Silicon deposition on guard cells increases stomatal sensitivity as mediated by K⁺ efflux and consequently reduces stomatal conductance

Abstract

Silicon (Si) has been widely reported to improve plant resistance to water stress via various mechanisms including cuticular Si deposition to reduce leaf transpiration. However, there is limited understanding of the effects of Si on stomatal physiology, including the underlying mechanisms and implications for resistance to water stress. We grew tall fescue (Festuca arundinacea Schreb. cv. Fortuna) hydroponically, with or without Si, and treated half of the plants with 20% polyethylene glycol to impose physiological drought (osmotic stress). Scanning electron microscopy in conjunction with X‐ray mapping found that Si was deposited on stomatal guard cells and as a sub‐cuticular layer in Si‐treated plants. Plants grown in Si had a 28% reduction in stomatal conductance and a 23% reduction in cuticular conductance. When abscisic acid was applied exogenously to epidermal leaf peels to promote stomatal closure, Si plants had 19% lower stomatal aperture compared to control plants (i.e. increased stomatal sensitivity) and an increased efflux of guard cell K+ ions. However, the changes in stomatal physiology with Si were not substantial enough to improve water stress resistance, as shown by a lack of significant effect of Si on water potential, growth, photosynthesis and water‐use efficiency. Our findings suggest a novel underlying mechanism for reduced stomatal conductance with Si application; specifically, that Si deposition on stomatal guard cells promotes greater stomatal sensitivity as mediated by guard cell K+ efflux.

Reciprocal Effects of Silicon Supply and Endophytes on Silicon Accumulation and Epichloë Colonization in Grasses

“…Moreover, morphological changes in hosts as a result of endophyte infection have resulted in, for instance, greater number of vascular bundles in perennial ryegrass (Franco et al, 2020). In line with this, Si has been reported in high concentrations both in the vascular bundles of perennial ryegrass (Dinsdale et al, 1979) and in tall fescue (Vandegeer et al, 2020). Thus, indirect morphological changes in hosts as a result of endophyte infection might further increase Si in host tissues.…”

Silicon in the Soil–Plant Continuum: Intricate Feedback Mechanisms within Ecosystems

“…Silicon in the cell wall is also involved in regulating stomatal movement and conductance, hence regulating water loss through stomata [ 193 , 242 , 243 , 244 ]. The sub-cuticular Si layer, which has long been suggested to play a role in water loss reduction [ 198 , 245 ], was recently found to reduce water loss from the cuticle by as much as 23% [ 246 ] (but see [ 242 ], who found no effect on water loss from the cuticle). Although most leaf surface water loss takes place through stomata [ 247 ], this 23% reduction can be significant.…”

Those in glass houses

“…With the water potential of the guard cell reduced, it rapidly deflates and closes the stomata. The increased ABA sensitivity demonstrated by Vandegeer et al (2021) had tangible repercussions on stomatal physiology, as the stomata of silicon‐treated plants closed significantly quicker and to a greater extent than their control counterparts when exposed to endogenous ABA.

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“…Higher plants too can benefit from this protective cladding, as silica deposited in the tissues of a wide variety of plants has been linked to enhanced resistance to bacterial and fungal infection, as well as increased tolerance to abiotic stresses such as metal toxicity and drought. In this issue of Physiologia Plantarum , Vandegeer et al (2021) investigated the mechanisms by which silicon deposited in the cells of tall fescue (Festuca arundinacea) altered the physiology of water transport, revealing applications for enhancing drought tolerance in this economically important pasture grass species.…”

“…In light of this, Vandegeer et al (2021) used a combination of structural and physiological analyses to gain a mechanistic understanding of the way that silicon supplemented to tall fescue grasses reduces osmotic stress. First, scanning electron microscopy and X‐ray mapping revealed a layer of silicon to be deposited below the cuticle—a waxy film composed of lipids and hydrocarbons that is secreted by and surrounds the leaf epidermis (Figure 1).…”