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nMAT3 is an essential maturase splicing factor required for holo-complex I biogenesis and embryo-development in Arabidopsis thaliana plants.

Group II introns are self-splicing and mobile genetic elements consisting of the catalytic intron-RNA and its related intron-encoded splicing maturase protein cofactor. Group II sequences are in particularly plentiful within the mitochondria of land plants, were they reside within many critical gene-loci. During evolution, the plant organellar introns have degenerated into ORF-less sequences that rely for their splicing on different host-acting protein cofactors, which may also provide 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 i1, i3 and i4 in Arabidopsis mitochondria, resulting with complex I biogenesis defects and altered respiratory activities. Functional complementation of nMAT3 restored the organellar defects and embryo-arrested phenotypes associated with 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. These likely cooperate together in the maturation of nad1 pre-RNAs. Our results provide with important insights into the roles of maturases in mitochondria gene-expression and the biogenesis of the respiratory system during early plant life. Supporting Information.