Plants tolerate substantial rates of plastid mistranslation via regulated proteostasis

Abstract

In bacteria, protein mistranslation can improve stress tolerance. Mitochondria and plastids evolved from bacteria and use a prokaryotic-type expression machinery to synthesize proteins. Interestingly, fungi and animal mitochondria are highly sensitive to mistranslation, which for instance manifests in lethal mitochondrial cardiomyopathy disorder. The response in plant cells is unknown. Glutaminyl-transfer RNAs (Gln-tRNA Gln ) of bacteria and endosymbiotic organelles are synthesized indirectly. Initially, tRNA Gln is aminoacylated with glutamate. Subsequently, Gln is produced through trans-amidation by the aminoacyl-tRNA amido-transferase complex GatCAB. Consequentially, compromised GatCAB activity yields misloaded Glu-tRNA Gln . Arabidopsis mutants with decreased GatCAB levels provide global insights into organellar mistranslation in plants: Our proteomics analyses revealed mutant-specific high plastid and low mitochondrial Gln-to-Glu misincorporation rates in organellar-expressed protein complexes with only modest protein abundance changes in plastids and none in mitochondria. We identify efficient compensatory mechanisms that mitigate the physiological consequences of elevated mistranslation in mutants. Interestingly, wild-type plants under temperature stress also have altered Gln-to-Glu misincorporation while temperature acclimation differs in Gln-to-Glu hypermistranslating mutants. Our study indicates that the response toward organellar mistranslation varies among eukaryotes and enables future detailed investigation of mistranslation compensation mechanisms in plant cells.