3. DISCUSSION
With growing evidence that root zone warming induces systemic disease
resistance in tomato, this work aimed to decipher the molecular
mechanisms underlying this phenomenon. We have shown that RZW activates
immunity in tomato, increasing the expression of defense genes and PRRs,
along with the induction of ethylene and ROS. This activated immune
system, in turn, results in systemic disease resistance to both
biotrophic and necrotrophic pathogens, indicating that it is a mechanism
common to several biotic signaling pathways.
Interestingly, we found that warming-induced immunity relies on the SA
signaling pathway. Heating treatments were previously shown to affect SA
signaling (Arofatullah et al., 2018; Sato et al., 2003; Widiastuti et
al., 2013; Snyman and Cronjé, 2008).
Our work indicates that root zone warming treatments are most effective
in promoting disease resistance to Bc after a short recovery
period (Figure 3), though, interestingly, in the case of Xcvdisease resistance, different recovery periods had similar effects
(Figure 4). Perhaps this is due to the different nature of the
pathogens, with root-zone warming initially priming SA mediated pathways
(Figure 9), which are also required for Xcv resistance (Xu et
al., 2018), while the effect on attributes required for necrotrophic
pathogen resistance require a longer period of ”acclimation”.
Evidences of commonalities between heat stress and biotic stress
signaling pathways have been previously reported (Zhang and Sonnewald,
2017; Suzuki and Katano, 2018; Jacob et al., 2017). In particular, HSPs
have been demonstrated to be involved in the response to both heat and
biotic stressors (di Donato and Geisler, 2019; Yu et al., 2016).
Over-expression of heat shock proteins in plants has been proposed as
one of the potential strategies to combat heat stress. HSPs function as
molecular chaperons, are involved in correct protein folding, assembly,
translocation, degradation and they also provide stability to integral
proteins and cell membranes under heat stress (Boston et al., 1996).
HSPs reportedly serve chaperone functions in quality control of plant
defense PRRs (Nekrasov et al., 2009; Lee et al., 2009). Interestingly,
we found that several PRRs were induced by the same root zone warming
treatment that was sufficient to promote pathogen resistance (Figure
6b), supporting the notion that PRR alterations in response to wounding
or biotic cues can be sufficient to activate plant defense (Zhou et al.,
2020; Saijo et al., 2018).
Low-level induction of HSPs concurrent with induced resistance toBc , On and Xcv suggest that the same mechanisms
which exert abiotic stress tolerance also activate immune mechanisms in
tomato, as was previously suggested (di Donato and Geisler, 2019; Yu et
al., 2016; Zhang and Sonnewald, 2017). The activation of HSPs by
pathogenic processes demonstrates the common signaling pathways which
can underlie the plants’ response to several different types of
stresses, which, ideally, would be those manipulated in order to
generate resistance and agriculturally desirable cultivars in the face
of combinatorial stress created by climate change. Of note is that,
similar to what we found for root-zone warming induced immunity toBc , acquired thermo-tolerance also requires a short acclimation
period, after which plants become more resistant to subsequent heat
application (Baniwal et al., 2004; Charng et al., 2007) perhaps
indicating that conserved machinery may be important in both types of
stress.
Interestingly, transgenic tomato plants expressing the Arabidopsis NPR-I
gene developed enhanced heat tolerance in addition to varying levels of
resistance against several tomato pathogens, testifying to the
connection between heat tolerance and biotic resistance (Lin et al.,
2004). This also supports our results demonstrating that warming-induced
resistance relies on an intact SA pathway (Figure 9). In addition to
HSPs, ROS scavenging abilities were reported to be essential in both
heat and biotic resistance (Piterková et al., 2013;
Vallélian-Bindschedler et al., 1998; Suzuki and Katano, 2018), and thus,
ROS homeostasis may be another underlying common mechanism that might
explain why increased heat tolerance also affords induced immunity and
pathogen resistance. Our results demonstrate that ROS inducing
mechanisms are affected by root zone warming (Figure 6b).
The use of pesticides and chemicals in agriculture is hazardous to human
health and lacks environmental sustainability. From a farmer’s
perspective, any improvement that reduces the cost of chemical
application is desirable. Heat induced systemic disease resistance
represents an attractive strategy to aid in combatting pathogens, given
its economical and environmentally friendly nature. Further, when
combining different priming agents to potentiate plant immunity, our
results indicate that warming treatments could best be combined with
JA-pathway ISR inducers, to achieve combined effects by potentiating
different immunity pathways simultaneously. Our results suggest that
mechanisms which govern acclimation to changing ambient temperatures may
be exploited in agriculture to promote disease resistance. Further
research will elucidate whether a potential use of root zone warming as
an eco-friendly disease control agent in agricultural systems is
feasible.