Appearance and elaboration of the ethylene receptor family during land plant evolution

Ethylene is perceived following binding to endoplasmic reticulum-localized receptors, which in Arabidopsis thaliana, include ETR1, ERS1, EIN4, ETR2, and ERS2. These receptors fall into two subfamilies based on conservation of features within their histidine kinase domain. Subfamily 1 contains ETR1 and ERS1 whereas subfamily 2 contains EIN4, ETR2, and ERS2. Because ethylene receptors are found only in plants, this raises questions of when each receptor evolved. Here it is shown that subfamily 1 receptors encoded by a multigene family are present in all charophytes examined, these being most homologous to ETR1 based on their evolutionary relationship as well as containing histidine kinase and receiver domains. In charophytes and Physcomitrella patens, one or more gene family members contain the intron characteristic of subfamily 2 genes, indicating the first step in subfamily 2 receptor evolution. ERS1 homologs appear in basal angiosperm species after Amborella trichopoda and, in some early and basal angiosperm species and monocots in general, it is the only subfamily 1 receptor present. Distinct EIN4 and ETR2 homologs appear only in core eudicots and ERS2 homologs appear only in the Brassicaceae, suggesting it is the most recent receptor to evolve. These findings show that a subfamily 1 receptor had evolved and a subfamily 2 receptor had begun to evolve in plants prior to the colonization of land and only these two existed up to the appearance of the first basal angiosperm. The appearance of ERS2 in the Brassicaceae suggests ongoing evolution of the ethylene receptor family.