Symplesiomorphies in the WUSCHEL clade suggest that the last common ancestor of seed plants contained at least four independent stem cell niches

Evolutionary studies addressing plant architecture have uncovered several significant dichotomies between lower and higher land plant radiations, which are based on differences in meristem histology and function. Here, we assess the establishment of different stem cell niches during land plant evolution based on genes of the stem cell-promoting WUSCHEL (WUS) clade of the WOX (WUSCHEL-related homeobox) gene family. WOX gene orthology was addressed by phylogenetic analyses of full-length WOX protein sequences and cellular expression pattern studies indicate process homology. Gene amplifications in the WUS clade were present in the last common ancestor (LCA) of extant gymnosperms and angiosperms. Whereas the evolution of complex multicellular shoot and root meristems relates to members in the WUS/WOX5 sub-branch, the evolution of marginal and plate meristems or the vascular cambium is associated with gene duplications that gave rise to WOX3 and WOX4, respectively. A fourth WUS clade member, WOX2, was apparently recruited for apical cell fate specification during early embryogenesis. The evolution and functional interplay of WOX3 and WOX4 possibly promoted a novel mode of leaf development, and evolutionary adaptations in their activities have contributed to the great diversity in shape and architecture of leaves in seed plants.