Exploding a myth: the capsule dehiscence mechanism and the function of pseudostomata in Sphagnum

Abstract

Summary• The nineteenth century air-gun explanation for explosive spore discharge in Sphagnum has never been tested experimentally. Similarly, the function of the numerous stomata ubiquitous in the capsule walls has never been investigated.• Both intact and pricked Sphagnum capsules, that were allowed to dry out, all dehisced over an 8-12 h period during which time the stomatal guard cells gradually collapsed and their potassium content, measured by X-ray microanalysis in a cryoscanning electron microscope, gradually increased. By contrast, guard cell potassium fell in water-stressed Arabidopsis.• The pricking experiments demonstrate that the air-gun notion for explosive spore discharge in Sphagnum is inaccurate; differential shrinkage of the capsule walls causes popping off the rigid operculum. The absence of evidence for a potassium-regulating mechanism in the stomatal guard cells and their gradual collapse before spore discharge indicates that their sole role is facilitation of sporophyte desiccation that ultimately leads to capsule dehiscence.• Our novel functional data on Sphagnum, when considered in relation to bryophyte phylogeny, suggest the possibility that stomata first appeared in land plants as structures that facilitated sporophyte drying out before spore discharge and only subsequently acquired their role in the regulation of gaseous exchange.

Fern and Lycophyte Guard Cells Do Not Respond to Endogenous Abscisic Acid

“…Such an assumption is far from certain, given that the earliest stomatalbearing land plants are characterized by few stomata with an irregular distribution, being frequently observed associated with reproductive structures (Paton and Pearce, 1957;Edwards, 1996). These stomata are rarely associated with air-filled substomatal spaces and have a debatable functional capacity (Edwards et al, 1998;Lucas and Renzaglia, 2002); current opinion favors a role of these stomata in nutrient transport (Boyce, 2008;Ligrone et al, 2012), aiding evaporative thermoregulation (Raven, 2002), and driving the desiccation of sporophytic tissues (Duckett et al, 2009;Ligrone et al, 2012). Furthermore, these early stomatalbearing land plants were ubiquitously confined to humid, wet environments (Edwards and Axe, 1992) and had very low rates of water loss, because of both internal anatomy and low stomatal densities (Konrad et al, 2000).…”

Evolution of the Stomatal Regulation of Plant Water Content

“…The one possible exception seems to be the basal moss genus Sphagnum where stomatal opening is likely a derived mechanism, being triggered by the loss of guard cell turgor (Duckett et al, 2009). This conspicuous inversion of the normal positive relationship between aperture and guard cell turgor pressure in the stomata of Sphagnum, however, is not apparent in more derived mosses or hornworts, suggesting that, like vascular plants, stomatal opening in basal species other than Sphagnum requires an increase in guard cell turgor (Wiggans, 1921;Heath, 1938).…”

An ATP Binding Cassette Transporter Is Required for Cuticular Wax Deposition and Desiccation Tolerance in the Moss Physcomitrella patens

“…The substantially thicker cuticle of the sporophyte capsule ( Figures 1D and 1E) may reflect the fact that the moss sporophyte is nutritionally depended on the female gametophores to which it is anchored, so a cuticle that is sufficiently permeable to allow gas exchange for photosynthesis is presumably not as important. Furthermore, the water status of the sporophyte capsule must be carefully controlled to ensure spore dispersal under the appropriate conditions (Duckett et al, 2009), which would be facilitated by the presence of a more robust cuticle. Taken together, these results suggest that the elaboration of the cuticle biosynthetic program in the sporophyte generation may have served as the foundation for producing a larger and more complex cuticle in the sporophyte-dominant, later-diverging land plants.…”