Yufei Sun, Ben Harpazi,  Akila Wijerathna-Yapa, Ebe Merilo, Jan de Vries, Daphna Michaeli, Maayan Gal, Andrew C. Cuming, Hannes Kollist, and Assaf Mosquna

PNAS December 3, 2019 116 (49) 24892-24899

Significance

Synthesis of abscisic acid (ABA) and proteins required for its downstream signaling are ancient and found in aquatic algae, but these primitive plants do not respond to ABA and lack ABA receptors. The present work traces the evolution of ABA as an allosteric regulatory switch. We found that ancient PYRABACTIN RESISTANCE 1’s homolog proteins have constitutive ABA-independent phosphatase-binding activity that, in land plants, has gradually evolved into an ABA-activated receptor. We propose that ABA-mediated fine-tuning of the preexisting signaling cascade was a key evolutionary novelty that aided these plants in their conquest of land.

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.

See https://www.pnas.org/content/116/49/24892

Figure 1:

Evolution of ABA receptors indicates an increase in ABA dependency as a result of reduction of basal activity. Recombinant 6×His-Sumo-ZcPYL8 (A), 6×His-MpPYL1 (B), PpPYL1, PpPYL3 (C), SmPYL1-5 (D), PYR1, PYL1-6, PYL8, PYL10, MBP-PYL9, and MBP-PYL11 (E) were expressed in E. coli, purified, and used in PP2C activity assays with 6×His-PP2C (ZcABI1, MpABI1, PpABI1A, or HAB1). Reactions were performed with 0.5 μM 6×His-PP2C and varying concentrations of PYL (0, 0.5, 1.0, 2.0 μM) in the absence (green) or presence (orange) of 10 μM ABA. PP2C activity is expressed as percentage of activity of PP2C in the absence of receptor. Graphs plot average values from 3 technical repeats, and error bars indicate SD. Results shown were reproduced with 3 independent protein purifications. Numbers of receptors encoded by corresponding species are shown in green circles. The phylogenetic tree of plant lineages was built according to Bowman et al. (20). The length of the branches does not indicate evolutionary dating. The inserted box depicts the dynamic response range of receptor activity. The numbers on the bar show the range of receptor activity from low at the left (without ABA) to high at the right (saturated with ABA). ZcPYL8 have no activity range. All of the values were captured at 1:2 PP2C:PYL ratio. Plant icons are not to scale.