Greatens Nicholas, Murithi Harun M, Coyne Danny, Clough Steven J, Sulyok Michael, Okunowo Wahab Oluwanisola, Abbas Hamed K, Shier W Thomas, Koch Bach Rachel A
SCINet Program and ARS AI Center of Excellence, Office of National Programs, Agricultural Research Service, United States Department of Agriculture, Beltsville, Maryland, United States of America.
Foreign Disease-Weed Science Research Unit, Agricultural Research Service, United States Department of Agriculture, Fort Detrick, Maryland, United States of America.
PLoS One. 2025 May 13;20(5):e0321896. doi: 10.1371/journal.pone.0321896. eCollection 2025.
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.
座囊菌纲病原菌大豆盾壳霉可引发大豆红叶斑病，这是非洲的一种主要病害。它是美国农业部动植物卫生检验局（USDA - PPQ）对美国生物安全至关重要的病原菌和毒素清单上的两种真菌植物病原菌之一，这反映出如果引入，它有造成高度破坏的可能性。尽管其具有重要性，但关于宿主感染的分子基础尚无已发表的报告。对大豆盾壳霉基因组的研究揭示了一个次生代谢物基因簇，其基因组成和结构与合成光激活苝醌毒素（如尾孢菌素）的基因簇相似。苝醌是一种非宿主特异性毒素，在光照下会产生活性氧，对植物宿主具有几乎普遍的毒性。对来自非洲东部和南部的大豆盾壳霉分离株在无菌条件下进行光照和黑暗培养。光照培养的菌株产生了典型的苝醌红粉色色素沉着。差异基因表达分析表明，生物合成基因簇中的八个基因中有六个，包括聚酮合酶基因，在光照下显著上调。液相色谱 - 质谱法证实产生了苝醌乙色酮A，这是其他真菌病原菌中一种已知的毒力因子。与在光照下培养的叶片相比，在黑暗中培养的叶片上形成的病斑明显更少，症状出现延迟。此外，我们在亲缘关系更远的座囊菌纲植物病原菌中鉴定出了直系同源基因簇，而之前并不知道它们的存在，这表明这些毒素对农业和真菌生态学具有更广泛的重要性。这项工作首次证明苝醌乙色酮A可能有助于大豆盾壳霉的毒力。
