Chronic exposure to increasing background ozone impairs stomatal functioning in grassland species

Abstract

Two species found in temperate calcareous and mesotrophic grasslands (Dactylis glomerata and Leontodon hispidus) were exposed to eight ozone treatments spanning preindustrial to post-2100 regimes, and late-season effects on stomatal functioning were investigated. The plants were grown as a mixed community in 14 L containers and were exposed to ozone in ventilated solardomes (dome-shaped greenhouses) for 20 weeks from early May to late September 2007. Ozone exposures were based on O 3 concentrations from a nearby upland area, and provided the following seasonal 24 h means: 21.4, 39.9 (simulated ambient), 50.2, 59.4, 74.9, 83.3, 101.3 and 102.5 ppb. In both species, stomatal conductance of undamaged inner canopy leaves developing since a midseason cutback increased linearly with increasing background ozone concentration. Imposition of severe water stress by leaf excision indicated that increasing background ozone concentration decreased the ability of leaves to limit water loss, implying impaired stomatal control. The threshold ozone concentrations for these effects were 15-40 ppb above current ambient in upland UK, and were within the range of ozone concentrations anticipated for much of Europe by the latter part of this century. The potential mechanism behind the impaired stomatal functioning was investigated using a transpiration assay. Unlike for lower ozone treatments, apparently healthy green leaves of L. hispidus that had developed in the 101.3 ppb treatment did not close their stomata in response to 1.5 lM abscisic acid (ABA); indeed stomatal opening initially occurred in this treatment.Thus, ozone appears to be disrupting the ABA-induced signal transduction pathway for stomatal control thereby reducing the ability of plants to respond to drought. These results have potentially wide-reaching implications for the functioning of communities under global warming where periods of soil drying and episodes of high vapour pressure deficit are likely to be more severe.

Determinants of stomatal sluggishness in ozone-exposed deciduous tree species

“…3). Similar findings were reported in previous studies (e.g., Paoletti, 2005;Mills et al, 2009;Paoletti and Grulke, 2010;Hoshika et al, 2012a). Maier-Maercker (1989) suggested that such slower stomatal response might be explained by delignification of the guard cell and subsidiary cells as recorded in ozonated Picea abies.…”

“…In manna ash, such slower stomatal responses were considered as accelerated senescence in the cell physiological processes (Paoletti et al, 2009). Mills et al (2009) found that O 3 reduced stomatal sensitivity to ABA. Wilkinson and Davies (2010) suggested that the loss of stomatal response to ABA may be related to O 3 -induced ethylene emissions.…”

“…However, slower or less efficient stomatal control may occur, especially a weaker ability to close stomata, referred to as "O 3 -induced stomatal sluggishness" (Paoletti, 2005;Mills et al, 2009;Paoletti et al, 2009;Paoletti and Grulke, 2010;Hoshika et al, 2012aHoshika et al, , 2013aDumont et al, 2013). Sluggishness may occur because O 3 reduces stomatal sensitivity to abscisic acid (ABA) (Mills et al, 2009). This loss of stomatal response to ABA is related to O 3 -induced ethylene emission (Wilkinson and Davies, 2010).…”

Ozone impacts on vegetation in a nitrogen enriched and changing climate

“…However, several studies have shown that drought does 29 not always reduce O3 -induced damage to plants in sensitive species (e.g. Mills et al, 2009;30 McLaughlin et al, 2007a;Robinson et al, 1998;Wagg et al, 2012;Wilkinson andDavies, 2009, 31 2010), and that the genetic variability in O3 sensitivity may be related to the extent to which O3 32 reduces the sensitivity of stomatal closure to soil drying. Such effects have been attributed to 1 reduced response to drought signals such as abscisic acid in the presence of ozone-induced stress 2 ethylene emission (Mills et al, 2009;Wilkinson andDavies 2009, 2010).…”

“…Despite the often reported decline in stomatal conductance at elevated O3, 25 stimulation of stomatal opening (Mills et al, 2009) and the induction of stomatal sluggishness 26 (Paoletti and Grulke, 2010) have also been observed (discussed later). On the other hand, elevated 27 CO2 reduces stomatal conductance (Curtis and Wang, 1998;Drake et al, 1997;Kim et al, 2010;28 Morgan, 2003) and therefore the uptake of O3 and its damaging impacts on plants (Fiscus et al, 29 1997;Harmens et al, 2007;McKee et al, 1997).…”