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Chloroplast gene expression involves the participation of hundreds of pentatricopeptide repeat (PPR) RNA binding proteins, and proteins in the PLS subfamily typically specify sites of RNA editing, whereas those in the P-subfamily typically stabilize RNA, activate translation, or promote intron splicing. Several P-type PPR proteins include a small MutS-related (SMR) domain, but the biochemical contribution of the SMR domain remains enigmatic. Here, we describe a rice ( Oryza sativa ) mutant, osatp4 , lacking the ortholog of ATP4, a PPR-SMR protein in maize ( Zea mays ). osatp4 mutants were chlorotic and had a plastid-ribosome deficiency when grown in the cold. Like maize ATP4, OsATP4 was required for the accumulation of dicistronic rpl16 - rpl14 transcripts. Surprisingly, OsATP4 was also required for the editing of a specific nucleotide in the ribosomal protein S8 transcripts, rps8 , and this function was conserved in maize. By contrast, rps8 RNA was edited normally in the maize PROTON gradient regulation3 mutant, pgr3 , which also lacks rpl16 - rpl14 transcripts, indicating that the editing defect in atp4 mutants is not a secondary effect of altered rpl16 - rpl14 RNA metabolism. Expression of the edited rps8 isoform in transgenic osatp4 mutants complemented the cold-sensitive phenotype, indicating that a rps8 expression defect accounts for the cold-sensitivity. We suggest that ATP4 stimulates rps8 editing by facilitating access of a previously characterized PLS-type RNA editing factor to its cognate cis-element upstream of the edited nucleotide.

The PPR-SMR Protein ATP4 Is Required for Editing the Chloroplast rps8 mRNA in Rice and Maize