The maternal-effect gene ZmGRP23 promotes PPR-DYW-mediated RNA editing in maize mitochondria

The maternal effect is a non-Mendelian inheritance phenomenon in which the maternal genotype regulates offspring traits via gametic cytoplasmic components or genomic imprinting. Hundreds of maternal-effect genes have been identified; however, the underlying molecular mechanisms and biological roles of these genes remain unclear. Here we report that ZmGRP23 is a maternal-effect gene that regulates maize (Zea mays) seed development by mediating mitochondrial RNA editing. The maize GLUTAMINE-RICH PROTEIN23 (GRP23) encodes an atypical pentatricopeptide repeat (PPR) protein with a unique C-terminal domain. ZmGRP23 exhibits maternal expression dominance in a genetic background-dependent manner (e.g., W22). Loss of ZmGRP23 function arrests zygotic development at very early stages and reduces pollen transmission. Low expression of ZmGRP23 reduces the RNA editing efficiency at 190 mitochondrial sites in the endosperm, and most of these sites depend on canonical PPR-DYW proteins for editing. ZmGRP23 shows no or weak interaction with the full length of canonical PPR-DYW proteins; however, it strongly interacts with the E and the carboxyl terminus of DYW domains of these proteins. PPR-DYW proteins strongly interact with maize multiple organellar RNA-editing factor1 (MORF1) and MORF8, both of which also bind ZmGRP23. ZmMORF enhances the interaction between ZmGRP23 and PPR-DYW proteins. This implies that ZmMORF binding may induce conformational changes in PPR-DYW proteins, exposing ZmGRP23 interaction interfaces and promoting ZmGRP23 recruitment. This study reveals that ZmGRP23 mediates mitochondrial RNA editing through non-canonical recruitment of canonical PPR-DYW proteins and implies that an epigenetic-mitochondrial regulatory axis bridges RNA editing plasticity to seed development.