Dek570-1, a PPR-DYW protein, is required for maize seed and plant development via modulation of C-to-U RNA editing in mitochondria and chloroplasts.

Main conclusion: Maize Dek570-1 affects the expression and function of organellar genes by performing cytidines-to-uridines RNA editing at specific sites of mitochondrial and chloroplast transcripts, thereby regulating seed and plant development. Cytidines-to-uridines (C-to-U) RNA editing at specific sites of mitochondrial and plastid transcripts is crucial for the expression and function of organellar genes, which requires PPR proteins. Here, we report the map-based cloning and characterization of Defective Kernel 570-1 (Dek570-1), which encodes a PPR-DYW protein and is an allele of Emp17. However, compared to the empty pericarp and embryonic lethality of emp17 (W22 background), dek570-1 (Zheng58 background) can produce small but viable seeds despite reducing the size of embryo and endosperm. dek570-1 plants are short and yellowed, but they can reproduce offspring. In mitochondria, loss-of-function of Dek570-1 abolishes the C-to-U editing at nad2-677 and ccmF_C-799 sites, and reduces the editing at ccmF_C-906 site, consistent with Emp17 deficiency. But unlike the reduced editing of the ccmF_C-966 site in emp17, the ccmF_C-966 site in dek570-1 is fully edited, and several other editing sites such as ccmF_C-87, ccmF_C-301, and ccmF_C-306 are also found. More noteworthy is that Dek570-1 is not only located in mitochondria like Emp17, but also in chloroplasts. Correspondingly, the editing at rpl20-308 site of dek570-1 chloroplasts was significantly reduced, affecting the expression of some rRNAs, plastid-encoded RNA polymerase (PEP)- and nuclear-encoded single-subunit RNA polymerase (NEP)-dependent genes, thereby reducing chlorophyll accumulation and photosynthetic rate. Together, these results indicate that Dek570-1 is essential for C-to-U editing at several sites in mitochondrial and chloroplast transcripts, as well as for seed and plant development, and that this locus (Zm00001d028422) may have generated some functional evolutionary divergence in maize with different genetic backgrounds.