Evidence of SO Accumulation and Signaling in Biotic
Interactions
Several studies indicate that biotic stressors can induce the
accumulation of markers associated with elevated SO levels (Figure 3).
Oxylipin profiling in A. thaliana challenged with virulent and
avirulent strains of Pseudomonas syringae pv. tomato (Pst)
revealed that this bacterial pathogen induced 8-fold or higher increases
in the hydroxy fatty acids 10-HO-FA and 15-HO-FA (Grun et al., 2007).
These two HO-FA species are generated exclusively by non-enzymatic
peroxidation of fatty acids by SO, and are considered diagnostic
signatures of SO accumulation (Triantaphylidès et al., 2008).
Meta-analyses of publicly-available A. thaliana transcript
profiles also indicated that transcriptional responses to artificial
induction of SO by Rose Bengal or by the conditional flu mutation
overlaped with transcriptional responses to P. syringae , aP. syringae pv. pisi effector protein (AvrRPS4), bacterial
molecular patterns (flagellin22, elongation factor thermo unstable
EF-Tu), a fungal elicitor (chitin), the fungal pathogenPeronospora parasitica, and a molecular pattern associated with
pathogen-induced damage to plant cell walls (oligogalacturonides) (Mor
et al., 2014). This study identified a suite of over 100 genes that
overlap among these plant responses to pathogens and SO. In addition,
Zhang and coworkers reported that SO accumulation in Arabidopsis
upregulated 22 transcription factors associated with plant resistance to
pathogens (Zhang et al., 2014). While this overlap could be due to
convergence of different stress responses at some other signaling node,
in combination with oxylipin profiles it suggests the possibility that
SO could mediate plant responses to P. syringae and other
pathogens.
Two recent studies also implicate chloroplast retrograde signaling (and
possibly SO?) in plant-insect interactions. Mitra and coworkers (2021)
reported that applying oral secretions from the Egyptian cotton leafworm
(Spodoptera littoralis ) to mechanically-generated wounds onA. thaliana leaves induced accumulation of the SO-responsive
metabolite β-cyclocitral, and that induction of β-cyclocitral by this
simulated herbivory was higher than in response to wounding alone.
β-cyclocitral in turn downregulated the
2-C-methyl-D-erythritol-4-phosphate (MEP) pathway that generates
primarily metabolites for use in photosynthesis, and the authors
proposed that β-cyclocitral was part of a mechanism to downregulate
primary metabolism in favor of defense (Mitra et al., 2021). Artificial
treatment of plants with β -cyclocitral reduced S. littoralisgrowth, suggesting that this response helps fend off attack. Further
work is needed to determine whether 1) β-cyclocitral is induced by
actual as well as simulated caterpillar herbivory; 2) this metabolite is
generated by SO, other ROS, or by enzymatic routes (Havaux, 2020); and
3) insect performance is affected by manipulation of endogenous
β-cyclocitral and/or SO accumulation. Other evidence for induction of
chloroplast signaling by biotic stress comes from a plant interaction
with a piercing-sucking insect and an insect-transmitted virus. WhenA. thaliana was challenged with an aphid species
(Macrosiphum euphorbiae ) for which it is a non-host, it
accumulated methylerythritol cyclodiphosphate (MEcPP) (Zeng et al.,
2022). Zeng and coworkers (2022) also observed MEcPP accumulation in
response to Cucumber Mosaic Virus (CMV), a virus transmitted by the
green peach aphid Myzus persicae , although MEcPP was not measured
in response to Myzus persicae or other aphids that can infestA. thaliana . Like β-cyclocitral, MEcPP is another chloroplastic
retrograde signaling molecule that accumulates during high light stress
and is probably redox-regulated (Phua et al., 2021). Although the
presence of MEcPP does not directly implicate SO, it is indicative of
retrograde signaling, and associated with conditions that induce SO.
Together, these studies indicate that exposure to insects, salivary
elicitors, or insect-transmitted viruses can stimulate retrograde
signaling in the chloroplast, and suggest that SO may be involved in at
least some of these responses.