Abstract
As a fascinating and complicated nanomotor, chloroplast ATP synthase comprises nine subunits encoded by both the nuclear and plastid genomes. Because of its uneven subunit stoichiometry, biogenesis of ATP synthase and expression of plastid-encoded ATP synthase genes requires assistance by nucleus-encoded factors involved in transcriptional, post-transcriptional, and translational steps. In this study, we report a P-class pentatricopeptide repeat (PPR) protein BFA2 (Biogenesis Factor required for ATP synthase 2) that is essential for accumulation of the dicistronic atpH/F transcript in Arabidopsis chloroplasts. A loss-of-function mutation in BFA2 results in a specific reduction of more than 3/4 of chloroplast ATP synthase, which is likely due to the absence of dicistronic atpH/F transcript. BFA2 protein contains 22 putative PPR motifs and exclusively localizes in the chloroplast. Bioinformatics and Electrophoretic Mobility Shift Assays (EMSA) analysis showed that BFA2 binds to the consensus sequence of the atpF-atpA intergenic region in a sequence-specific manner. However, translation initiation of the atpA was not affected in the bfa2 mutant. Thus, we propose that the chloroplast PPR protein BFA2 mainly acts as barrier to prevent the atpH/F transcript degradation by exoribonucleases by binding to the consensus sequence of the atpF-atpA intergenic region.
Highlights
Chloroplasts in photosynthetic eukaryotes are thought to have originated from cyanobacteria through endosymbiosis
We report the characterization of a chloroplast pentatricopeptide repeat (PPR) protein called BFA2 (Biogenesis Factors required for ATP synthase 2) that binds to the atpF-atpA intergenic region in a sequence-specific manner
The relaxation of nonphotochemical quenching (NPQ) is less efficient in the bfa2 mutants and NPQ is maintained at high levels compared with WT (Figure 1C)
Summary
Chloroplasts in photosynthetic eukaryotes are thought to have originated from cyanobacteria through endosymbiosis. Most of the genes from the cyanobacterial ancestor were transferred to the nucleus of the host cell and chloroplasts have only retained about 100 genes (Martin et al, 2002) These plastid genes encode proteins required for transcription and translation as well as the essential components of photosynthetic complexes. To ensure efficient gene expression, chloroplasts require a vast number of nuclear-encoded protein factors facilitating transcription, RNA stabilization, splicing, editing, and translation (Stern et al, 2010; Barkan, 2011). Among these factors, pentatricopeptide repeat (PPR) proteins are highly prominent and involved in BFA2 Stabilizes Dicistronic atpH/F mRNA various steps of RNA metabolism and protein translation (Schmitz-Linneweber and Small, 2008). The PLSclass PPR proteins usually contain C-terminal E and DYW motifs which are required for RNA editing (Shikanai, 2015)
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