Mitochondria play key roles in cellular-energy metabolism and are vital for plant-life, such as for successful germination and early-seedling establishment. Most mitochondria contain their own genetic system (mtDNA, mitogenome), with an intrinsic protein-synthesis machinery. Although the challenges of maintaining prokaryotic-type structures and functions are common to Eukarya, land plants possess some of the most complex organelle composition of all known organisms. Angiosperms mtDNAs are characteristically the largest and least gene-dense among the eukaryotes. They often contain highly-variable intergenic regions of endogenous or foreign origins and undergo frequent recombination events, which result in different mtDNA configurations, even between closely-related species. The expression of the mitogenome in angiosperms involves extensive mtRNA processing steps, including numerous editing and splicing events. Why do land-plant’s mitochondria have to be so complex? The answer to this remains a matter of speculation. We propose that this complexity may have arisen throughout the terrestrialization of plants, as a means to control embryonic mitochondrial functions —a critical adaptive trait to optimize seed germination. The unique characteristics of plant mtDNA may play pivotal roles in the nuclear-regulation of organellar biogenesis and metabolism, possibly to control embryos quiescence or dormancy, essential determinants for the establishment of viable plantlets that can survive post-germination.
Group-II introns are self-splicing mobile genetic elements consisting of catalytic intron-RNA and its related intron-encoded splicing maturase protein cofactor. Group-II sequences are particularly plentiful within the mitochondria of land plants, where they reside within many critical gene loci. During evolution, the plant organellar introns have degenerated, such as they lack regions that are are required for splicing, and also lost their evolutionary related maturase proteins. Instead, for their splicing the organellar introns in plants rely on different host-acting protein cofactors, which may also provide a means to link cellular signals with respiratory functions. The nuclear genome of Arabidopsis thaliana encodes four maturase-related factors. Previously, we showed that three of the maturases, nMAT1, nMAT2 and nMAT4, function in the excision of different group-II introns in Arabidopsis mitochondria. The function of nMAT3 (encoded by the At5g04050 gene locus) 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 1, 3 and 4 in Arabidopsis mitochondria, resulting in complex-I biogenesis defects and altered respiratory activities. Functional complementation of nMAT3 restored the organellar defects and embryo-arrested phenotypes associated with the nmat3 mutant line. Notably, nMAT3 and nMA4 were found to act on the same RNA targets but have no redundant functions in the splicing of nad1 transcripts. The two maturases, nMAT3 and nMAT4 are likely to cooperate together in the maturation of nad1 pre-RNAs. Our results provide important insights into the roles of maturases in mitochondria gene expression and the biogenesis of the respiratory system during early plant life.
Group 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. Brown, G.G., Colas des Francs-Small, C. and Ostersetzer-Biran, O. (2014) Group II intron splicing factors in plant mitochondria. Front Plant Sci, 5, 35. Redefining the structural motifs that determine RNA binding and RNA editing by pentatricopeptide repeat proteins in land plants. Plant J, 85, 532-547.
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