Fig. 6: The multifunctional evolution of DAF/OAF-like genes in plants.

In the eudicot Arabidopsis, the DAF/OAF ancestor duplicated into three genes (DAF, OAF, DAFL2) through two duplication events and eventually evolved to divergent functions through subfunctionalization in regulating various flower development. OAF retains its functions in regulating carpel/ovule development, DAF retains its functions in regulating sepal/petal/anther/carpel development and DAFL2 retains its functions in regulating sepal/petal/carpel development from their DAF/OAF-like ancestor. OAF regulates ovule development through a miR847-OAF-CAD9 signaling pathway. OAF negatively regulates CAD9 activity to prevent the early developing (before stage 10) ovules from lignification whereas miR847 acts upstream of OAF to suppress OAF expression during the period of late stage (after stage 12) ovule development, resulting in the increased activity of CAD9 to promote the formation of lignin in the ovules and ensure the normal embryo and seed development. In contrast to OAF, DAF retains the functions in specifically regulating anther dehiscence through a DAF-DAD1-JA signaling pathway and retains putative functions in regulating sepal/petal development similar to DAFL2 and carpel development similar to OAF/DAFL2 from their DAF/OAF-like ancestor. In the monocot orchid (Orchidaceae), only one PaOAF gene was identified which likely evolved to retain most of the DAF/OAF ancestor’s functions. PaOAF maintains a conserved function similar to Arabidopsis OAF in regulating ovule development by preventing the early lignification of the developing ovules before 70 DAP. The decrease in PaOAF expression during late ovule development caused the formation of lignin and resulted in normal embryo and seed development. In OAF mutants and PaOAF-VIGS, precocious lignification of the ovules caused sequential defects in embryo/seed development. PaOAF may lose the function in regulating anther dehiscence as DAF due to evolutionary formation of the specific anther cap and pollinium structures in orchids. PaOAF may still have a function in regulating sepal/petal/carpel development in orchids, but this remains to be investigated.