2.3 Elevated tropospheric O3 stress
Tropospheric O3 is a harmful secondary air pollutant
that negatively affects crop productivity through both direct oxidative
damage to plant cells, and through its role as a greenhouse gas and
subsequent contribution to global warming (Ainsworth, 2017).
Tropospheric O3 concentrations
([O3]) have more than doubled since pre-industrial
times (Monks et al., 2015) and while there is spatial heterogeneity in
global tropospheric [O3], O3 levels
remain high in major agricultural growing regions during the
crop-growing season (Ainsworth, 2017). It is estimated that on a global
scale, O3 pollution has led to a 2-15% decrease in
yield for crops such as wheat, rice, maize, and soybean (Avnery et al.,
2011; Van Dingenen et al., 2009).
Plant uptake of O3 occurs through both stomatal and
non-stomatal pathways (soil and cuticular deposition), with the primary
form of O3 entry occurring through the leaf stomata
(Ainsworth, 2017). Upon entry into the intercellular air space of leaves
O3 reacts to produce reactive oxygen species (ROS),
leading to cellular damage (Ahlfors et al., 2009; Grimes et al., 1983;
Heath, 1987). Perception, signaling and detoxification of
O3 and ROS has been well reviewed (Ainsworth et al.,
2012; Ainsworth, 2017; Vainonen & Kangasjarvi, 2015), and includes
altered redox balance, increases in cytosolic calcium, mitogen-activated
protein kinase (MAPK) signaling cascades, and altered expression of
genes involved in hormone and antioxidant metabolism, respiration, and
photosynthesis (Ainsworth, 2017).
The physiological response of plant responses to O3 and
their agronomic consequences have also been previously reviewed (for
list see Ainsworth, 2017; Montes et al., 2022), and demonstrate chronic
elevated [O3] decrease photosynthesis and stomatal
conductance in C3 plants, and increase rates of
respiration (Morgan et al., 2003; Ainsworth, 2008; Feng et al., 2008).
Additionally, decreased photosynthetic rates are associated with a
decrease in photosynthetic proteins, pigment, and nitrogen (N) content,
and increased rates of respiration are associated with changes in leaf
antioxidant balance (Dutilleul et al., 2003). These reductions in plant
primary metabolism can lead to reduction in plant growth rates, leaf
area and biomass accumulation (both aboveground and belowground) (Morgan
et al., 2003; Ainsworth, 2008; Feng et al., 2008).
As with other abiotic stresses, the timing of O3 stress
can play a role in the overall impact on plant productivity;
O3 can directly impact reproductive development in
plants (Black et al., 2000; Leisner & Ainsworth, 2012) and
O3 exposure during reproductive development can lead to
a greater reduction in photosynthesis than during vegetative development
in some plants (Morgan et al., 2003; Ainsworth, 2008; Feng et al.,
2008). Overall, O3 impacts plants at the community,
whole plant, leaf, and cellular level and can lead to reductions in crop
yield and overall biomass accumulation (Ainsworth et al., 2012). While
there is significant within-species variation in O3tolerance in crops (Ainsworth, 2017; Booker et al., 2009), future work
is needed to see successful gains in breeding and biotechnological
approaches to improving resiliency to O3 in crops.
2.4 Elevated atmospheric CO2
Anthropogenic CO2 emissions have increased the
atmospheric [CO2] since the beginning of the
industrial revolution, with the global concentration increasing from 340
ppm in 1980 to 417 ppm in February of 2022 (GML-NOAA, 2022). If
CO2 emissions are maintained, the Representative
Concentration Pathway model (RCP) 8.5 predicts that atmospheric
[CO2] could reach between 550-600 ppm by 2050 (IPCC,
2021). Therefore, it is important to understand the effects of elevated
CO2 on crop physiology, yield and its interaction with
other abiotic factors as well as biotic stresses such as crop diseases.
The effects of elevated CO2 at the crop, plant and
genetic level have been widely studied before (for review see Ainsworth
& Rogers, 2007; Ainsworth & Long, 2020) but a better understanding of
the interactive effects of CO2 with other abiotic and
biotic stress is needed.
As a substrate of photosynthesis, elevated concentrations of atmospheric
CO2 increase photosynthesis of C3 plants
between 20 to 45% by saturating Rubisco and decreasing photorespiration
(Ainsworth & Rogers, 2007; Leakey et al., 2009; Walker et al., 2016).
Of these, C3 legume crops such as soybean, peanut, and
peas (Pisum sativum ) have higher photosynthetic rates than other
C3 crops due to the benefits of biological nitrogen
fixation on plant N and sugar metabolic status (Ainsworth & Rogers,
2007; Sanz-Saez et al., 2015). In C4 plants, however,
elevated CO2 does not increase photosynthesis directly
as they already possess a CO2 concentration mechanism
that saturates Rubisco and avoids photorespiration (Leakey et al.,
2009). For that reason, C4 crops such as maize, sorghum
and other C4 grasses such as Panicum coloratumonly show higher photosynthetic rates when grown under elevated
CO2 when also exposed to drought stress. This is a
result of reduced transpiration that allows the crops to save more water
in the soil and maintain higher photosynthetic rates during drought
(Leakey et al., 2009).
The major function of stomata is to maximize CO2fixation while minimizing water loss. As atmospheric
[CO2] increase, the intercellular
CO2 concentration in C3 and
C4 plants increases as well, and therefore plants
respond by decreasing both stomatal aperture and stomatal density,
resulting in lower water loss at the leaf level (Leakey et al., 2009;
Ainsworth & Long, 2020). This decrease in stomatal conductance
translates to a decrease in canopy evapotranspiration that results in
increased soil moisture content (Leakey et al., 2009). In some cases,
however, elevated [CO2] stimulate leaf growth and
canopy expansion and therefore canopy transpiration is increased (Gray
et al., 2016; Parvin et al., 2019). These factors need to be taken in
account when studying the interaction with diseases as a reduced
stomatal conductance and number could limit the entrance of leaf
pathogens and reduce disease severity (Eastburn et al., 2011).
Under elevated [CO2], plants tend to produce more
sugars due to increased photosynthetic rates (Ainsworth et al., 2004).
Feedback inhibition occurs if plants are not able to distribute those
sugars from the sources (leaves) to the sink organs (roots, flowers
developing seeds) at the same pace that sugars are assimilated, which in
turn, inhibits the expression of photosynthetic genes and limits
photosynthesis (Ainsworth et al., 2004). This photosynthetic limitation
at elevated [CO2] produced by a sink limitation is
more common in crops that produce more leaves (sources) and not as many
seeds (sinks), as reproductive organs are stronger carbon (C) sinks.
This has been demonstrated in wheat, where cultivars with higher harvest
index (produce more seeds) were more responsive to elevated
[CO2] than cultivars that produced more vegetative
biomass (Aranjuelo et al., 2013). Additionally, this increase in
carbohydrate content is followed by a reduction in the assimilation of N
(Rubio-Asensio & Bloom, 2017; Bloom et al., 2020; Adavi & Shathee,
2021) that, combined, results in a dilution of the N content in all
plant tissues and an increase in the C/N ratio that could affect disease
growth (Ainsworth & Long, 2004).
Due to a reduction of the transpiration stream and the dilution effect
produced by an increase in carbohydrate concentration in seeds and
leaves, mineral concentrations tend to decrease at elevated
[CO2] (McGrath & Lobell, 2013; Myers et al., 2014;
Ebi & Loladze, 2019; Loladze et al., 2019; Ebi et al., 2021). The
decrease of micronutrients like iron (Fe), zinc (Zn), and selenium (Se)
is significant, as they are essential nutrients for human nutrition and
its deficiency in diets affects more than 2 billion people in the world
(Ebi & Loladze, 2019; Loladze et al., 2019; Ebi et al., 2021). This
decrease in nutrient concentration due to a reduced transpiration at
elevated [CO2] can be significant for other
nutrients that are important for the integrity of membranes and cell
walls such as silicone, calcium (Ca) and boron (B), as it could
facilitate the infection of some pathogens.
The stimulation of photosynthesis at elevated [CO2]
usually results in biomass and yield increases in C3plants (Bishop et al., 2014; Sanz-Saez et al., 2017; Hu et al., 2022).
The magnitude of the positive effect depends on the crop species and the
interactions between biotic and abiotic factors (Ainsworth & Long,
2020). However, genotypic variation in the biomass and yield response to
elevated [CO2] has been found in several crops under
controlled and open environments (Aranjuelo et al., 2013; Bishop et al.,
2014; Sanz-Saez et al., 2017). Additionally, under elevated
[CO2], leaf area is stimulated, and the canopy
closes earlier in the season and is denser than at ambient
[CO2] (Srinivasan et al., 2017; Sanz-Saez et al.,
2017). A canopy that closes earlier in the season and is denser could
produce a more humid microclimate that favors the appearance of
diseases.
CROSSTALK BETWEEN ABIOTIC AND BIOTIC STRESS
Plants respond to individual biotic or abiotic stresses or simultaneous
challenge by biotic and abiotic stresses in a complex and unique manner
at the physiological, transcriptional, and cellular levels (Suzuki et
al., 2014; Zhang et al., 2022). Common responses of plants to abiotic
stresses are stomatal closure, reduced photosynthesis, increased ROS
scavenging activity, reduced leaf growth, and increased root length, as
described above. In response to biotic stress, plants respond to
challenges by bacterial, fungal, and viral pathogens or nematodes in
different ways depending on the biotrophic or necrotrophic lifestyle of
pathogens. Some commonly observed responses to these biotic stresses
include stomata closure, reduced photosynthesis, production of ROS,
phytoalexin production, and local cell death. Overlap in the regulatory
networks that control plant responses to both abiotic stress, pathogen
recognition and defense therefore include ROS signaling, expression of
plant hormones, changes in redox status and ion flux, and changes in
cell wall integrity (Kissoudis et al., 2014; Rivero et al., 2022),
indicating crosstalk and convergence of mechanisms to combat general
stress (Walley et al., 2007; Atkinson & Urwin et al., 2012; Kissoudis
et al., 2014).
With climate change comes the higher likelihood that plants might be
challenged with simultaneous stressors in agricultural fields and
accompanied variable levels of pathogen pressure, as changes in the
growing environment (i.e., temperature, water availability) can affect
plant disease epidemics and other plant-microbe interactions (Rivero et
al., 2022). These combined stresses have the potential to pose an even
greater threat to global food security and climate resilience than each
stress alone (Rivero et al., 2022). Previous work has shown that
susceptibility to hemibiotrophic or necrotrophic pathogens is increased
under abiotic stress, while susceptibility to biotrophic pathogens is
reduced when combined with abiotic stress (Saijo & Loo, 2019).
Therefore, to engineer a more sustainable future food supply we need to
understand how biotic and abiotic stress combinations act in
combination. This includes understanding stress signaling crosstalk in
plant signaling, gene expression, metabolism, and development. Below we
summarize our current knowledge of crosstalk in signaling and plant
metabolic pathways that occurs when plants are exposed to combined
abiotic and biotic stresses. In the following section we outline
trade-offs between plant responses to combined biotic and abiotic stress
conditions with targets for future research efforts.