MSP1 encodes an essential RNA-binding PPR factor required for nad1 maturation and complex I biogenesis in Arabidopsis mitochondria

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Summary Mitochondria are semi-autonomous organelles that serve as hubs for aerobic energy metabolism. The biogenesis of the respiratory (OXPHOS) system relies on nuclear-encoded factors, which regulate the transcription, processing and translation of mitochondrial (mt)RNAs. These include proteins of primordial origin, as well as eukaryotic-type RNA-binding families recruited from the host genomes to fu nc tion in mitogenome expression. Pentatricopeptide repeat (PPR) proteins constitute a major gene-family in angiosperms that is pivotal in many aspects of mtRNA metabolism, such as editing, splicing or stability. Here, we report the analysis of MITOCHONDRIA STABILITY/PROCESSING PPR FACTOR1 ( MSP1 , At4g20090), a canonical mitochondria-localized PPR protein that is necessary for mitochondrial biogenesis and embryo-development. Functional complementation confirmed that the phenotypes result from a disruption of the MSP1 gene. As a loss-of-function allele of Arabidopsis MSP1 leads to seed abortion, we employed an embryo-rescue method for the molecular characterization of msp1 mutants. Our data show that msp1 embryo-development fails to proceed beyond the heart-torpedo transition stage as a consequence of a severe nad1 pre-RNA processing-defect, resulting in the loss of respiratory complex I (CI) activity. The maturation of nad1 involves the processing of three RNA-fragments, nad1 . 1, nad1 . 2 and nad1 . 3 . Based on biochemical analyses and the mtRNA profiles in wild-type and msp1 plants, we concluded that through its association with a specific site in nad1 . 1 , MSP1 facilitates the generation of its 3’-terminus and stabilizes it -a prerequisite for nad1 exons a-b splicing. Our data substantiate the importance of mtRNA metabolism for the biogenesis of the respiratory machinery during early-plant development.