Abstract
Group II introns are common features of most angiosperm mitochondrial genomes. Intron splicing is thus essential for the expression of mitochondrial genes and is facilitated by numerous nuclear-encoded proteins. However, the molecular mechanism and the protein cofactors involved in this complex process have not been fully elucidated. In this study, we characterized three new pentatricopeptide repeat (PPR) genes, called MISF26, MISF68, and MISF74, of Arabidopsis and showed they all function in group II intron splicing and plant development. The three PPR genes encode P-type PPR proteins that localize in the mitochondrion. Transcript analysis revealed that the splicing of a single intron is altered in misf26 mutants, while several mitochondrial intron splicing defects were detected in misf68 and misf74 mutants. To our knowledge, MISF68 and MISF74 are the first two PPR proteins implicated in the splicing of more than one intron in plant mitochondria, suggesting that they may facilitate splicing differently from other previously identified PPR splicing factors. The splicing defects in the misf mutants induce a significant decrease in complex I assembly and activity, and an overexpression of mRNAs of the alternative respiratory pathway. These results therefore reveal that nuclear encoded proteins MISF26, MISF68, and MISF74 are involved in splicing of a cohort of mitochondrial group II introns and thereby required for complex I biogenesis.
Highlights
Mitochondria are essential eukaryotic organelles that are responsible for energy production via aerobic respiration and are thought to have originated from the endosymbiotic association of an ancient α-proteobacterium (Gray et al, 1999; Andersson et al, 2003; Gray, 2012)
After molecular characterization of the corresponding mutants, we named these genes Mitochondrial Intron Splicing Factor 26 (MISF26), Mitochondrial Intron Splicing Factor 68 (MISF68), and Previous studies have shown that pentatricopeptide repeat (PPR) proteins are RNAbinding proteins and function in a wide range of mitochondrial and plastid RNA processing events (Barkan and Small, 2014; Hammani and Giegé, 2014)
This study reveals the function of three new mitochondria-targeted PPR proteins and shows that they are essential for the splicing of six separate mitochondrial introns
Summary
Mitochondria are essential eukaryotic organelles that are responsible for energy production via aerobic respiration and are thought to have originated from the endosymbiotic association of an ancient α-proteobacterium (Gray et al, 1999; Andersson et al, 2003; Gray, 2012). A small proportion of the ancestral genes have been retained in modern mitochondria. Mitochondrial genomes exhibit considerable variations in size, structure and organization (Kubo and Newton, 2008; Gualberto and Newton, 2017). Plant mitochondrial genomes are highly recombinogenic and complex RNA expression processes have likely evolved in response (Hammani and Giegé, 2014). The splicing of numerous introns, which interrupt protein-coding genes, is required to generate translatable mature mRNAs and is accomplished for the most part by nuclear-encoded protein transfactors
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