Abstract
Ground-level ozone pollution is already decreasing global crop yields (from ∼2.2–5.5% for maize to 3.9–15% and 8.5–14% for wheat and soybean, respectively), to differing extents depending on genotype and environmental conditions, and this problem is predicted to escalate given climate change and increasing ozone precursor emissions in many areas. Here a summary is provided of how ozone pollution affects yield in a variety of crops, thus impacting global food security. Ozone causes visible injury symptoms to foliage; it induces early senescence and abscission of leaves; it can reduce stomatal aperture and thereby carbon uptake, and/or directly reduce photosynthetic carbon fixation; it can moderate biomass growth via carbon availability or more directly; it can decrease translocation of fixed carbon to edible plant parts (grains, fruits, pods, roots) due either to reduced availability at source, redirection to synthesis of chemical protectants, or reduced transport capabilities via phloem; decreased carbon transport to roots reduces nutrient and water uptake and affects anchorage; ozone can moderate or bring forward flowering and induce pollen sterility; it induces ovule and/or grain abortion; and finally it reduces the ability of some genotypes to withstand other stresses such as drought, high vapour pressure deficit, and high photon flux density via effects on stomatal control. This latter point is emphasized here, given predictions that atmospheric conditions conducive to drought formation that also give rise to intense precursor emission events will become more severe over the coming decades.
Introduction
Although essential in the upper atmosphere, gaseous ozone is also present in the lower atmosphere where it is a pollutant formed from the effects of sunlight on vehicular and industrial emissions. In the northern hemisphere, mean background ozone concentrations have risen from ∼10–15 ppb in pre-industrial times to the current level of 35 ppb (Vingarzin, 2004; see Fuhrer, 2009). Effects of this now phytotoxic concentration of ozone on crop yields have been studied extensively in the last 30 years, and several syntheses of these findings exist (e.g. Mills et al., 2007; Emberson et al., 2009; Feng et al., 2009; Pleijel, 2011). On the whole, wheat and soybean are particularly sensitive; potato, rice and maize are moderately sensitive; whilst barley has been found to be ozone resistant, with South Asian varieties of food staples being at least as sensitive as those grown in the USA and Europe (Emberson et al., 2009). Global models indicate that ozone reduced crop yields by a larger margin than the reduction attributable to climate change in the year 2000 (Van Dingenen et al., 2009; The Royal Society, 2008). Estimated reductions of global yields ranged from 2.2–5.5% for maize, to 3.9–15% and 8.5–14% for wheat and soybean, respectively (Avnery, 2011a). Economic losses for Europe in 2000, based on ozone effects on 23 crops, were estimated to be 6.7 billion Euros (Holland et al., 2006); and global crop production losses in the same year were estimated to have been 79–121 Mt worth US$11–18 billion (Avnery, 2011a). In a recent meta-analysis of 30 experiments representing nine countries in North America, Europe, and Asia, and spanning 18 wheat genotypes, average wheat yield improvement by removing ozone from the air entering open-topped chambers in the field was 9% (Pleijel, 2011).
Crop plants are often irrigated, or planted to coincide with adequate rainfall, which, as well as maximizing growth, induces the opening of stomatal pores in the leaf surface for gas exchange for photosynthesis. It is through these open pores that ozone gains entry to the plant. Yield is reduced both by cumulative background ozone effects on several aspects of growth and productivity over the course of the growing season, and by the often more immediately visible effects induced by discrete ozone ‘episodes’ or concentration peaks frequently superimposed on the background level in spring and summer months. Such episodes, lasting for several days and covering scores to thousands of square kilometres, occur when local climatic conditions conducive to ozone formation and persistence coincide with significant precursor emissions. Ozone concentrations are elevated to peaks of >60 ppb each day, with concentrations as high as 150–180 ppb being recorded in years such as 2006 in many areas of the Mediterranean Basin and central Europe (EAA, 2006).
The visible injury symptoms manifest as chlorotic or necrotic patches on the leaf surface in the form of stippling, which can coalesce to form larger injured areas, and these leaves often senesce and abscise early. Other visible yield impediments stem from reductions in general plant biomass growth, and reduced flowering. Less visible ozone effects include reduced grain/pod filling, and/or ovule and grain abortion in later developmental stages (see below). Thus, in field crops, such as some varieties of wheat, rice, maize, bean, soybean, oil seed rape, and sorghum, ozone reduces grain size, grain weight, grain nutritional quality, and/or grain number (e.g. Mulholland et al., 1998; Biswas and Jiang, 2011). In pod crops such as bean, pods are smaller, or of a reduced number. In tuber crops such as potato, tuber size rather than tuber number is reduced. Crop quality, for example protein or oil content of pods or grains, can also be affected (see Fuhrer, 2009).
Furthermore, ground-level background ozone concentrations are still increasing (by an average of 0.3 ppb per year), as a result of increased human activity, and this is predicted to reduce global yields still further, particularly given that climate change will exacerbate ozone formation in some regions (The Royal Society, 2008; see Fuhrer, 2009). Avnery et al. (2011b) predict that global yield losses in the year 2030 will be worth up to US$35 billion, with losses of 4–26% expected for wheat, 9.5–19% for soybean, and 2.5–8% for maize dependent on the scenario used. The frequency of episodes is also predicted to increase, and this may be especially severe in Southern Asia and in Africa (The Royal Society, 2008). Not only does this threaten agricultural sustainability in general, but research shows that current global models may have underestimated the potential impact of future ozone concentrations on crop damage, because ambient ozone concentrations can prevent stomata of some sensitive genotypes from closing as fully as usual in response to stresses such as drought and high vapour pressure deficit (VPD; see below). This is relevant to the vulnerability of ‘local’ food supply in an unpredictable climate.
Here a description is given of how ozone is reducing our food supply, with emphasis on its effects in a variable and changing environment.
Mechanisms for ozone-induced yield reduction
Whilst some genotypes may be more vulnerable to one in particular of the mechanisms described in this section, it is most likely that several of these interact to curtail productivity, and that these interactions will be altered by the environment (e.g. Guidi et al., 2010; Biswas and Jiang, 2011). It should also be noted that the effects of ozone described in this section refer in the main to those known to occur in relatively unstressed plants. However, ozone effects on plants experiencing additional abiotic stresses, such as a lack of soil moisture, can be very different, and this is described in a separate section below. This difference is highlighted in particular in the case of ozone-induced control of stomatal aperture via hormonal signalling (ethylene). Indeed the same signal (increased ethylene accumulation) can either close stomata or open them, depending on the extent of other co-occuring stresses, and this will impact on yield.
Effects of ozone on carbon gain and carbon use that impact on crop yield.
Effects of ozone on carbon gain and carbon use that impact on crop yield.
Visible injury
Inside leaves, ozone interacts with the contents of the substomatal apoplast and with adjoining cell membranes and walls, to form reactive oxygen species (ROS) such as hydrogen peroxide, superoxide, and hydroxyl radicals (reviewed in Fiscus et al., 2005). This induces a chain reaction whereby further oxidative bursts occur within adjoining cells. ROS that remain unscavenged can cause a variety of foliar injury symptoms such as interveinal necrosis and early senescence and abscission, as described above. Such symptoms have been confirmed on 27 crop species growing in farmers’ fields across Europe (Mills et al., 2011), and are caused by free radical induction of unregulated and/or programmed cell death. Evidence is growing that these processes are in part mediated via the plant hormones ethylene, jasmonic acid, and salicylic acid (for reviews, see Fiscus et al., 2005; Kangasjärvi et al., 2005).
Visible injuries are one way in which ozone can eventually reduce yield, even if they only occur at early vegetative stages of crop growth. Leaf injury, senescence, and/or abscission directly reduce yields in leafy biomass crops such as alfalfa, lettuce, spinach, chicory, and cabbage. However, in non-foliage crops, visible injuries also affect yield (e.g. of grain and pod crops) by reducing the amount of leaf area per se, or the amount of healthy green leaf area available for carbon fixation for further biomass growth and/or grain filling (e.g. Mulholland et al., 1998; McKee and Long, 2001; see below).
Carbon acquisition, transport, and use
Figure 1 depicts ozone impacts on carbon gain and use affecting yield. Many yield-depressive ozone effects on biomass growth and grain filling are only measurable post-harvest, as effects are often cumulative across the full growing season (Wittig et al., 2007, 2009; Singh and Agrawal, 2010). Farmers may be unaware that such crop losses are caused by ozone. Such reductions in biomass growth have traditionally been linked to ozone-induced reductions in biochemical photosynthetic carbon fixation processes (reviewed in Fiscus et al., 2005). Ozone-induced stomatal closure has also been implicated (Torsethaugen et al., 1999; McAinsh et al., 2002; Overmeyer et al., 2008) in reducing carbon availability. Mechanisms for ozone-induced reductions in stomatal aperture have been described in depth in Overmyer et al. (2008). Furthermore, logically, direct reductions of shoot and root cellular expansion via ozone-induced ethylene generation can be implied (see Wilkinson and Davies, 2010; and below).
Reductions in whole plant biomass induce yield reductions in grain and pod crops by reducing the availability of leaf surface area to fix and provide carbon (C) for reproductive parts (Fig. 1). The figure depicts the various different contributions to the reduced availability of photosynthate for grains or pods, stemming from (i) reduced photosynthetic efficiencies; (ii) reduced stomatal conductance (gs); (iii) reduced green foliage biomass (e.g. McKee and Long, 2001) as a result of reduced new growth, shortening of the life cycle, injury, senescence, and abscission; (iv) reduced root biomass; or (v) reduced partitioning of available C to grains/pods in favour of synthesis of protective chemicals (Betzelberger et al., 2010; see below), or as a result of reduced phloem translocation efficiency (e.g. McKee and Long, 2001; Grantz, 2006).
The ozone-induced reduction in root biomass (which indirectly reduces yield) is understood to arise either from a reduction in C translocation from the shoot to the root via the phloem (either due to reduced availability at source or as a result of the blockage of phloem sieve plates with callose tissue, e.g. Grantz, 2006; Wittig et al., 2009; Asensi-Fabado et al., 2010) and/or from an effect of ozone on the concentrations of the plant hormones such as ethylene that control root growth (suggested in Wilkinson and Davies, 2010). Ozone-induced reductions in root biomass impact indirectly on the shoot and therefore on grain/pod production via a reduction in the ability of the plant to take up the nutrients and water required to sustain growth and yield. In addition, root biomass crops such as potato, onion, and carrot are directly vulnerable to reductions in root biomass (e.g. Asensi-Fabado et al., 2010).
Effects on reproductive parts
There are direct effects of ozone to reduce bud formation and flowering, to cause pollen sterility, and to induce flower, ovule, or grain injury and abortion, which are discussed in detail by Black et al. (2000; 2007) and Mulholland et al. (1998). Some of these effects may potentially occur through plant hormones such as ethylene (see below).
Growth stage vulnerability
Some studies suggest that ozone exposure in the vegetative phase is most yield depressive, whilst others describe that the reproductive stage is most vulnerable (e.g. Heagle, 1989; Mulholland et al., 1998), with, for example, the sensitivity of seed crop yield to ozone having been shown to be greatest during the period between flowering and seed maturity in some studies (e.g. Lee et al., 1988; Pleijel et al., 1998). However, Singh and Agrawal (2010) showed that the presence of ethylene diurea (EDU; a compound that can be used to protect plants against ozone damage via an unknown mechanism, that is used as an experimental tool) was necessary at all stages of wheat crop production, in order to prevent ozone-induced yield penalties, implying that ozone effects on yield were more cumulative. Vulnerability at a given key stage of crop development, or vulnerability that arises more cumulatively, is likely to be environmentally and/or genotypically determined. For example, indeterminate species in particular can compensate for ozone effects at the vegetative stage and even for discrete ozone episodes occurring within the reproductive phase (e.g. Black et al., 2007).
The basis of genotypic sensitivity to ozone
Crop species differ widely in their susceptibility to ozone, and lists of species/genotypes that fall into sensitive and resistant categories can be accessed elsewhere (e.g. Heagle, 1989; Mills et al., 2007). There is a wide intra- as well as interspecific variation in plant sensitivity to ozone (e.g. Maggs and Ashmore, 1998; Biswas et al., 2008; Brosche et al., 2010), and recent studies have identified some genetic loci associated with ozone resistance and/or susceptibility in wheat and rice (e.g. Ainsworth et al., 2008; Frei et al., 2010), amongst other crops.
However, it must be noted that the definition of crop ‘sensitivity’ to ozone can be rather imprecise. For example, crops can be sensitive to ozone regarding the visible injury symptoms seen on foliage at early growth stages, but, apart from in foliage crops (such as leafy salad crops and alfalfa) this does not necessarily give rise to an equivalent negative impact on grain/pod/fruit yield in fully developed crops. In fact, Sawada and Kohno (2010) have shown in rice, and Picchi et al. (2010) in wheat, that cultivars in which grain yields are most impacted by ozone are those which showed the least visible injury symptoms to foliage. Picchi et al. (2010) proposed that this may be related to genotypic variation in the extent of the stomatal closure response to ozone. Cultivars where ozone closes stomata could be said to be relatively ozone insensitive in reference to visible injury, as the ozone ‘dose’ will be reduced subsequent to this closure, preventing further foliar injury. However, prolonged stomatal closure reduces C fixation, and thereby the amount of assimilate available for grains/pods/leaves; thus, these cultivars may be more ‘sensitive’ to ozone in terms of yield.
Nevertheless, there is scope for the impacts of increased ozone concentrations on food security to be mitigated by choosing/developing genotypes with greater ozone tolerance with respect to yield. Genotypic variability in sensitivity to ozone can arise through several mechanisms.
The extent of detoxification
Some of the genotypic variability in ozone tolerance has been attributed to levels of detoxifying antioxidants [ascorbic acid (AsA), glutathione, tocopherol, carotenoids, flavonoids, and phenolics] and/or ROS scavengers (superoxide dismutase, catalase, or peroxidases) present in and/or generated by certain genotypes in response to ozone stress (Blokhina et al., 2003; Conklin and Barth, 2004; Eltayeb et al., 2007). Naturally occurring genetic variation in ozone tolerance of visible leaf injury in rice was dissected into two distinct quantitative trait loci (QTLs; Frei et al., 2008). These were developed into two chromosome segment substitution lines (Frei et al., 2010). Tolerance in one of the lines was related to lower expression of genes encoding ascorbic oxidase, and AsA catabolism was proposed to be reduced such that this line had higher concentrations of apoplastic AsA when exposed to ozone. Genes related to ethylene and jasmonic acid metabolism were also differentially regulated between the tolerant and sensitive lines.
Changes in stomatal conductance
The extent to which ozone-induced stomatal closure occurs will influence carbon gain and yield in crop plants (Fig. 1), and this has been shown to be genotype dependent (Wittig and Ainsworth, 2007;,Overmyer et al., 2008; Biswas and Jiang, 2011). However, inherent rates of gs prior to the onset of ozone stress have also been linked to variability of susceptibility of wheat and rice varieties to ozone, because they control ozone flux to the plant interior (Brosche et al., 2010). In general, modern wheat cultivars released in the last two decades are the most vulnerable, and these also display the highest gs (Biswas et al., 2008; but see Biswas and Jiang, 2011), because breeding for high yield has a functional link to increased stomatal CO2 influx. This hypothesis is supported by our findings in clover clones: Fig. 2 shows that an ozone-sensitive clover accession (NC-S) has a higher level of gs in drying soil than its ozone-resistant counterpart (NC-R; originally selected by Heagle et al., 1994). Importantly, this difference is particularly dramatic in the presence of ozone, and it is proposed that ozone may prevent full stomatal closure under drought (see below). Poor stomatal closure under drought implies both excessive water loss and inwardly directed ozone flux, giving rise to poor plant performance (Wilkinson and Davies, 2009, 2010). Whilst clover is an important pasture crop, it is expected that this mechanism will also dictate some of the varietal sensitivity to ozone in human staples. For example, it was recently demonstrated that genotypic variation in the sensitivity of stomatal aperture to external factors may be linked to yield tolerance to ozone in wheat (Biswas and Jiang, 2011; see below).
Stomatal conductance (gs) in sensitive (NC-S) and resistant (NC-R) clover accessions in drying soil (50% full capacity, assessed via daily weighing of evapo-transpirational water loss) in the presence (70 ppb) and absence (15 ppb) of elevated ozone concentrations; temperature maintained at 21–23 °C; photon flux density 6–700 μmol m−2 s−1 during a 14 h photoperiod. Ozone exposure was carried out in 1.0 m3 boxes inside a greenhouse. Measurements were initiated 10 d after transfer to ozone treatments; plants were purchased as root plugs and allowed to re-grow in a greenhouse for 2 weeks prior to ozone treatment initiation. gs was measured weekly at 10:00 h using a porometer (AP4, Delta-T Devices, Cambridge, UK); n=12–16, two gs measurements for each of 6–8 plants; SE and significant differences (*P < 0.05, **P < 0.01, Student’s t-test) between NC-R and NC-S are shown. (This figure is available in colour at JXB online.)
Stomatal conductance (gs) in sensitive (NC-S) and resistant (NC-R) clover accessions in drying soil (50% full capacity, assessed via daily weighing of evapo-transpirational water loss) in the presence (70 ppb) and absence (15 ppb) of elevated ozone concentrations; temperature maintained at 21–23 °C; photon flux density 6–700 μmol m−2 s−1 during a 14 h photoperiod. Ozone exposure was carried out in 1.0 m3 boxes inside a greenhouse. Measurements were initiated 10 d after transfer to ozone treatments; plants were purchased as root plugs and allowed to re-grow in a greenhouse for 2 weeks prior to ozone treatment initiation. gs was measured weekly at 10:00 h using a porometer (AP4, Delta-T Devices, Cambridge, UK); n=12–16, two gs measurements for each of 6–8 plants; SE and significant differences (*P < 0.05, **P < 0.01, Student’s t-test) between NC-R and NC-S are shown. (This figure is available in colour at JXB online.)
Changes in photosynthetic capacity
(Flowers et al. 2007; snap bean), (Biswas and Jiang 2011; wheat), (Betzelburger et al. 2010; soybean), and (Pang et al. 2009; rice), amongst others, have determined that genetic variability in ozone susceptibility in terms of yield is related to direct ozone effects on biochemical photosynthetic processes. However, it is important to note that genetic variability in photosynthetic capacity will, to some extent, depend on genetic variability in both gs-related parameters and the efficiency of ozone detoxification, which both contribute to the final amount of ROS present at the photosynthetic apparatus.
The extent of ethylene production
The production of the gaseous plant hormone ethylene from shoot tissues is frequently observed in plants exposed to ozone pollution (see Kangasjärvi et al., 2005; Wilkinson and Davies, 2009, 2010), including many crop species (see Wilkinson and Davies, 2009), and the extent of ozone-induced ethylene production has been shown to be commensurate with visible leaf injury and abscission (e.g. Mehlhorn et al., 1991; Tamaoki et al., 2003; Overmyer, 2008). Ozone sensitivity in terms of leaf injury is greater in ethylene-overproducing Arabidopsis mutants (see Kangasjärvi et al., 2005) than in ethylene-insensitive mutants (Overmyer et al., 2008). Recently ethylene accumulation has also been associated with stomatal closure in general (i.e. in unpolluted plants) (see Wilkinson and Davies, 2009, 2010), as well as being correlated with genetic variability in the extent of ozone-induced stomatal closure (Kangasjärvi et al., 2005). It has also been shown to be involved in ozone-induced disruption of the plant’s defence mechanisms against abiotic stresses such as drought, by altering the sensitivity of stomata to a second plant hormone, abscisic acid (ABA; Wilkinson and Davies, 2009, 2010; see below). It is predicted that genotypic variability in ethylene production of human staples will also determine yield responses to ozone, because (i) there are many data demonstrating variable ethylene generation by crop plants in response to ozone (see above); and (ii) outside of ozone biology, ethylene is also known to play a role in controlling leaf and root growth, in regulating carbon gain and water loss through stomata, in carbon partitioning to grains, and in grain abortion (see below).
Ozone by environment interactions
There is a great deal of variability in injury, yield, growth, and stomatal responses to ozone (e.g. Wittig et al., 2007, 2009), some as a result of inherent genetic variability as described above, and/or some that arises as a result of variable growth conditions. Interactions between ozone stress and atmospheric CO2 concentrations have been reviewed elsewhere (e.g. Long et al., 2005). Here the fact that ozone episodes frequently co-occur with climatic conditions that also induce soil drying is highlighted.
It is widely understood that drought-induced stomatal closure will limit ozone uptake, thereby mitigating ozone-induced crop yield losses (e.g. Fagnano et al., 2009; Fuhrer, 2009). However, several studies have established that drought is not always protective in the presence of ozone concentrations in the ambient range (see Wilkinson and Davies, 2009, 2010; Biswas and Jiang, 2011), and it is shown here that some genetic variability in ozone sensitivity may be related to the extent to which ozone reduces the sensitivity of stomatal closure to soil drying (Fig. 2). Paoletti and Grulke (2010) also describe that stomata open and close less sensitively in response to changes in light intensity, and Biswas and Jiang (2011) very recently demonstrated that faster stomatal control in response to changing light intensity occurred in ozone-stressed plants of a more ozone-tolerant primitive tetraploid wheat species than in those of a less tolerant recently released genotype of hexaploid wheat. However, stomatal control became slower in the tetraploid species when ozone stress was combined with drought, and the primitive species lost ozone tolerance.
It has been shown that in drying soil, or when leaves are detached from the plant and allowed to dry out, stomata of some species close much less sensitively in ozone-polluted air (Mills et al., 2009; Wilkinson and Davies, 2009, 2010; Figs 2, 3). This effect will reduce the protective effect of drought-induced stomatal closure on the ozone dose that these plants receive, and on the regulation of plant water loss (e.g. McLaughlin et al., 2007), and therefore increase vulnerability to the drought episode (particularly when combined with a reduced root biomass; Wittig et al., 2009), with secondary impacts on leaf water potential and xylem cavitation likely. It is predicted that this will eventually cause secondary reductions in growth and yield, and/or increased injury, abscission, senescence, and death (Wilkinson and Davies, 2009, 2010), particularly if the vulnerable plants begin to experience additional/subsequent stresses such as wind, biotic attack, high light/VPD, or flood/storm conditions. Recent data (in preparation) describe a growing number of species, including some crops (notably Phaseolus vulgaris), that exhibit ozone-induced reductions in the stomatal closing response in either the presence or absence of soil drying. Below is described the potential mechanism behind these effects, and behind the linked ozone effect whereby stomata also close less sensitively in response to other stresses such as high salinity, light, and VPD (e.g. Robinson et al., 1998; Paoletti and Grulke, 2010; Biswas and Jiang, 2011). The authors speculate on how genetically widespread these effects might be, thus exploring their consequences for food security.
Effect of ozone concentration (control=15 ppb; + ozone=70 ppb) on the response of the pasture forb Leontodon hispidus stomatal conductance (gs) to soil drying. Re-calculated from Wilkinson and Davies (2009). Significant differences (*P < 0.05, **P < 0.01, Student’s t-test) between well-watered (WW) and droughted (DD) treatments are shown. Reproduced by kind permission of Wiley-Blackwell Publishing. (This figure is available in colour at JXB online.)
Effect of ozone concentration (control=15 ppb; + ozone=70 ppb) on the response of the pasture forb Leontodon hispidus stomatal conductance (gs) to soil drying. Re-calculated from Wilkinson and Davies (2009). Significant differences (*P < 0.05, **P < 0.01, Student’s t-test) between well-watered (WW) and droughted (DD) treatments are shown. Reproduced by kind permission of Wiley-Blackwell Publishing. (This figure is available in colour at JXB online.)
Ozone-induced disruption of plant signalling
The concentration of ABA in plant tissues usually increases linearly with soil drying. Generally stomata close and leaves grow more slowly in response to ABA sent upwards from the roots, reducing the loss of valuable water to the air (for reviews, see Davies and Zhang, 1991; Wilkinson and Davies, 2002; Tardieu et al., 2010). ABA also moderates stomatal aperture and leaf growth in response to other stresses such as high VPD, high salinity, and temperature extremes. Reports of Ozone effects on ABA concentration differ; it has been shown that ozone increases ABA concentrations in some genotypes, but that it decreases it or has no effect on it in others (see Wilkinson and Davies, 2009). The sensitivity of guard cells, leaf cells, and/or cells of reproductive organs to a given concentration of ABA can also be altered by the aerial environment. In some genotypes ozone increases plant calcium concentrations and this is associated with ozone-induced stomatal closure and reduced C fixation, possibly by increasing stomatal sensitivity to ABA (McAinsh et al., 2002). Alternatively or in addition, it is proposed that the implications of another recently defined effect of ozone, to reduce the responsiveness of stomata to ABA signalling (Wilkinson and Davies, 2009, 2010), could have as yet unexplored and serious consequences for food security, via its effect to increase gaseous ethylene production.
It has long been known that ozone increases the generation of ethylene from the leaves of sensitive plants (see above). Outside of ozone science, ethylene has traditionally been regarded as a shoot growth inhibitor and a promoter of ripening, senescence, and abscission (Abeles et al., 1992; Morgan and Drew, 1998). However, evidence has also recently been emerging for a role for ethylene in stomatal movements in the unpolluted plant (Desikan et al., 2006; Tanaka et al., 2007). This directed our investigations to show (Wilkinson and Davies, 2009) that an ozone-induced up-regulation of ethylene was responsible for the observed ozone-induced reduction in stomatal sensitivity to ABA, drought, and other closing stimuli described above (Figs 2, 3). A ‘cartoon’ of the mechanism by which ozone disrupts the stomatal response to ABA via ethylene is shown in Fig. 4. It is proposed that this may occur in response to any stress that produces ABA (or increases its access to xylem transport pathways) such as high VPD/temperature, high salinity, high light stress, or nutrient deficiency (Wilkinson and Davies, 2002; Rossel et al., 2006; Wilkinson and Hartung, 2009).
Model describing effects of ozone-induced ethylene production on ABA-induced stomatal closure. Under stresses such as soil drying (and high photon flux density, high vapour pressure deficit) ABA is up-regulated, and it closes stomata so that leaves retain water. However, in some sensitive genotypes, ozone-induced ethylene causes stomatal guard cells to lose their sensitivity to ABA such that stomatal pores remain more open. Plants will take up more ozone and lose more water than they would have done in the absence of ozone.
Model describing effects of ozone-induced ethylene production on ABA-induced stomatal closure. Under stresses such as soil drying (and high photon flux density, high vapour pressure deficit) ABA is up-regulated, and it closes stomata so that leaves retain water. However, in some sensitive genotypes, ozone-induced ethylene causes stomatal guard cells to lose their sensitivity to ABA such that stomatal pores remain more open. Plants will take up more ozone and lose more water than they would have done in the absence of ozone.
It has been predicted (Wilkinson and Davies, 2009, 2010; Wilkinson and Hartung, 2009) that many crop plants (in addition to P. vulgaris) will be susceptible to ozone via disruption of the stomatal signalling mechanism in this way, by searching the literature for those in which ozone is known to up-regulate ethylene. These include varieties of pea and pinto bean (Mehlhorn et al., 1991), potato (Sinn et al., 2004), tomato (Bae et al., 1996), snap bean (Elagoz and Manning, 2005), and some wheat and rice cultivars (e.g. Tiwari et al., 2005); and for those in which stomatal responses to the environment are known to be ‘sluggish’, for example snap bean (Paoletti and Grulke, 2010). Recently Biswas and Jiang (2011) showed differential stomatal control in wheat species under combined ozone and drought stress, although it was difficult to implicate this effect directly in yield differences.
In addition to its effects on senescence, abscission, and stomatal closure, it has long been known that ethylene can directly reduce shoot growth and root growth in non-polluted plants (Abeles et al., 1992; Morgan and Drew, 1997; Pierik et al., 2007; Wilkinson and Davies, 2010). It has been proposed (Wilkinson and Davies, 2010) that ozone also reduces leaf and root biomass via the up-regulation of ethylene production in ozone-sensitive species, in addition to or instead of the general reduction in carbon fixation which has traditionally been assumed to be the basis for ozone-induced reductions in plant biomass growth. It is likely that ethylene also has a more direct impact on grain yield in response to ozone stress. A clear link between ethylene and yield susceptibility to heat stress has been demonstrated in certain wheat genotype classes (Hays et al., 2007). Yang et al. (2006) also demonstrated that higher ABA/ethylene ratios were associated with superior grain quality and higher grain filling rates (Fig. 5). The importance of the biology of stress ethylene in the regulation of grain filling and yield in rice is already recognized (e.g. Naik and Mohapatra, 2000). It seems reasonable to assume that ozone-induced ethylene will have similarly direct detrimental effects on grain yields and quality. This remains to be tested and will generate valuable knowledge related to mitigating ozone effects on yield.
Relationships between grain-filling rate and concentrations of ABA (a), ethylene (b), and the ratio of ABA to 1-aminocyclopropane-1-carboxylic acid (ACC) (c) in superior (filled symbols) and inferior (open symbols) grains of wheat (cvs Yangmai 6 and Yangmai 11) during linear grain growth. Treatments were well watered (WW), moderately soil dried (MD), and severely soil dried (SD). Reproduced from Yang et al. (2006) by kind permission of Wiley-Blackwell Publishing.
Relationships between grain-filling rate and concentrations of ABA (a), ethylene (b), and the ratio of ABA to 1-aminocyclopropane-1-carboxylic acid (ACC) (c) in superior (filled symbols) and inferior (open symbols) grains of wheat (cvs Yangmai 6 and Yangmai 11) during linear grain growth. Treatments were well watered (WW), moderately soil dried (MD), and severely soil dried (SD). Reproduced from Yang et al. (2006) by kind permission of Wiley-Blackwell Publishing.
Implications for food security
There is clear evidence that the effects of ozone pollution described here are already occurring in many areas of the world [e.g. Europe (Mills et al., 2011); SE Asia (Emberson et al., 2009)]. Furthering our understanding of the mechanisms by which ozone impacts on crop species, including how ozone interferes with hormonal signalling in response to a variable environment, may help to develop new ways of protecting food crops from the current and increasing threat from ozone. Since the highest ozone concentrations are predicted to occur in those areas of the world where the population is increasing most rapidly (The Royal Society, 2008), and where water is likely to be most scarce (Bates et al., 2008), there are urgent needs for global cooperation in reducing ozone precursor emissions, development of management methods for protecting crops from ozone in the field under variable environments, and selecting and breeding for new ozone-tolerant varieties of our most important staple food crops.
We wish to thank Defra for financial contributions to this study (Contracts AQ0816 and AQ0815).
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