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).