Production of the light-activated elsinochrome phytotoxin in the soybean pathogen Coniothyrium glycines hints at virulence factor

Authors: GREATENS, NICHOLAS - Oak Ridge Institute For Science And Education (ORISE); MURITHI, HARUN, M. - International Institute Of Tropical Agriculture (IITA); COYNE, DANNY - International Institute Of Tropical Agriculture (IITA); Clough, Steven; SULYOK, MICHAEL - University Of Natural Resources And Life Sciences, Vienna; OKUNOWO, WAHAB - University Of Lagos; Abbas, Hamed; SHIER, W.THOMAS - University Of Minnesota; Koch Bach, Rachel

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/13/2025
Publication Date: 5/13/2025
Citation: Greatens, N., Murithi, H., Coyne, D., Clough, S.J., Sulyok, M., Okunowo, W., Abbas, H.K., Shier, W., Koch Bach, R.A. 2025. Production of the light-activated elsinochrome phytotoxin in the soybean pathogen Coniothyrium glycines hints at virulence factor. PLOS ONE. https://doi.org/10.1371/journal.pone.0321896.
DOI: https://doi.org/10.1371/journal.pone.0321896

Interpretive Summary: Coniothyrium glycines is a fungal species that causes a severe disease of soybean called red leaf blotch in Africa. This pathogen has the potential to pose a severe threat to soybean production in the United States were it to establish here. Even given its importance to the biosecurity of the United States, nothing is known regarding how C. glycines causes disease. Without this understanding, effective disease control measures cannot be developed. We show that C. glycines contains the genetic machinery to synthesize a toxin that is known to play a major role in disease development by other plant pathogens that also produce this toxin. Moreover, production of this toxin is greater when exposed to light. This research is important because it provides the first understanding as to how C. glycines infects soybeans. The results of this work will be used by soybean breeders and extension specialists to more effectively develop resistant soybean germplasm and disease management plans that will be necessary to safeguard the nation’s soybean industry should the pathogen ever establish.

Technical Abstract: The Dothideomycete pathogen Coniothyrium glycines causes red leaf blotch of soybean, a major disease in Africa. It is one of two fungal plant pathogens on the USDA PPQ Select Agents and Toxins list of pathogens important to the biosecurity of the United States, reflective of its potential to be highly destructive if introduced. Despite its importance, there are no published reports regarding the molecular basis of host infection. Examination of the C. glycines genome revealed a secondary metabolite gene cluster that is similar in gene content and organization to clusters that synthesize light-activated perylenequinone toxins, such as cercosporin. Perylenequinones are non-host specific toxins that, upon exposure to light, generate reactive oxygen species, which have near-universal toxicity to plant hosts. Coniothyrium glycines isolates from eastern and southern Africa were cultured axenically under light and dark conditions. Light-grown cultures produced red-pink pigmentation typical of perylenequinones. Differential gene expression analysis showed that six of the eight genes in the biosynthetic gene cluster, including the polyketide synthase gene, were significantly upregulated in light. Liquid chromatography-mass spectrometry confirmed production of the perylenequinone elsinochrome A, a known virulence factor in other fungal pathogens. On leaves incubated in the dark, significantly fewer lesions formed and symptoms were delayed, compared to leaves incubated in the light. In addition, we identified orthologous gene clusters in more distantly related Dothideomycete plant pathogens where their presence was previously unknown, indicating a broader importance of these toxins to agriculture and fungal ecology. This work provides the first evidence that elsinochrome A may contribute to the virulence of C. glycines.