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.