Stomatal morphology and physiology explain varied sensitivity to abscisic acid across vascular plant lineages

Abstract

Abscisic acid (ABA) can induce rapid stomatal closure in seed plants, but the action of this hormone on the stomata of fern and lycophyte species remains equivocal. Here, ABA-induced stomatal closure, signaling components, guard cell K+ and Ca2+ fluxes, vacuolar and actin cytoskeleton dynamics, and the permeability coefficient of guard cell protoplasts (Pf) were analyzed in species spanning the diversity of vascular land plants including 11 seed plants, 6 ferns and one lycophyte. We found that all 11 seed plants exhibited ABA-induced stomatal closure, but the fern and lycophyte species did not. ABA-induced hydrogen peroxide elevation was observed in all species, but the signaling pathway downstream of nitric oxide production, including ion channel activation, was only observed in seed plants. In the angiosperm faba bean (Vicia faba), ABA application caused large vacuolar compartments to disaggregate, actin filaments to disintegrate into short fragments and Pf to increase. None of these changes was observed in the guard cells of the fern Matteuccia struthiopteris and lycophyte Selaginella moellendorffii treated with ABA, but a hypertonic osmotic solution did induce stomatal closure in fern and the lycophyte. Our results suggest that there is a major difference in the regulation of stomata between the fern and lycophyte plants and the seed plants. Importantly, these findings have uncovered the physiological and biophysical mechanisms that may have been responsible for the evolution of a stomatal response to ABA in the earliest seed plants.

Metabolism‐mediated mechanisms underpin the differential stomatal speediness regulation among ferns and angiosperms

“…On the other side, evidence suggests that hydraulic and osmotic mechanisms independent of ABA are the major drivers of stomatal closure in ferns (Brodribb & McAdam, 2011; Cardoso & McAdam, 2019; Cardoso et al, 2019; McAdam & Brodribb, 2012a, 2012b). Indeed, it was recently shown that ferns and lycophyte species lack ABA‐responsiveness but an osmotic‐mediated stomatal closure mechanism is likely found in these species (Gong et al, 2021). However, this study was performed using an extremely high concentration of sorbitol (800 mM).…”

Gaining or cutting SLAC: the evolution of plant guard cell signalling pathways

“…These results are consistent with previous findings of a lack of stomatal closure response to endogenous ABA levels in ferns [28,29], and the lack of stomatal phenotype for ABA-insensitive mutants of the C. richardii OST1 ortholog GAIA1 [31] in sharp contrast to the wilty phenotypes of angiosperm ABA biosynthesis and signalling mutants [49,[62][63][64]. In addition, a recent study showed a lack of ABAmediated K + efflux from the guard cells of fern and lycophyte species, further emphasising differences between the stomatal responses of seed plants and other vascular plant groups [65]. Together, these results support a passive model for stomatal closure in ferns [29], whereby guard cell turgor is dependent on leaf turgor rather than ABA-dependent activation of guard cell-expressed ion channels.…”

GABA: A Key Player in Drought Stress Resistance in Plants

“…Regulation of the stomatal pore aperture is a major factor in determining plant productivity and drought tolerance [ 11 , 12 , 13 , 14 , 15 ]. GABA-induced stomatal control has gained particular attention in recent years.…”