RNA editing is a tightly controlled process by which cytidines are converted to uridines in RNAs transcribed from the chloroplast and mitochondrial genomes in flowering plants. Multiple organellar RNA editing factor (MORF) complex was recently shown to be highly associated with C-to-U RNA editing activity of vascular plant editosome. However, mechanisms by which MORF9 mediates plastid RNA editing to control plant development in response to environmental cues remains obscure. In this study, we found that loss of MORF9 function impaired PSII efficiency, NDH activity, and carbohydrate production, rapidly promoted nuclear gene expression including sucrose transporter and sugar/energy responsive genes, and attenuated seedling development under sugar starvation conditions. Sugar repletion increased MORF9 and MORF2 expression in wild-type seedlings and promoted inefficiency of matK-706C, accD-794C, ndhD-383C and ndhF-290C RNA editing in morf9 mutant. This RNA editing inefficiency was associated with altered cell division in root meristem zone and nuclear gene expression in the morf9 mutant. Using gin2, snrk1, morf9 single and double mutants and overexpression of SnRK1 (KIN10) or HXK1 in the morf9 mutant background demonstrated that RNA editing efficiency of ndhD-383C and ndhF-290C sites was diminished in the gin2/morf9 double mutants, and editing efficiency of matK-706C, accD-794C, ndhD-383C and ndhF-290C sites was significantly diminished in the snrk1/morf9 double mutants. Overexpressing HXK1 or SnRK1 promoted RNA editing rate of matK, accD, ndhD, and ndhF in leaves of morf9 mutants，indicating that HXK1 might be required for MORF9 mediated ndhD-383C and ndhF-290C editing, while SnRK1 may only be required for MORF9 mediated ndhF-290C site editing. Collectively these findings suggest that sugar and/or its intermediary metabolites impair MORF9 mediated plastid RNA editing resulting in derangements of plant root development.

RNA editing converts cytidines to uridines in the RNAs transcribed from the chloroplast and mitochondrial genomes in flowering plants. Multiple organellar RNA editing factor (MORF) complex is discovered to be highly associated with C-to-U RNA editing activity of vascular plant editosome. However, mechanism of MORF9 mediating plastid RNA editing controlling plant development and in response to environmental cues remains limited. In this study, we found that loss of MORF9 function impaired PSII efficiency, NDH activity, and carbohydrate production, rapidly promoted nuclear gene expression including sucrose transporter and sugar/energy responsive genes, exhibiting a retard seedling development under sugar starvation condition. When exogenous application of sugar increased transcript and protein level of MORF9 and MORF2 in wild-type, and enhanced the decreasing of matK-706C, accD-794C, ndhD-383C and ndhF-290C RNA editing efficiency in morf9 mutant, and partially recovered altered cell division of root meristem zone, and nuclear gene expression in morf9 mutant. Using gin2, snrk1, morf9 single and double mutants and overexpressing SnRK1 (KIN10) or HXK1 in morf9 mutant background genetically addressed that RNA editing efficiency of ndhD-383C and ndhF-290C sites was declined in the gin2morf9, that of matK-706C, accD-794C, ndhD-383C and ndhF-290C sites was significantly declined in the snrk1morf9, while overexpressing HXK1 or SnRK1 promoted RNA editing rate of matK, accD, ndhD, and ndhF in leaves of morf9 mutant，indicating that HXK1 might require for MORF9 mediating ndhD-383C and ndhF-290C editing, SnRK1 only require for MORF9 mediating ndhF-290C site editing. It suggests that sugar as an energy/sugar signal impairs MORF9 mediating plastid RNA editing affecting plant root development.