The need for speed: fast stomatal closure requires a high
ABA sensitivity
The fast stomatal responses of angiosperms confers a better capacity to
respond to variations in environmental cues and thus provided a great
competitive advantage to this group of plants during land plant
colonization (Raven 2014). Despite the fact that the mechanisms by which
stomatal speediness is regulated are unclear (Lawson & Vialet-Chabrand
2018), especially among different phylogenetic groups, our results
strengthen the hypothesis that the slower fern stomatal response is
associated to a reduced capacity to respond to ABA (Brodribb & McAdam
2011; McAdam & Brodribb 2012; Cardoso et al. 2019). This idea is
supported by the results in which exogenous application of ABA rapidly
reduced g s in the angiosperm, whilst fern stomata
did not respond to this phytohormone in the time period analysed. It is
important to emphasize, however, that ferns stomata requires longer time
to respond to stomatal closure stimulus such as dark and high
CO2 concentration (Franks & Britton-Harper 2016; Limaet al. 2019). Thus, we cannot currently conclude that the stomata
of the ferns investigated here lack ABA responsiveness.
Interestingly, the stomata of the ferns used here responded to exogenous
application of sucrose and mannitol, and to changes in the
CO2 concentration and during the light-to-dark
transition. Furthermore, our results revealed that the diel course ofg s is similar between ferns and angiosperms in
relative terms, with a maximum g s observed in the
initial period of the day, as typically observed under tropical
conditions (Antunes et al. 2012, 2017). This result indicates
that fern stomata is able to respond to the natural circadian rhythm,
which is controlled by a complex regulatory network associated to
changes in environmental cues such as temperature, air humidity, VPD,
CO2 concentration and light quality and quantity
(Gardner et al. 2006; Graf et al. 2010; Shalit-Kanehet al. 2018). Taken together, these results strengthen the idea
that fern stomata are responsive to environmental cues, although the
velocity of these responses are much lower than those observed in
angiosperms (Franks & Britton-Harper 2016). Given the discrepancy
between ferns stomatal responses to ABA and sucrose, this suggests that
ferns first acquired ABA-independent mechanisms for the regulation of
stomatal speediness. In the next section, we discuss how
mesophyll-derived metabolites may contribute to explaining the slower
stomatal responses found in ferns and how fern stomata can respond to
environmental cues such as darkness and high CO2concentration with no or at least reduced ABA sensitivity.