What are the evolutionary origins of stomatal responses to abscisic acid in land plants?

Abstract

The evolution of active stomatal closure in response to leaf water deficit, mediated by the hormone abscisic acid (ABA), has been the subject of recent debate. Two different models for the timing of the evolution of this response recur in the literature. A single-step model for stomatal control suggests that stomata evolved active, ABAmediated control of stomatal aperture, when these structures first appeared, prior to the divergence of bryophyte and vascular plant lineages. In contrast, a gradualistic model for stomatal control proposes that the most basal vascular plant stomata responded passively to changes in leaf water status. This model suggests that active ABA-driven mechanisms for stomatal responses to water status instead evolved after the divergence of seed plants, culminating in the complex, ABA-mediated responses observed in modern angiosperms. Here we review the findings that form the basis for these two models, including recent work that provides critical molecular insights into resolving this intriguing debate, and find strong evidence to support a gradualistic model for stomatal evolution.

Reactive oxygen species signaling and stomatal movement in plant responses to drought stress and pathogen attack

“…Notably, the respiratory burst oxidase homologs (RBOHs) NADPH oxidases, and the core ABA signaling components, emerged at almost the same time within guard cells, in mosses during land plant evolution; these components are not found in algae (Umezawa et al ; Mittler et al ; Lind et al ; Sussmilch et al ). This pattern of emergence suggests that apoplastic ROS, guard cells and ABA signaling mechanism are the co‐evolutionary results of the adaptation of land plants to dry environmental conditions (Umezawa et al ; Mittler et al ; Lind et al ; Sussmilch et al ). However, the evolution of stomata also opened the door for pathogen invasion (Schroeder et al ; Melotto et al ).…”

Differential responses of stomatal kinetics and steady‐state conductance to abscisic acid in a fern: comparison with a gymnosperm and an angiosperm

“…Angiosperms regulate plant water status actively, with stomatal responses mediated by the ancient phytohormone, abscisic acid (ABA). A gradualistic model (Brodribb & McAdam, ; Sussmilch et al ., ) suggests that this metabolic (hydroactive) stomatal response to tissue water deficit evolved recently, after the divergence of spermatophytes (seed plants) from Monilophyta and Lycophyta (formerly ferns and fern allies) c . 400 million yr ago (Ma).…”

“…Angiosperms regulate plant water status actively, with stomatal responses mediated by the ancient phytohormone, abscisic acid (ABA). A gradualistic model (Brodribb & McAdam, 2011a;Sussmilch et al, 2017) suggests that this metabolic (hydroactive) stomatal response to tissue water deficit evolved recently, after the divergence of spermatophytes (seed plants) from Monilophyta and Lycophyta (formerly ferns and fern allies) c. 400 million yr ago (Ma). ABA-mediated stomatal responses to humidity and CO 2 in this model are considered to have developed even later (Brodribb et al, 2009;McAdam & Brodribb, 2014), after divergence of angiosperms from gymnosperms (c. 360 Ma; Pryer et al, 2004).…”

From reproduction to production, stomata are the master regulators

“…Foliar ABA levels can be significantly increased within 5–20 min of decreased air humidity in angiosperms (McAdam et al , ; McAdam et al , ), whereas in gymnosperms it takes hours of severe dehydration for ABA levels to reach those required for stomatal closure (McAdam and Brodribb, , ). One genetic explanation for this difference in speed is the presence of a dedicated short‐chain dehydrogenase/reductase (SDR) enzyme that is specific to the ABA biosynthesis pathway in angiosperms, ABA DEFICIENT 2 (ABA2) (Cheng et al , ; González‐Guzmán et al , ), and not represented in other plant lineages, which have only non‐specific SDR enzymes (Moummou et al , ; McAdam et al , ; Sussmilch et al , ). The observed slow rates of ABA synthesis in angiosperm aba2 mutants suggest that the non‐specific SDR enzymes can catalyse this step, but less efficiently than ABA2 enzymes (Wang et al , ; González‐Guzmán et al , ; McAdam et al , ).…”