-amino-acid motifs (14). Length variants of PPR repeats INTRODUCTION have been detected however, with repeats that are longer Mitochondria are essential organelles that are the site of (L) or shorter (S) than the initially-recognized 35-amino- cellular respiration, and a variety of other important bio- acid (P) motif (11,15). PLS PPR proteins, which contain chemical processes such as heme biosynthesis, part of the ordered series of P, L and S motifs, have been almost ex- urea cycle and Fe–S cluster formation. They descent from clusively associated with RNA editing in both mitochon- *To whom correspondence should be addressed. Tel: +33 130 833 070; Fax: +33 130 833 319; Email: [email protected] †These authors contributed equally to the paper as first authors. Present address: Fabien Aube,´ Laboratoire de Biologie et Modelisation´ de la Cellule, Ecole Normale Superieure´ 69007 Lyon, France. C The Author(s) 2017. Published by Oxford University Press on behalf of Nucleic Acids Research. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact [email protected] 6120 Nucleic Acids Research, 2017, Vol. 45, No. 10 dria and chloroplasts (16,17). In contrast, PPR proteins ex- process was initially described to occur in plastids and was clusively composed of P-type repeats were shown to par- shown to apply for both 5 and 3 end formation in this or- ticipate in various aspects of organellar RNA expression ganelle, whereas it seems limited to 3 processing in mito- ranging from gene transcription to mRNA translation (for chondria (46–48). review see (12,18)). Recent crystal structures of PPR pro- Still, much remains to be understood regarding RNA teins showed that PPR repeats fold into a hairpin formed processing and stabilization in plant mitochondria. In par- by two antiparallel alpha helices whose repetition assem- ticular, the type and number of mitochondrial transcripts ble into a right-handed superhelical spiral (19–23). Indeed, that are processed and stabilized by helical repeat proteins PPR domains organize highly specific RNA binding in- like PPR sitting on their 3 end awaits clarification. In this terfaces and PPR–RNA co-crystallization studies revealed study, we analyzed the function of the mitochondria stabil- that the solenoid like structure formed by the succession of ity factor 2 (MTSF2) protein in Arabidopsis and demon- PPR repeats wraps around single-stranded RNA (24,25). strated that this mitochondria-targeted PPR protein is re- Evolutionary, biochemical and structural data support that quired for the 3 processing and stabilization of the nad1 combinations involving amino acid 5 and 35 in each repeat exons 2–3 precursor transcript. This pre-mRNA is one of are critical for RNA recognition and form contacts with the the three nad1 precursor transcripts that are unified by two RNA base to be bound (15,26–30). trans-splicing reactions to create the mature nad1 mito- The production of translation-competent mRNAs im- chondrial mRNA. Our analysis reveals that the protein- plies the correct processing of 5 and 3 extremities as based mechanism permitting the stabilization and the 3 end well as the stabilization of mature transcripts. The defini- processing is not limited to mature mitochondrial mRNA tion of mRNA ends appears to be particularly essential but concerns also precursor transcripts that are substrates in plant mitochondria where genes are transcribed from of trans-splicing reactions. multiple promoters and transcription termination is not tightly controlled (31–33). A global analysis of mitochon- drial mRNA ends in Arabidopsis thaliana revealed that MATERIALS AND METHODS most protein-coding transcripts exhibit multiple 5 extrem- Plant material ities whereas their 3 end is generally very well defined and unique (34). Moreover, the relative abundance of individ- The N654650 (mtsf2-1) Arabidopsis mutant line was ob- ual 5 ends identified for some transcripts can differ among tained from the European Arabidopsis Stock Centre (http: Arabidopsis natural accessions (35,36). Further analyses //arabidopsis.info/). mtsf2-1 mutant plants were genotyped have revealed that most
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