SO Production by Photosensitizers in Plant Biotic Interactions
The earliest work to suggest a role for SO in plant biotic interactions was focused on Type II phototoxins found in plants and fungi. Phototoxins, also called photosensitizers, are compounds whose toxicity is dependent upon the absorption of light energy. Whereas Type I phototoxins act by generating free radicals, Type II compounds generate SO; energy absorbed from light is transferred from the excited Type II photosensitizer to ground state triplet oxygen, which causes the unpaired electrons to shift to opposite spin states, significantly increasing the reactivity of the oxygen molecule (Baptista et al., 2017). In plants, Type II phototoxins can act as phytoalexins—defensive plant secondary metabolites that are induced by biotic stress—and phytoanticipins, chemical defenses that are produced constitutively (Flors & Nonell, 2006). The most extensively studied examples are furanocoumarins and phenalenones, which can have activities against phytopathogenic fungi, bacteria, nematodes, and herbivorous insects.
Phototoxic furanocoumarins are common in the epidermis of species in the Umbelliferae, and Rutaceae, and in plants such as wild parsley or citrus they are a source of phytophotodermatitis—light-dependent skin irritation in humans (Nguyen et al., 2020). Thus, it is logical to hypothesize that they may function as an anti-herbivore defense. The linear furanocoumarin xanthotoxin has known toxicity to the southern fall armyworm (Spodoptera aridania Cramer), and this toxicity was enhanced when artificial diet containing xanthotoxin was treated with ultra-violet (UV) light, which promotes SO production by phytoalexins (Berenbaum,1978). Furthermore, when plants from Umbelliferae and Rutaceae were treated with UV light, they generated a high flux of SO in the stable gas-phase on the leaf surface that was projected to be sufficient to damage herbivores on the plant (Berenbaum & Larson, 1988). Together, these results suggest that gaseous SO produced by phototoxins at the leaf surface contribute to plant defenses against herbivores, possibly through direct toxicity to the pest.
Another group of Type II photosensitizing phytoalexins, the phenalenones, have light-dependent, SO-mediated toxicity against root-knot nematodes (Song et al., 2017) and the fungal pathogenFusarium oxysporum (Lazzaro et al., 2004), and, in banana, are associated with resistance to the burrowing nematode (Holscher et al., 2014). It is unclear whether SO-dependent toxicity mediates the effects of phenalenones on such soil-born pathogens in planta given their limited light exposure. However, these compounds are in banana also correlated with resistance to the foliar pathogen Mycosphaerella fidjiensis (Otalvaro et al., 2002), and are generally regarded as broad-spectrum light-activated phytoalexins (Flors & Nonell, 2006). Further work is needed to determine if SO is produced in vivo by these compounds and influences the infection process.
Besides having directly toxic effects on pests and pathogens, SO could potentially also impact host plant resistance by modulating programmed cell death (PCD) in the host. SO is known to regulate PCD in abiotic stress responses (Laloi & Havaux, 2015), and this capability merits further investigation in the context of phototoxin production and biotic interactions. Furthermore, while plants may utilize SO-generating phototoxins for defense, there is also evidence that certain necrotrophic pathogens produce Type II phototoxins such as cercosporin and DHN-melanin that act as virulence factors (Beltran-Garcia et al., 2014; Koh et al., 2023). The fungal toxin cercosporin, for example, changes leaf conductance by permeabilizing guard cell membranes, inhibits photosynthesis, directly oxidizes host RNA, and triggers SO-associated transcript profiles (Koh et al., 2023). This light-dependent damage causes cell death and foliar lesions in the host plant, facilitating the infection process by necrotrophic fungi in the genus Cercospora (Rezende et al., 2020). Thus, studies on both plant- and pathogen-derived phototoxins indicate that Type II photosensitizers are utilized as weapons on both sides of the arms race between plants and their biotic attackers.