scholarly journals nMAT3 is an essential maturase splicing factor required for holo-complex I biogenesis and embryo-development in Arabidopsis thaliana plants

2020 ◽  
Author(s):  
Sofia Shevtsov-Tal ◽  
Corinne Best ◽  
Roei Matan ◽  
Sam Aldrin Chandran ◽  
Gregory G. Brown ◽  
...  
Keyword(s):  
Complex I ◽  
Rna Binding ◽  
Embryo Rescue ◽  
Group Ii Introns ◽  
Pentatricopeptide Repeat ◽  
Terrestrial Plants ◽  
Rna Helicases ◽  
Coding Regions ◽  
Group Ii ◽  
Mitochondrial Introns

SummaryGroup II introns are large catalytic RNAs that are particularly prevalent in the organelles of terrestrial plants. In angiosperm mitochondria, group II introns reside in the coding-regions of many critical genes, and their excision is essential for respiratory-mediated functions. Canonical group II introns are self-splicing and mobile genetic elements, consisting of the catalytic intron-RNA and its cognate intron-encoded endonuclease factor (i.e. maturase, Pfam-PF01348). Plant organellar introns are extremely degenerate, and lack many regions that are critical for splicing, including their related maturase-ORFs. The high degeneracy of plant mitochondrial introns was accompanied during evolution by the acquisition of ‘host-acting’ protein cofactors. These include several nuclear encoded maturases (nMATs) and various other splicing-cofactors that belong to a diverse set of RNA-binding families, e.g. RNA helicases (Pfam-PF00910), Mitochondrial Transcription Termination Factors (mTERF, Pfam-PF02536), Plant Organelle RNA Recognition (PORR, Pfam-PF11955), and Pentatricopeptide repeat (PPR, Pfam-PF13812) proteins. Previously, we established the roles of MatR and three nuclear-maturases, nMAT1, nMAT2, and nMAT4, in the splicing of different subsets of mitochondrial introns in Arabidopsis. The function of nMAT3 (AT5G04050) was found to be essential during early embryogenesis. Using a modified embryo-rescue method, we show that nMAT3-knockout plants are strongly affected in the splicing of nad1 introns i1, i3 and i4 in Arabidopsis mitochondria. The embryo-defect phenotype is tightly associated with complex I biogenesis defects. Functional complementation of nMAT3 restored the splicing defects and altered embryogenesis phenotypes associated with the nmat3 mutant-line.

scholarly journals The PPR-related splicing cofactor MSP1/EMB1025 protein, encoded by At4g20090, encode an essential protein that is required for the splicing of nad1 intron 1 and for the biogenesis of complex I in Arabidopsis mitochondria

2019 ◽  
Author(s):  
Corinne Best ◽  
Michal Zmudjak ◽  
Oren Ostersetzer-Biran
Keyword(s):  
Complex I ◽  
Rna Binding ◽  
Embryo Rescue ◽  
Plant Mitochondria ◽  
Rna Stability ◽  
Pentatricopeptide Repeat ◽  
Ppr Protein ◽  
Intron 1 ◽  
Rna Maturation ◽  
Embryonic Arrest

AbstractGroup II introns are particularly plentiful within plant mitochondrial genomes (mtDNAs), where they interrupt the coding-regions of many organellar genes, especialy within complex I (CI) subunits. Their splicing is essential for the biogenesis of the respiratory system and is facilitated by various protein-cofactors that belong to a diverse set of RNA-binding cofactors. These including maturases, which co-evolved with their host-introns, and various trans-acting factors, such as members of the pentatricopeptide-repeat (PPR) protein family. The genomes of angiosperms contain hundreds of PPR-related genes that are postulated to reside within the organelles and affect diverse posttranscriptional steps, such as editing, RNA-stability and processing or translation. Here, we report the characterization of MSP1 (Mitochondria Splicing PPR-factor 1; also denoted as EMB1025), which plays a key role in the processing of nad1 pre-RNAs in Arabidopsis mitochondria. Mutations in MSP1 gene-locus (At4g20090) result in early embryonic arrest. To analyze the putative roles of MSP1 in organellar RNA-metabolism we used a modified embryo-rescue method, which allowed us to obtain sufficient plant tissue for the analysis of the RNA and protein profiles associated with msp1 mutants. Our data indicate that MSP1 is essential for the trans-splicing of nad1 intron 1 in Arabidopsis mitochondria. Accordingly, msp1 mutants show CI biogenesis defects and reduced respiratory-mediated functions. These results provide with important insights into the roles of nuclear-encoded factors during early plant development, and contribute to our limited understanding of the importance of RNA-maturation and splicing in plant mitochondria during early embryogenesis.

scholarly journals PPR-SMR1 is required for the splicing of multiple mitochondrial introns, interacts with Zm-mCSF1, and is essential for seed development in maize

2019 ◽  
Vol 70 (19) ◽  
pp. 5245-5258 ◽  
Author(s):  
Zongliang Chen ◽  
Hong-Chun Wang ◽  
Jiayu Shen ◽  
Feng Sun ◽  
Miaodi Wang ◽  
...  
Keyword(s):  
Seed Development ◽  
Complex I ◽  
Splicing Factors ◽  
Group Ii Introns ◽  
Group Ii ◽  
Mitochondrial Introns

Two maize nucleus-encoded splicing factors, PPR-SMR1 and Zm-mCSF1, are required for the splicing of most mitochondrial group II introns and subsequent complex I biogenesis, and therefore play important roles in seed development.

scholarly journals Nuclear Encoded RNA Splicing Factors in Plant Mitochondria

2009 ◽  
Author(s):  
Oren Ostersetzer-Biran ◽  
Alice Barkan
Keyword(s):  
Rna Splicing ◽  
Plant Mitochondria ◽  
Group Ii Intron ◽  
Nuclear Genes ◽  
Metabolic Energy ◽  
Splicing Factors ◽  
Group Ii Introns ◽  
Intron Splicing ◽  
Group Ii ◽  
Mitochondrial Introns

Mitochondria are the site of respiration and numerous other metabolic processes required for plant growth and development. Increased demands for metabolic energy are observed during different stages in the plants life cycle, but are particularly ample during germination and reproductive organ development. These activities are dependent upon the tight regulation of the expression and accumulation of various organellar proteins. Plant mitochondria contain their own genomes (mtDNA), which encode for a small number of genes required in organellar genome expression and respiration. Yet, the vast majority of the organellar proteins are encoded by nuclear genes, thus necessitating complex mechanisms to coordinate the expression and accumulation of proteins encoded by the two remote genomes. Many organellar genes are interrupted by intervening sequences (introns), which are removed from the primary presequences via splicing. According to conserved features of their sequences these introns are all classified as “group-II”. Their splicing is necessary for organellar activity and is dependent upon nuclear-encoded RNA-binding cofactors. However, to-date, only a tiny fraction of the proteins expected to be involved in these activities have been identified. Accordingly, this project aimed to identify nuclear-encoded proteins required for mitochondrial RNA splicing in plants, and to analyze their specific roles in the splicing of group-II intron RNAs. In non-plant systems, group-II intron splicing is mediated by proteins encoded within the introns themselves, known as maturases, which act specifically in the splicing of the introns in which they are encoded. Only one mitochondrial intron in plants has retained its maturaseORF (matR), but its roles in organellar intron splicing are unknown. Clues to other proteins required for organellar intron splicing are scarce, but these are likely encoded in the nucleus as there are no other obvious candidates among the remaining ORFs within the mtDNA. Through genetic screens in maize, the Barkan lab identified numerous nuclear genes that are required for the splicing of many of the introns within the plastid genome. Several of these genes are related to one another (i.e. crs1, caf1, caf2, and cfm2) in that they share a previously uncharacterized domain of archaeal origin, the CRM domain. The Arabidopsis genome contains 16 CRM-related genes, which contain between one and four repeats of the domain. Several of these are predicted to the mitochondria and are thus postulated to act in the splicing of group-II introns in the organelle(s) to which they are localized. In addition, plant genomes also harbor several genes that are closely related to group-II intron-encoded maturases (nMats), which exist in the nucleus as 'self-standing' ORFs, out of the context of their cognate "host" group-II introns and are predicted to reside within the mitochondria. The similarity with known group-II intron splicing factors identified in other systems and their predicted localization to mitochondria in plants suggest that nuclear-encoded CRM and nMat related proteins may function in the splicing of mitochondrial-encoded introns. In this proposal we proposed to (i) establish the intracellular locations of several CRM and nMat proteins; (ii) to test whether mutations in their genes impairs the splicing of mitochondrial introns; and to (iii) determine whether these proteins are bound to the mitochondrial introns in vivo.  

scholarly journals APO1 Promotes the Splicing of Chloroplast Group II Introns and Harbors a Plant-Specific Zinc-Dependent RNA Binding Domain

2011 ◽  
Vol 23 (3) ◽  
pp. 1082-1092 ◽  
Author(s):  
Kenneth P. Watkins ◽  
Margarita Rojas ◽  
Giulia Friso ◽  
Klaas J. van Wijk ◽  
Jörg Meurer ◽  
...  
Keyword(s):  
Rna Binding ◽  
Binding Domain ◽  
Group Ii Introns ◽  
Rna Binding Domain ◽  
Group Ii

Nuclear-Encoded Maturase Protein 3 is Required for the Splicing of Various Group II Introns inMitochondria during Maize (zea mays L.) Seed Development

2020 ◽  
Author(s):  
Weiwei Chen ◽  
Yu Cui ◽  
Zheyuan Wang ◽  
Rongrong Chen ◽  
Cheng He ◽  
...  
Keyword(s):  
Zea Mays ◽  
Seed Development ◽  
Complex I ◽  
Positional Cloning ◽  
Zea Mays L ◽  
Mitochondrial Complex I ◽  
Group Ii Introns ◽  
Loss Of Function ◽  
Mitochondrial Complex ◽  
Group Ii

Abstract Splicing of plant organellar group II introns from precursor-RNA transcripts requires the assistance of nuclear-encoded splicing factors. Maturase (nMAT) is a kind of such factors, as its three homologs (nMAT1, 2, and 4) has been identified for splicing of various mitochondrial introns in Arabidopsis. However, function of nMAT in maize (Zea mays L.) is unknown. In this study, we identified a seed development mutant, Empty Pericarp 2441 (emp2441) from maize, which showed severely arrested embryogenesis and endosperm development. Positional cloning and transgenic complementation assays revealed that Emp2441 encoded a maturase-related protein, ZmnMAT3. ZmnMAT3 highly expressed during seed development and its protein located in the mitochondria. The loss-of-function of ZmnMAT3 resulted in reduced splicing efficiency of various mitochondrial group II introns, particularly of the trans-splicing of nad1 intron 1, 3, and 4, which consequently abolished the transcript of nad1 and severely impaired the assembly and activity of mitochondrial complex I. Moreover, the Zmnmat3 mutant showed defective mitochondrial structure and induced the expression and activity of alternative oxidases. These results indicated that ZmnMAT3 is essential for mitochondrial complex I assembly during kernel development in maize.

Two Novel PLS-Class Pentatricopeptide Repeat Proteins Are Involved in the Group II Intron Splicing of Mitochondrial Transcripts in the Moss Physcomitrella patens

2020 ◽  
Vol 61 (10) ◽  
pp. 1687-1698
Author(s):  
Mizuho Ichinose ◽  
Airi Ishimaru ◽  
Chieko Sugita ◽  
Kensaku Nakajima ◽  
Yasuhiro Kawaguchi ◽  
...  
Keyword(s):  
Posttranscriptional Regulation ◽  
Rna Binding ◽  
Physcomitrella Patens ◽  
Rna Binding Proteins ◽  
Group Ii Intron ◽  
Pentatricopeptide Repeat ◽  
Mobility Shift ◽  
Intron 1 ◽  
Ppr Proteins ◽  
Group Ii

Abstract Pentatricopeptide repeat (PPR) proteins are RNA-binding proteins that function in posttranscriptional regulation as gene-specific regulators of RNA metabolism in plant organelles. Plant PPR proteins are divided into four classes: P, PLS, E and DYW. The E- and DYW-class proteins are mainly implicated in RNA editing, whereas most of the P-class proteins predominantly participate in RNA cleavage, splicing and stabilization. In contrast, the functions of PLS-class proteins still remain obscure. Here, we report the function of PLS-class PpPPR_31 and PpPPR_9 in Physcomitrella patens. The knockout (KO) mutants of PpPPR_31 and PpPPR_9 exhibited slower protonema growth compared to the wild type. The PpPPR_31 KO mutants showed a considerable reduction in the splicing of nad5 intron 3 and atp9 intron 1. The PpPPR_9 KO mutants displayed severely reduced splicing of cox1 intron 3. An RNA electrophoresis mobility shift assay showed that the recombinant PpPPR_31 protein bound to the 5′ region of nad5 exon 4 and the bulged A region in domain VI of atp9 group II intron 1 while the recombinant PpPPR_9 bound to the translated region of ORF622 in cox1 intron 3. These results suggest that a certain set of PLS-class PPR proteins may influence the splicing efficiency of mitochondrial group II introns.

scholarly journals Chloroplast RH3 DEAD Box RNA Helicases in Maize and Arabidopsis Function in Splicing of Specific Group II Introns and Affect Chloroplast Ribosome Biogenesis

2012 ◽  
Vol 159 (3) ◽  
pp. 961-974 ◽  
Author(s):  
Yukari Asakura ◽  
Erin Galarneau ◽  
Kenneth P. Watkins ◽  
Alice Barkan ◽  
Klaas J. van Wijk
Keyword(s):  
Ribosome Biogenesis ◽  
Group Ii Introns ◽  
Rna Helicases ◽  
Specific Group ◽  
Dead Box ◽  
Group Ii

scholarly journals Organellar Introns in Fungi, Algae, and Plants

Cells ◽  
2021 ◽  
Vol 10 (8) ◽  
pp. 2001
Author(s):  
Jigeesha Mukhopadhyay ◽  
Georg Hausner
Keyword(s):  
Gene Expression ◽  
Ribosomal Proteins ◽  
Heterologous Gene Expression ◽  
Group I Introns ◽  
Group Ii Introns ◽  
Homing Endonucleases ◽  
Organellar Genomes ◽  
Chloroplast Genomes ◽  
Group I ◽  
Group Ii

Introns are ubiquitous in eukaryotic genomes and have long been considered as ‘junk RNA’ but the huge energy expenditure in their transcription, removal, and degradation indicate that they may have functional significance and can offer evolutionary advantages. In fungi, plants and algae introns make a significant contribution to the size of the organellar genomes. Organellar introns are classified as catalytic self-splicing introns that can be categorized as either Group I or Group II introns. There are some biases, with Group I introns being more frequently encountered in fungal mitochondrial genomes, whereas among plants Group II introns dominate within the mitochondrial and chloroplast genomes. Organellar introns can encode a variety of proteins, such as maturases, homing endonucleases, reverse transcriptases, and, in some cases, ribosomal proteins, along with other novel open reading frames. Although organellar introns are viewed to be ribozymes, they do interact with various intron- or nuclear genome-encoded protein factors that assist in the intron RNA to fold into competent splicing structures, or facilitate the turn-over of intron RNAs to prevent reverse splicing. Organellar introns are also known to be involved in non-canonical splicing, such as backsplicing and trans-splicing which can result in novel splicing products or, in some instances, compensate for the fragmentation of genes by recombination events. In organellar genomes, Group I and II introns may exist in nested intronic arrangements, such as introns within introns, referred to as twintrons, where splicing of the external intron may be dependent on splicing of the internal intron. These nested or complex introns, with two or three-component intron modules, are being explored as platforms for alternative splicing and their possible function as molecular switches for modulating gene expression which could be potentially applied towards heterologous gene expression. This review explores recent findings on organellar Group I and II introns, focusing on splicing and mobility mechanisms aided by associated intron/nuclear encoded proteins and their potential roles in organellar gene expression and cross talk between nuclear and organellar genomes. Potential application for these types of elements in biotechnology are also discussed.

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