Adaptive Significance of Intracellular SO Accumulation and
Signaling in Biotic Interactions
If biotic stressors can induce intracellular SO or other components of
SO-mediated chloroplast signaling, the next important question is
whether these responses contribute to resistance or susceptibility to
biotic stress. When oxylipin profiles were compared in A.
thaliana plants challenged with virulent and avirulent strains of
Pst, 12-HO-FAs accumulated more rapidly in the incompatible
interaction, suggesting a correlation with resistance (Grun et al.,
2007). However, levels of 10- and 15-HO-FAs were not reported in this
experiment, and the role of SO in this response is unclear because
12-HO-FAs can result from the action of free radicals as well as SO.
Other studies have utilized mutants and/or treatments that induce SO to
explore the influence of this ROS on pathogen resistance. In theflu mutant, induction of SO by a L:D:L shift also triggered
accumulation of salicylic acid and expression ofPathogensis-Related Protein 1 (PR1 ) (Ochsenbein et al.,
2006). Salicylic acid, which is synthesized in the chloroplast, mediates
systemic acquired resistance (SAR) to P. syringae and many other
biotic attackers, and PR1 is a highly conserved marker of SAR
that contributes to multiple forms of disease resistance (Breen et al.,
2017). Zhang and coworkers (2014) further reported that subjecting
wild-type A. thaliana to a pre-treatment (a brief combined
exposure to low temperature and light stress) that induced SO-mediated
adaptation to subsequent high light exposure also upregulated PR1expression and reduced infection by a virulent Pst strain. PR1induction was absent in the ex1/ex2 mutant, and bacterial growth
on pre-treated ex1/ex2 was higher than on pretreated wild-type
plants. These results suggest that activation of EX1 -dependent SO
signaling triggers salicylate-mediated resistance to the hemi-biotropic
bacterial pathogen P. syringae .
Conversely, EX1 -signaling contributes to the susceptibility ofA. thaliana to tenuazonic acid, a non-host-specific toxin
produced by the necrotrophic fungus Alternaria alternata .
Although A. thaliana is not a host for A. alternata(Narusaka et al. 2005), it forms lesions in response to tenuazonic acid,
a virulence factor that facilitates the infection of host plants by
inducing cell death. The toxin disrupts the electron transport chain at
PSII and is expected to promote the generation of SO (Chen et al.,
2015). Compared to wild-type, the ex1ex2 mutant displays less
bleaching and transcriptional reprogramming in response to tenuazonic
acid treatment (Chen et al., 2015). This suggests that at least some of
the effects of this toxin are mediated through SO signaling, although SO
accumulation, cell death, and fungal growth were not directly measured.
Jasmonic acid contributes to non-host resistance to A. alternatain A. thaliana (Narusaka et al., 2005), and many plant pathogens
are thought to capitalize on cross-talk between salicylate- and
jasmonate signaling to promote virulence (Hou. & Tsuda, 2022). Thus, it
is possible that in response to artificially high doses of tenuazonic
acid, EX1-mediated induction of salicylate signaling could suppress
jasmonate-dependent defenses. However, it is important to note that
neither phytohormone was measured in this interaction, and that putative
SO accumulation is in some cases accompanied by jasmonic acid induction
(Przybyla et al., 2008; Mor et al. 2014). Moreover, because Arabidopsis
is a non-host, it is not possible to correlate alternations in host
signaling with changes in the extent of fungal infection. Further
studies are therefore needed to unravel the roles of SO and EX1 in the
interactions between necrotrophic fungi and host- and non-host plants.
Information about the influence of SO signaling on the outcomes of
plant-insect interactions is also limited. Mitra and coworkers (2021)
reported that exogenous application of β-cyclocitral to A.
thaliana decreased growth of the Egyptian cotton leafworm on foliage.
This suggests that signaling between the chloroplast and the nucleus can
trigger herbivore defenses, and may help balance resource allocation
between primary metabolism and defense. However, further work is needed
to confirm that this retrograde signaling is induced by real herbivory,
and to determine if it involves SO. While the piercing-sucking insectM. euphorbiae on a non-host (A. thaliana ) induces the
chloroplast signal MEcPP and the defense signaling molecules pipecolic
acid and N-hydroxy-pipecolic acid (Zeng et al., 2022), the adaptive
significance of this response is also unclear. Do MEcPP, pipecolic acid,
and/or N-hydroxy-pipecolic acid contribute to non-host resistance, and
is SO involved? Would similar or different responses be observed in a
compatible interaction with other aphid species such as M.
persicae or Brevicoryne brassicae that can successfully colonizeA. thaliana ? These questions remain unresolved, and even less is
known about the potential role of SO in response to other herbivores.