A Single Ancient Origin for Prototypical Serine/Arginine-Rich Splicing Factors1[W][OA]

Eukaryotic pre-mRNA splicing is a process involving a very complex RNA-protein edifice.
Serine/arginine-rich (SR) proteins play essential roles in pre-mRNA constitutive and
alternative splicing, and have been suggested to be crucial in plant-specific forms of
developmental regulation and environmental adaptation. Despite their functional importance,
little is known about their origin and evolutionary history. SR splicing factors have a modular
organization featuring at least one RRM domain and a C-terminal region enriched in Ser/Arg
dipeptides. To investigate the evolution of SR proteins, we infer phylogenies for >12,000
RRM domains representing >200 broadly sampled organisms. Our analyses reveal that the
RRM domain is not restricted to eukaryotes and that all prototypical SR proteins share a
single ancient origin, including the plant-specific SR45 protein. Based on these findings, we
propose a scenario for their diversification into four natural families, each corresponding to a
main SR architecture, and a dozen subfamilies, of which we profile both sequence
conservation and composition. Finally, using operational criteria for computational discovery
and classification, we catalogue SR proteins in 20 model organisms, with a focus on green
algae and land plants. Altogether, our study confirms the homogeneity and antiquity of SR
splicing factors, while establishing robust phylogenetic relationships between animal and
plant proteins, which should enable functional analyses of lesser characterized SR family
members, especially in green plants.