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

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.