Abscisic acid receptors functionally converge across 500 million years of land plant evolution

Abscisic acid (ABA) functions as a central regulator of dehydration responses in land plants. As such, ABA signaling was pivotal in facilitating the colonization of terrestrial habitats. The conserved ABA signal transduction module consists of 2C-type protein phosphatases (PP2Cs) and their ABA-triggered inhibitors, PYRABACTIN RESISTANCE 1-like proteins (PYLs). Recent evidence indicates that ABA perception emerged from a latent signaling pathway involving a constitutively PP2C-inhibiting PYL homolog. Consequently, ancestral ABA receptors exerted high background signaling, limiting the dynamic range of ABA-dependent signaling. In angiosperms, ABA receptor families are characteristically large and diverse and include a clade-specific subgroup whose members form homodimers, thereby assuming strict ABA dependency. Here, we show that ABA receptors in mosses originate from an independent expansion, giving rise to three subfamilies. Yeast two-hybrid and in vitro PP2C-inhibition assays indicate that moss PYLs feature low basal activities. However, size-exclusion chromatography and additional lines of evidence suggest that moss PYLs are predominantly monomeric. A combination of mutational analysis with biochemical and physiological assays reveals that the reduced basal activities of moss PYLs are achieved through unique sets of amino acid variations. Finally, introducing causal variations to dimeric receptors dramatically compromises their ABA responsiveness, suggesting that the two evolutionary trajectories are mutually exclusive. Hence, mosses appear to have evolved a parallel mechanism to mitigate the ancestrally high background signal of the core ABA perception apparatus. This convergence highlights the shared imperative of expanding the amplitude of a central, highly adaptive signaling pathway.