Gain, loss, and fusion: ancient and eventful origin of <i>DIVARICATA</i> and <i>DRIF</i> genes

Comprising one of the largest plant gene families, MYB genes are major regulators of growth and development across plant tissues. Their evolutionary history is complex with recurrent gain and loss of the MYB domains, sometimes within the same multi-domained gene, creating a reticulate phylogenetic history, with various parts of the same gene having conflicting phylogenetic histories. Multiple MYB genes may co-operate or compete, thus constituting an on/off switch regulating transcription of downstream genes. We determined the phylogenetic origin of the multi-domained MYB regulators called DIVARICATA (DIV) genes, their cofactors the DRIF genes, and their competitors the LFG genes. We report that DIV arose through the fusion of two simpler MYB genes that resulted in a gene with three MYB domains (MYBA-MYB1-MYB2). The MYBA domain was later lost through a non-gradual process resulting in the two-domained MYB1-MYB2 DIV genes in green plants (including flowering plants). Further truncation of the MYB1 domain resulted in LFG genes that have only the MYB2 domain. The MYBA and the MYB2 domains were derived from the SHAQKY clade of MYB domains; the MYB1 domain and the MYBD domain of DRIF were derived from the clade associated with the SANT2 domain of ZUO1/ZRF genes. We discuss how the duplication and truncation of DIV has been repeatedly recruited in the evolution of on/off switches. Components of the DIV-based regulatory network, and their close homologs, are present in a diversity of eukaryotes suggesting that their interaction may be ancestral to a large group of eukaryotes.