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.