Species-specific loss of chloroplast ndhB -872 RNA editing in tea and tomato is caused by impaired QED1 mediated MORF recruitment

Abstract

Chloroplast RNA editing is a critical post transcriptional modification that significantly influences photosynthesis, growth and development in plants. However, the editing sites and frequency of RNA editing events exhibit considerable variation among different plant species. The ndhB-872 site, within the ndhB gene which encodes a subunit of the NDH complex, is edited in Arabidopsis but is not edited in tea (Camellia sinensis) and tomato (Solanum lycopersicum). The mechanism underlying the evolutionary loss of this editing event and its impact on crop physiology have remained unknown. In this study, analysis of 55 land plant species reveals that the RNA editing factor QED1 (QUINTUPLE EDITING FACTOR 1) has undergone co-evolution in correlation with its ndhB-872 target site. Structural modeling and protein–protein interaction analyses indicated that species-specific structural variation in QED1 impaired the recruitment of chloroplast-localized MORF2/9 cofactors, leading to the loss of ndhB-872 editing. Heterologous overexpression of AtQED1 successfully restored the ndhB-872 editing in tea and tomato plants. Re-establishing ndhB-872 editing in tomato led to reduced photosynthetic electron transport, smaller leaf area, white leaf spots in seedlings, and a three-week delay in fruit ripening. Furthermore, CRISPR/Cas9 knockout of SlMORF2.1 and SlMORF9 demonstrated that the assembly of the QED1-MORF2/9 complex is critical for ndhB-872 editing. Together, these findings revealed the functional necessity of ndhB-872/QED1 co-evolution in tea and tomato, elucidate the critical role of ndhB-872 editing in tomato photosynthetic homeostasis, and offer promising methods for targeted manipulation of ndhB-872 editing in crop improvement.