Origin, evolution and diversification of plant ARGONAUTE proteins

Argonaute (AGO) proteins are central players in RNA interference in eukaryotes. They associate with small RNAs (sRNA) and lead to transcriptional or posttranscriptional silencing of targets, thereby regulating diverse biological processes. The molecular and biological functions of AGO proteins have been extensively characterized, particularly in a few angiosperm species, leading to the recognition that the AGO family has expanded to accommodate diverse sRNAs thereby performing diverse biological functions. However, understanding of the expansion of AGO proteins in plants is still limited, due to a dearth of knowledge of AGO proteins in green algal groups. Here, we identified more than 2900 AGO proteins from 244 plant species, including green algae, and performed a large-scale phylogenetic analysis. The phylogeny shows that the plant AGO family gave rise to four clades after the emergence of hydrobiontic algae and prior to the emergence of land plants. Subsequent parallel expansion in ferns and angiosperms resulted in eight main clades in angiosperms: AGO2, AGO7, AGO6, AGO4, AGO1, AGO10a, AGO10b and AGO5. On the basis of this phylogeny, we identified two novel AGO4 orthologs that Arabidopsis does not have, and redefined AGO10, which is composed of AGO10a and AGO10b. Finally, we propose a hypothetical evolutionary model of AGO proteins in plants. Our studies provide a deeper understanding of the phylogenetic relationships of AGO family members in the green lineage, which would help to further reveal their roles as RNAi effectors.

Automated summary

Argonaute (AGO) proteins are essential for RNA interference in eukaryotes, regulating biological processes by silencing target genes through association with small RNAs. A comprehensive phylogenetic analysis identified multiple AGO proteins in 244 plant species, revealing the evolutionary history of the plant AGO family and their roles as RNAi effectors. This study provides insights into the expansion and diversification of AGO proteins in plants, shedding light on their functional roles in different biological processes.