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

Abstract

Recent results suggest that metabolism‐mediated stomatal closure mechanisms are important to regulate differentially the stomatal speediness between ferns and angiosperms. However, evidence directly linking mesophyll metabolism and the slower stomatal conductance (gs) in ferns is missing. Here, we investigated the effect of exogenous application of abscisic acid (ABA), sucrose and mannitol on stomatal kinetics and carried out a metabolic fingerprinting analysis of ferns and angiosperms leaves harvested throughout a diel course. Fern stomata did not respond to ABA in the time period analysed. No differences in the relative decrease in gs was observed between ferns and the angiosperm following provision of sucrose or mannitol. However, ferns have slower gs responses to these compounds than angiosperms. Metabolomics analysis highlights that ferns have a higher accumulation of secondary rather than primary metabolites throughout the diel course, with the opposite being observed in angiosperms. Our results indicate that metabolism‐mediated stomatal closure mechanisms underpin the differential stomatal speediness regulation among ferns and angiosperms, in which the slower stomatal closure in ferns is associated with the lack of ABA‐responsiveness, to a reduced capacity to respond to mesophyll‐derived sucrose and to a higher carbon allocation toward secondary metabolism, which likely modulates both photosynthesis‐gs and growth‐stress tolerance trade‐offs.

Maize GOLDEN2-LIKE proteins enhance drought tolerance in rice by promoting stomatal closure

“…4B ), which mimicked the effects of drought stress. Our finding is consistent with the previous study that suggested the fast stomatal closure requires a high ABA sensitivity ( Candido-Sobrinho et al 2022 ). Our results also implied that ZmGLKs may function in the ABA biosynthesis pathway, as indicated by the higher ABA accumulation ( Supplemental Fig.…”

“…This has been demonstrated by model simulations and experimental data that major C 4 crops are capable of more rapid stomatal closure compared to C 3 crops in response to water deficit, resulting in the high water use efficiency (WUE) ( McAusland et al 2016 ; Wang et al 2021 ; Ozeki et al 2022 ). Notably, previous studies have demonstrated that slower stomatal closure in ferns is associated with reduced responsiveness to ABA and sugars compared to angiosperms ( Lima et al 2019 ; Candido-Sobrinho et al 2022 ), while the rapid transport of ions and osmolytes between guard cells and subsidiary cells in grass species contributes to the fast stomatal movement ( Chen et al 2017 ). Rice plants overexpressing ZmGLK s have improved carbohydrate contents ( Li et al 2020 ), consistent with SlGLK gene expression in tomato plants ( Powell et al 2012 ; Nguyen et al 2014 ); this may contribute to rapid stomatal closure at the metabolic level.…”

Species‐specific stomatal ABA responses in juvenile ferns grown from spores

“…1b; see also details in the Materials and Methods section). In line with previous studies on mature ferns (Hõrak et al, 2017;Xiong & Flexas, 2020;Cândido-Sobrinho et al, 2022), stomatal conductance (g s ) and net photosynthesis rate (A net ) in juvenile ferns were generally low (Fig. 1c,d).…”

“…2c,e,g,h,j). This might explain why no ABA responses were previously found in shorter experiments (Cândido-Sobrinho et al, 2022).…”

Species-specific stomatal ABA responses in juvenile ferns grown from spores

“…1b; see also details in Materials and Methods). In line with previous studies on mature ferns (Hõrak et al ., 2017; Xiong & Flexas, 2020; Cândido-Sobrinho et al ., 2022), stomatal conductance ( g s ) and net photosynthesis rate ( A net ) in juvenile ferns were generally low (Fig. 1c, d,).…”