A ligand-independent origin of abscisic acid perception

Abstract

Land plants are considered monophyletic, descending from a single successful colonization of land by an aquatic algal ancestor. The ability to survive dehydration to the point of desiccation is a key adaptive trait enabling terrestrialization. In extant land plants, desiccation tolerance depends on the action of the hormone abscisic acid (ABA) that acts through a receptor-signal transduction pathway comprising a PYRABACTIN RESISTANCE 1-like (PYL)–PROTEIN PHOSPHATASE 2C (PP2C)–SNF1-RELATED PROTEIN KINASE 2 (SnRK2) module. Early-diverging aeroterrestrial algae mount a dehydration response that is similar to that of land plants, but that does not depend on ABA: Although ABA synthesis is widespread among algal species, ABA-dependent responses are not detected, and algae lack an ABA-binding PYL homolog. This raises the key question of how ABA signaling arose in the earliest land plants. Here, we systematically characterized ABA receptor-like proteins from major land plant lineages, including a protein found in the algal sister lineage of land plants. We found that the algal PYL-homolog encoded by Zygnema circumcarinatum has basal, ligand-independent activity of PP2C repression, suggesting this to be an ancestral function. Similarly, a liverwort receptor possesses basal activity, but it is further activated by ABA. We propose that co-option of ABA to control a preexisting PP2C-SnRK2-dependent desiccation-tolerance pathway enabled transition from an all-or-nothing survival strategy to a hormone-modulated, competitive strategy by enabling continued growth of anatomically diversifying vascular plants in dehydrative conditions, enabling them to exploit their new environment more efficiently.

Abscisic acid dynamics, signaling, and functions in plants

“…Emergence of PYL receptors apparently occured before terrestrial occupation. The ancient ZcPYL8 encoded in Zygnema circumcarinatum cannot bind with ABA and possesses ABA‐independent inhibition of PP2Cs (Sun et al 2019). The PYL canonical ABA receptors have been reported only in land plants, suggesting that ABA signaling was critical for plants during the transition from an aquatic to a terrestrial environment (Lind et al 2015; Wang et al 2015a; Bowman et al 2017; Jahan et al 2019).…”

“…They also inhibit proline accumulation and suppress resistance responses to drought and cold stresses through suppressing SnRK2 activation (Bhaskara et al 2017; Ding et al 2019). Ancient PYL without ABA binding affinity has been reported in algae, while PP2Cs and SnRK2s from algae have conserved functions compared with those from higher plants (Lind et al 2015; de Vries et al 2018; Cheng et al 2019; Sun et al 2019).…”

Plant Secondary Metabolites as Defenses, Regulators, and Primary Metabolites: The Blurred Functional Trichotomy

“…Natural selection acts on these metabolic networks, resulting in the evolution of network topologies that maximize fitness. Over evolutionary time, these topologies likely include dynamic transitions between secondary metabolites and hormones, for instance (Malinovsky et al, 2017;Sun et al, 2019b). Overall, the functional integration of secondary metabolites at a given point in evolution is a likely consequence of the interaction between complex environments with highly connected plant metabolic networks.…”

Ties between Stress and Lipid Droplets Pre-date Seeds

“…Transcriptomic and genomic instigations [70,71] showed that several Zygnematophyceae encode a full homologous genetic chassis for what can be considered to be the bona fide module for ABA perception and signal transduction (ABA signaling is reviewed by Cutler et al [72]). Recent functional investigations revealed that the protein-protein interactions between these homologs operate as in land plants [73,74]. That said, these protein-protein interactions appear to act in an ABA-independent mannereven in Zygnematophyceae where a protein homologous to the receptor known from land plants is present [74].…”

“…Recent functional investigations revealed that the protein-protein interactions between these homologs operate as in land plants [73,74]. That said, these protein-protein interactions appear to act in an ABA-independent mannereven in Zygnematophyceae where a protein homologous to the receptor known from land plants is present [74]. What this means is that signaling circuits that are known to be triggered by ABA in land plants, and which respond in the algae upon desiccation, are more ancient; the regulatory role that ABA plays in these circuits likely emerged during plant terrestrialization [74].…”