Stomatal Guard Cells Co-opted an Ancient ABA-Dependent Desiccation Survival System to Regulate Stomatal Closure

Abstract

During the transition from water to land, plants had to cope with the loss of water through transpiration, the inevitable result of photosynthetic CO2 fixation on land [1, 2]. Control of transpiration became possible through the development of a new cell type: guard cells, which form stomata. In vascular plants, stomatal regulation is mediated by the stress hormone ABA, which triggers the opening of the SnR kinase OST1-activated anion channel SLAC1 [3, 4]. To understand the evolution of this regulatory circuit, we cloned both ABA-signaling elements, SLAC1 and OST1, from a charophyte alga, a liverwort, and a moss, and functionally analyzed the channel-kinase interactions. We were able to show that the emergence of stomata in the last common ancestor of mosses and vascular plants coincided with the origin of SLAC1-type channels capable of using the ancient ABA drought signaling kinase OST1 for regulation of stomatal closure.

Evolution of the Stomatal Regulation of Plant Water Content

“…One or more of these requirements for ABA-driven stomatal responses does not occur in nonseed plants. In lycophytes and ferns, native SnRK2s are unable to activate native SLACs , while a functional SnRK2-SLAC pairing, albeit weak, observed in P. patens (Lind et al, 2015) is not specific to the guard cells Vesty et al, 2016) and likely plays a role in nitrate homeostasis. In well-studied angiosperms there is a potent pairing of native SnRK2s and SLACs that are specifically expressed in guard cells (Li and Assmann, 1996;Geiger et al, 2009;Fujii et al, 2011).…”

Stomatal Function across Temporal and Spatial Scales: Deep-Time Trends, Land-Atmosphere Coupling and Global Models

“…These studies hypothesize that, before the evolution of seed plants, stomatal control, particularly in response to water deficit, was largely hydropassive (referred to here as the passive origin model, after Brodribb and McAdam, 2011; also described as the gradualistic model in McAdam and Brodribb, 2012). This hypothesis has been rejected in a number of studies utilizing a variety of methods, including cross-species genetic complementation, bioinformatics, and leaf gasexchange measurements, which together suggest that active stomatal sensitivity to ABA and CO 2 are traits common to all major land plant divisions Ruszala et al, 2011;Lind et al, 2015;Franks and Britton-Harper, 2016;Cai et al, 2017;Chen et al, 2017).…”

“…Understanding and predicting larger scale carbon, water, and energy cycles requires accurate estimates of the leaf diffusive (stomatal) conductances to water vapor and CO 2 (g w and g c , respectively [definitions for these and other terms are given in Table I]) using stomatal conductance models. Despite considerable progress in the development and application of these models, theoretical questions remain about some of the most basic stomatal sensitivities to environmental variables, such as the response to CO 2 and water deficit (Brodribb and McAdam, 2011;Chater et al, 2011;Ruszala et al, 2011;Franks, 2013;Lind et al, 2015;Franks and Britton-Harper, 2016).…”

Fern Stomatal Responses to ABA and CO2 Depend on Species and Growth Conditions

“…Furthermore, the P. patens and Selaginella moellendorffii homologs of OPEN STOMATA1 (OST1), a SnRK-type kinase that participates in ABA-induced stomatal closure via phosphorylation of the central guard cell anion channel SLOW ANION CHANNEL1 (SLAC1) in Arabidopsis (Arabidopsis thaliana; Geiger et al, 2009;Lee et al, 2009;Vahisalu et al, 2010), complemented the ABA insensitivity of stomatal closure in the Arabidopsis ost1 mutant Ruszala et al, 2011). The P. patens deletion mutant that lacked OST1 had impaired ABA-induced stomatal closure , and P. patens OST1 and several other OST1-like SnRKs from different nonvascular plants could activate Arabidopsis SLAC1 in oocytes (Lind et al, 2015). These data indicate that the core stomatal ABA-signaling pathway is conserved in plants.…”