MORF9‐dependent specific plastid RNA editing inhibits root growth under sugar starvation in Arabidopsis

• Published in: Plant, cell and environment cell and environment, 2024-06, Vol.47 (6), p.1921-1940
• Main Authors: Xie, Yakun, Yu, Jinfa, Tian, Faan, Li, Xue, Chen, Xinyan, Li, Yanyun, Wu, Binghua, Miao, Ying
• Format: Article
• Language: English
• Subjects: Arabidopsis - genetics; Arabidopsis - growth & development; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Carbohydrates; Editing; Gene expression; Gene Expression Regulation, Plant; Metabolites; MORF; Mutants; Mutation; Photosystem II; Photosystem II Protein Complex - genetics; Photosystem II Protein Complex - metabolism; Plant growth; Plant roots; Plant Roots - genetics; Plant Roots - growth & development; Plant Roots - metabolism; Plants; Plastids - genetics; Plastids - metabolism; Ribonucleic acid; RNA; RNA editing; RNA Editing - genetics; Root development; Seedlings; Sucrose; Sucrose transporter; Sugar; sugar response/regulation; Sugars - metabolism
• ISSN: 0140-7791; 1365-3040
• DOI: 10.1111/pce.14856

Multiple organellar RNA editing factor (MORF) complex was shown to be highly associated with C‐to‐U RNA editing of vascular plant editosome. However, mechanisms by which MORF9‐dependent plastid RNA editing controls plant development and responses to environmental alteration remain 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 root growth under sugar starvation conditions. Sugar repletion increased MORF9 and MORF2 expression in wild‐type seedlings and reduced RNA editing of matK‐706, accD‐794, ndhD‐383 and ndhF‐290 in the morf9 mutant. RNA editing efficiency of ndhD‐383 and ndhF‐290 sites was diminished in the gin2/morf9 double mutants, and that of matK‐706, accD‐794, ndhD‐383 and ndhF‐290 sites were significantly diminished in the snrk1/morf9 double mutants. In contrast, overexpressing HXK1 or SnRK1 promoted RNA editing rate of matK‐706, accD‐794, ndhD‐383 and ndhF‐290 in leaves of morf9 mutants, suggesting that HXK1 partially impacts MORF9 mediated ndhD‐383 and ndhF‐290 editing, while SnRK1 may only affect MORF9‐mediated ndhF‐290 site editing. Collectively, these findings suggest that sugar and/or its intermediary metabolites impair MORF9‐dependent plastid RNA editing resulting in derangements of plant root development. Summary statement Sugar supplementation alters MORF9 levels and MORF9‐dependent plastid RNA editing, which in turn affects nuclear gene expression and root growth in Arabidopsis, suggesting that plastid RNA editing regulates auxin‐related root growth and sugar starvation response via a retrograde signalling pathway.