Evolution and divergence of the role of plant ethylene receptor-related histidine kinases in abscisic acid signaling

Plant responses to the water environment are mediated by ethylene (submergence response) and abscisic acid (ABA, drought response). Ethylene is perceived by a family of histidine kinase receptors (ETR-HKs), which regulate the activity of the downstream B3 Raf-like (RAF) kinase CONSTITUTIVE TRIPLE RESPONSE1 (CTR1) in an ethylene-dependent manner. We previously demonstrated in the moss Physcomitrium patens that SNF1-related protein kinase 2 (SnRK2), an essential kinase in osmostress responses in land plants, is activated by the B3-RAF kinase ARK, which is also regulated by ETR-HKs in an ABA- and osmostress-dependent manner. Whether this regulatory mechanism is evolutionarily conserved in land plants remains unknown. We demonstrate through a cross-species complementation assay that ETR-HKs from a terrestrial alga, bryophytes, and a lycophyte, but not those from angiosperms, retain the ability to activate ARK/SnRK2-mediated ABA signaling in the moss. This suggests that the role of ETR-HKs in ABA signaling was ancestral but lost in seed plants. The γ-loop in the C-terminal receiver domain is crucially involved in this specification of ETR-HK function.