Multiple paths of plant host toxicity are associated with the fungal toxin cercosporin

Abstract

The Cercospora species of fungi are responsible for leaf spot disease affecting many key economic crops. Most of these fungi secrete a toxic photodynamic molecule, cercosporin, that reacts with light and oxygen to produce reactive singlet oxygen ( 1 O 2 ) contributing to fungal virulence. We show similar cellular localization and aetiology of cercosporin in the non-host Arabidopsis and the host Nicotiana benthamiana. Cercosporin accumulates in cell membranes in an oxidized state and in plastids in a mixture of redox states in a manner that is dependent on ongoing photosynthetic processes. We observed that cercosporin rapidly compromised photosynthesis as measured by F v /F m , NPQ, and photosystem I (PSI) parameters.Stomatal guard cells in particular demonstrated rapid light-dependent membrane permeabilization that led to changes in leaf conductance. We showed that cercosporin-mediated 1 O 2 generation oxidized RNA to form 8-oxoguanosine (8-oxoG), leading to translational attenuation and induction of 1 O 2 signature gene transcripts. We also identified a subset of cercosporin-induced transcripts that were independent of the photodynamic effect. Our results point to the multimodal action of cercosporin that includes the inhibition of photosynthesis, the direct oxidation of nucleic acid residues and the elicitation of complex transcriptome responses.8-hydroxyguanosine (8-oxoG), fungal elicitor, gene expression regulation, oxidative stress, singlet oxygen ( 1 O 2 ) | INTRODUCTIONCercosporin is a potent photosensitizer molecule produced by fungal species in the genus Cercospora. Cercospora can exhibit a hemibiotrophic lifestyle infecting through a latent almost symptomless phase that facilitates hyphae colonization followed by transition to necrotrophy (Rangel et al., 2020). These fungi are responsible for leaf spot disease, a malaise affecting a plethora of crop plants, including corn, soybean, tobacco, coffee and sugar beet (Farr et al., 1989), which leads to the necrosis of leaf tissue, decreasing crop productivity. The chemical cercosporin and other members of the perylenequinone family including hypocrellins and calphostins are

Singlet oxygen signalling and its potential roles in plant biotic interactions

“…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 (Beltrán-García 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).…”

“…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 (Beltrán-García 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 (Santos Rezende et al, 2020).…”

Fun in the Sun: Singlet Oxygen Harnessing the Power of Light in Response to Biotic Stresses

“…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).…”

“…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).…”

Osmotic stress in roots drives lipoxygenase-dependent plastid remodeling through singlet oxygen production

“…These abiotic stresses include dryness, salinity, injury, and in certain conditions exposure to high light. A common link between them was found to be singlet oxygen-generated perturbations in mRNA translation that is brought about by direct singlet oxygen oxidation of RNA (Koh et al, 2023(Koh et al, , 2021. It was shown that guanosine residues in mRNA are readily and specifically oxidized to 8-hydroxyguanosine that blocks consecutive mRNA translation.…”