Summary Mitochondrial biogenesis relies on nuclearly encoded factors, which regulate the expression of the organellar‐encoded genes. Pentatricopeptide repeat (PPR) proteins constitute a major gene family in angiosperms that are pivotal in many aspects of mitochondrial (mt)RNA metabolism (e.g. trimming, splicing, or stability). Here, we report the analysis of MITOCHONDRIA STABILITY/PROCESSING PPR FACTOR1 (MSP1, At4g20090), a canonical PPR protein that is necessary for mitochondrial functions and embryo development. Loss‐of‐function allele of MSP1 leads to seed abortion. Here, we employed an embryo‐rescue method for the molecular characterization of msp1 mutants. Our analyses reveal that msp1 embryogenesis fails to proceed beyond the heart/torpedo stage as a consequence of a nad1 pre‐RNA processing defect, resulting in the loss of respiratory complex I activity. Functional complementation confirmed that msp1 phenotypes result from a disruption of the MSP1 gene. In Arabidopsis, the maturation of nad1 involves the processing of three RNA fragments, nad1.1, nad1.2, and nad1.3. Based on biochemical analyses and mtRNA profiles of wild‐type and msp1 plants, we concluded that MSP1 facilitates the generation of the 3′ terminus of nad1.1 transcript, a prerequisite for nad1 exons a–b splicing. Our data substantiate the importance of mtRNA metabolism for the biogenesis of the respiratory system during early plant life.
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 function 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 ofMITOCHONDRIA 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 theMSP1gene. As a loss-of-function allele ofArabidopsis MSP1leads to seed abortion, we employed an embryo-rescue method for the molecular characterization ofmsp1mutants. Our data show that msp1 embryo-development fails to proceed beyond the heart-torpedo transition stage as a consequence of a severenad1pre-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,nad1.2andnad1.3. Based on detailed analyses of the mtRNA profiles in wild-type andmsp1plants, we concluded that through its association with a specific site innad1.1, MSP1 facilitates the generation of its 3'-terminus and stabilizes it - a prerequisite fornad1exons a-b splicing. Our data substantiate the importance of mtRNA metabolism for the biogenesis of the respiratory machinery during early-plant development.
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