SMG1 is an ancient nonsense-mediated mRNA decay effector.

ABSTRACT

Nonsense-mediated mRNA decay (NMD) is a eukaryotic process that targets selected mRNAs for destruction, for both quality control and gene regulatory purposes. SMG1, the core kinase of the NMD machinery in animals, phosphorylates the highly conserved UPF1 effector protein to activate NMD. However, SMG1 is missing from the genomes of fungi and the model flowering plant Arabidopsis thaliana, leading to the conclusion that SMG1 is animal-specific and questioning the mechanistic conservation of the pathway. Here we show that SMG1 is not animal-specific, by identifying SMG1 in a range of eukaryotes, including all examined green plants with the exception of A. thaliana. Knockout of SMG1 by homologous recombination in the basal land plant Physcomitrella patens reveals that SMG1 has a conserved role in the NMD pathway across kingdoms. SMG1 has been lost at various points during the evolution of eukaryotes from multiple lineages, including an early loss in the fungal lineage and a very recent observable gene loss in A. thaliana. These findings suggest that the SMG1 kinase functioned in the NMD pathway of the last common eukaryotic ancestor.