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.