Angiosperm ovules consist of three proximal-distal domains, the nucellus, chalaza and funiculus, each demarcated by developmental fate and specific gene expression. Mutation in three paralogous class III homeodomain leucine zipper (HD-ZIPIII) genes leads to aberrations in ovule integument development. Expression of WUSCHEL (WUS) is normally confined to the nucellar domain, but in this triple mutant expression expands into the chalaza. Micro-RNA induced suppression of this expansion partially suppresses the effects of the HD-ZIPIII mutations on ovule development implicating ectopic WUS expression as a component of the mutant phenotype. bell 1 (bel1) mutants produce aberrant structures in place of the integuments and WUS expresses ectopically in these structures. Combination of bel1 with the HD-ZIPIII triple mutant leads to a striking phenotype where ectopic ovules emerge from nodes of ectopic WUS expression along the funiculi of the primary ovules. The synergistic phenotype indicates that BEL1 and HD-ZIPIII genes act in at least partial independence in confining WUS expression to the nucellus and maintaining ovule morphology. The branching ovules of the mutant resemble branched ovules of some fossil gymnosperms implicating BEL1 and HD-ZIPIII genes as players in evolution of the unbranched ovule form in extant angiosperms.