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The adaptation of plants to land required multiple morphological innovations. Among these include a variety of lateral organs that are initiated from apical meristems, in which the mantainance of undifferentiated stem cells is regulated by the homeodomain WUSCHEL-RELATED (WOX) transcription factors. Expansion of the  WOX  gene family has been associated with whole genome duplication (WGD) events and postulated to have been pivotal to the evolution of morphological complexity in land plants. Previous studies have classified the  WOX  gene family into three superclades (e.g., the ancient clade, the intermediate clade, and the modern clade). In order to improve our understanding of the evolution of the  WOX  gene family, we surveyed the  WOX  gene sequences from 38 genomes and 440 transcriptomes spanning the Viridiplantae and Rhodophyta. The WOX phylogeny inferred from 1039 WOX proteins drawn from 267 species with improved support along the backbone of the phylogeny suggests that the plant-specific WOX family contains three ancient superclades, which we term Type 1 (T1WOX, the WOX10/13/14 clade), Type 2 (T2WOX, the WOX8/9 and WOX11/12 clades), and Type 3 (T3WOX, the WUS, WOX1/6, WOX2, WOX3, WOX4 and WOX5/7 clades). Divergence of the T1WOX and T2WOX superclades may predate the diversification of vascular plants. Synteny analysis suggests contribution of WGD to expansion of the  WOX  family. Promoter analysis finds that the capacity of the  WOX  genes to be regulated by the auxin and cytokinin signaling pathways may be deeply conserved in the Viridiplantae. This study improves our phylogenetic context for elucidating functional evolution of the  WOX  gene family, which has likely contributed to the morphological complexity of land plants.

Large-scale phylogenomic analysis suggests three ancient superclades of the WUSCHEL-RELATED HOMEOBOX transcription factor family in plants