3.3 Elevated [O3] and plant biotic stress interactions
Increased O3 exposure has shown to have secondary impacts on plants by altering the incidence of pests or pathogens, or by mediating the ability of a plant to respond to these biotic pressures (Fuhrer, 2009; Eastburn et al., 2011). Plants exposed to elevated O3 have been shown to be more prone to attacks by necrotrophic pathogens, root-rot fungi as well as insects such as bark beetles, while obligate biotrophic infections may be lessened on plants pre-exposed to elevated O3 (Karnosky et al., 2002; Sandermann, 2000; Tiedemann & Firsching, 2000). These differential effects have been shown to stem from physiological differences (such as reduced net photosynthesis and premature ripening and senescence) and corresponding gene expression changes in the plant (different signaling pathways involved in responding to necrotrophic vs. biotrophic pathogens). Conclusions drawn for specific pests and disease interactions with elevated O3 are controversial, however (Fuhrer, 2009), as responses can differ even within fungal genera. For example, wheat plants infected with leaf rust (Puccinia reconditaf. sp. tritici ) showed symptoms of O3 damage earlier and with higher severity compared to plants without rust infection (Tiedemann & Firsching, 2000), whereas O3-fumigated plants showed resistance towardsBipolaris in barley (Plazek et al. 2000).
Changes in the leaf surface topography, and in turn, chemical composition, in response to O3, result in alterations in leaf wettability and solute retention (Karnosky et al., 2002). These alterations can influence attachment of pathogens to the leaf surface. Leaf surface attachment and successful epiphytic colonization is a crucial step during pathogenesis of foliar bacterial pathogens (Lindow & Brandl 2003; Potnis et al., 2014). For example, studies involving the foliar bacterial pathogen P. glycinea on soybean exposed to elevated [O3] both pre- and post-inoculation showed reduced bacterial infection severity and a reduced number of lesions (Laurence & Wood, 1978), while there was no effect or protection against bacterial blight (X. phaseoli ) on white bean (P. vulgaris ) when plants were exposed to elevated [O3] (Temple & Bisessar, 1979). This indicates future work looking at O3 impacts on specific plant-pathogen systems is needed to obtain a comprehensive view of plant resilience to future climate.
At the molecular level, the signaling pathways altered by elevated [O3] can influence the plant defense-growth trade-off/dilemma that plants face when attached by the pathogen (Kangasjärvi et al., 1994; Eastburn et al. 2011). Plant defense signaling pathways in response to pathogen infection and elevated O3 have been shown to share components such as ROS production. The oxidative burst caused by elevated O3was also shown to affect antagonistic and synergistic interactions between JA, SA, ET, and ABA, all of which are plant growth regulators, as well as important components of the plant defense network against biotrophic and necrotrophic pathogens (Eastburn et al. 2011; Kangasjärvi et al., 1994). Plant exposure to O3 also increases the activity of several enzymes in the phenylpropanoid, flavonoid and lignin pathways, which play a role in plant defense (Kangasjärvi et al., 1994). Reaction of O3 with the plant apoplastic space and cell membrane causes increased production of linoleic acid (Mudd, 1998), and in turn biosynthesis of JA, which may attenuate SA-dependent hypersensitive response (HR) and cell death pathways in plants (Rao et al. 2000a,b). Suppression of SA-dependent HR would mean that disease resistance against pathogens would be compromised. Functional SA-signaling pathways are also required for O3-induced ET biosynthesis, which is also needed for induction of HR-like cell death (Rao et al., 2002). O3-induced ET biosynthesis is also linked to increased biosynthesis of ABA, which regulates both stomatal conductance in plants and sugar signaling (Ahlfors et al., 2004; Leon & Sheen, 2003). This crosstalk can lead to trade-offs in plant growth and defense, which may ultimately affect the plant’s ability to respond to biotic stresses.
3.4 Atmospheric elevated [CO2] and plant biotic stress interactions
As elevated [CO2] does not directly affect thein vitro growth of plant pathogens (Zhang et al., 2015), the observed interactions between disease and elevated [CO2] are due to the physiological changes that elevated CO2 exerts on plants and the consequences that this has on pathogen severity and incidence. The plant response to infection with different microorganisms (bacteria, fungi, and viruses) under elevated [CO2] can be very variable and depending on primary and secondary effects of elevated [CO2] on plants.
Elevated CO2 reduces stomatal density and aperture and therefore infectivity of different bacterial and fungal diseases that infect plants through stomata may be reduced (Ainsworth & Rogers, 2007; Eastburn et al., 2011; Li et al., 2015). In a growth chamber study investigating the interactions of P. syringae in tomato it was observed that under elevated [CO2] stomatal aperture was reduced approximately 30%, and the pathogen was not able to reverse stomatal closure to pre-infection levels, which is a strategy used by the pathogen in ambient [CO2] (Li et al., 2015). It is hypothesized that this defense against disease under elevated [CO2] is also due to a stimulation of the SA defense pathway that results in the production of nitric oxide that stimulates stomatal closure. The increased SA defense under elevated [CO2] has been demonstrated to reduce infection and severity of Tomato Mosaic Virus and P. syringae in tomatoes (Zhang et al., 2015). However, the JA defense pathway is not stimulated at elevated [CO2] and a disequilibrium between the SA and JA pathways produces an increase in incidence and severity of diseases that are controlled by the JA defense, such as B. cinerea (Zhang et al., 2015). This demonstrates the complexity of hormone signaling responses to the combined abiotic and biotic stress conditions and that more research is needed to understand the effects of elevated [CO2] on the plant defense system and the interaction with multiple diseases.
Additional work has shown the decrease in disease susceptibility in the field. A 3-year field experiment performed under elevated [CO2] conditions found the incidence of powdery mildew (Peronospora manshurica ) was reduced by 60% in soybean. It was hypothesized this was likely due to decreased stomatal conductance in soybean plants grown under elevated [CO2], lowering the pathogen’s ability to enter through the stomata. Additionally, the decrease in stomatal conductance may have led to lower transpiration and therefore decreased humidity in the canopy, which leads to less favorable conditions for mildew growth (Eastburn et al., 2010, 2011). Conversely, the incidence of brown spot (Septoria glycines ) and sudden death syndrome (Fusarium viguliforme ) were not affected by elevated [CO2] (Eastburn et al., 2010). This indicates that a reduction in stomatal conductance and transpiration in plants grown under elevated [CO2] may not always benefit the host in detriment of the pathogen.
Work done on rice blast fungus (Pyricularia oryzae ) found leaf lesions increased by 65% in plants grown in elevated [CO2], which was attributed to disruption in the leaf cuticle and cell wall (Cruz-Mirieles et al., 2021). Silicate accumulation in rice leaves increases cuticle strength and therefore resistance to rice blast (Kim et al., 2002; Rodrigues et al., 2004). Additionally, when plants are grown at elevated levels of CO2, plant transpiration is reduced due to lower stomatal conductance (Leakey et al., 2009) reducing the bulk of nutrients that reach the canopy (McGrath & Lobell, 2013). This decreases the amount of silicate in rice leaves debilitating the cuticles and cell walls which facilitates the infection of rice blast fungus (Kobayasi et al., 2006).
When considering the infection of pathogens that are carried by insect vectors, the physiological effects of elevated CO2 on plant growth may also impact the fitness of the insect vector. For example, aphids (Ropalosiphum padi ) are insect vectors for barley yellow dwarf virus (BYDV), which can decrease yield and quality up to 70% in infected wheat plants (Smith & Sward, 1982). As elevated CO2 increases the carbohydrate content and reduces the amino acid content of leaves and phloem sap (Ainsworth & Long, 2005; Trebicki et al., 2016), the growth and reproduction of aphids may be reduced as they need a higher proportion of N than C for proper development (Trebicki et al., 2016). In non-infected plants grown under elevated CO2, this has been demonstrated, as growth and reproduction of aphids is slower in comparison with plants grown under ambient [CO2]. However, when the plants are infected with BYDV, the quantity of amino acids in the phloem sap and the aphid’s gut was higher than non-infected plants. This would suggest that BYDV may cause metabolic changes in wheat that favor the growth and reproduction of the aphid under elevated CO2 (Trebicki et al., 2016). This has been further demonstrated in field experiments where wheat plants grown in elevated [CO2] in Australia have shown higher incidence of BYDV in a 4-year experiment (Trebicki et al., 2017).
It has been hypothesized that the higher virus incidence observed under elevated [CO2] could also be caused by a secondary effect of elevated CO2 over the plants and insects that facilitate virus transmission (Ainsworth & Long, 2020). As elevated CO2 decreases stomatal conductance and transpiration (Leakey et al., 2009), canopy temperature can increase by 1-2 °C at midday in comparison with the ambient CO2 plots (Bernacchi et al., 2007) which can increase aphid performance and therefore the spread viruses (O’Neill et al., 2011; Trebicki et al., 2017; Ainsworth & Long, 2020).
In this review we have shown with different examples that the disease effect on crops under elevated [CO2] depends on how elevated CO2 both directly and indirectly affects the plant and is also dependent on the type of pathogens and the mechanisms of infection and defense. Although the research on how the interaction between disease and elevated [CO2] affects plants has increased in the last 20 years, more information is necessary to evaluate how a CO2-enriched atmosphere will affect the plant-pathogen interactions. To do so, more research needs to be done to understand the interaction between different abiotic stresses such as drought and high temperature and plant pathogens under elevated [CO2].
TRADE-OFFS AND FEEDBACKS IN PLANT RESPONSES TO ABIOTIC AND BIOTIC STRESSES
Responding to multiple stresses is costly because plants need to balance efficient resource allocation between defense and growth, which may compromise plant productivity and ultimately yield. Increased resistance to pathogens can be accompanied by a decrease in plant fitness that decreases tolerance to both abiotic stress and ambient growth conditions (Huang et al., 2010; Todesco et al., 2010; Kissoudis et al., 2014). Plants have developed mechanisms that allow them to sense biotic/abiotic stresses and respond to them, minimizing damage while conserving valuable resources for growth and reproduction. Identifying genes that are involved in balancing a plant’s response to multiple stresses while restoring its fitness in growth is a challenging task for breeding programs focused on developing stress-tolerant plant varieties (Ashraf & Aisha, 2009; Fukuoka et al., 2015; Cohen & Leach, 2020).