The origin, evolution, and functional divergence of the Dicer-like (DCL) and Argonaute (AGO) gene families in plants

Dicer-like (DCL) and Argonaute (AGO) proteins play a crucial role in plant epigenetics. However, the evolutionary origins and roles of these gene families in plant adaptation, stress response, and development remain unclear. This study explores the origin and functional evolution of DCLs and AGOs across 36 plant species spanning diverse taxonomic groups. Member identification, phylogenetic analysis, evolutionary trajectory analysis, and functional divergence analysis were conducted. The results show that the DCL and AGO originated in Rhodophytes and underwent two major expansions: during algal terrestrialization and the transition from lower to higher plants. In seed plants, DCLs diversified into four classes following two whole-genome duplication (WGD) events, whereas AGOs diversified into seven classes through two WGD events and one tandem duplication event. Expression analyses in Physcomitrium patens, Zea mays, Arabidopsis thaliana, and Fragaria vesca revealed high expression of these gene families in reproductive tissues, with notably lower expression in pollen. Additionally, the expression of these genes exhibits different responses to various environmental stresses in A. thaliana and Z. mays, highlighting their important roles in adaptation to environmental fluctuations. The present research reveals the functional diversification of DCLs and AGOs and their crucial roles in facilitating terrestrial adaptation and rapid land colonization.