Laboratory of Phytopathology, Wageningen University, Wageningen, The Netherlands.
Department of Biology, Institute for Molecular Plant Physiology, RWTH University, Aachen, Germany.
Nat Commun. 2024 Jul 31;15(1):6448. doi: 10.1038/s41467-024-50748-5.
Saponins are plant secondary metabolites comprising glycosylated triterpenoids, steroids or steroidal alkaloids with a broad spectrum of toxicity to microbial pathogens and pest organisms that contribute to basal plant defense to biotic attack. Secretion of glycosyl hydrolases that enzymatically convert saponins into less toxic products was thus far the only mechanism reported to enable fungal pathogens to colonize their saponin-containing host plant(s). We studied the mechanisms that the fungus Botrytis cinerea utilizes to be tolerant to well-characterized, structurally related saponins from tomato and Digitalis purpurea. By gene expression studies, comparative genomics, enzyme assays and testing a large panel of fungal (knockout and complemented) mutants, we unraveled four distinct cellular mechanisms that participate in the mitigation of the toxic activity of these saponins and in virulence on saponin-producing host plants. The enzymatic deglycosylation that we identified is novel and unique to this fungus-saponin combination. The other three tolerance mechanisms operate in the fungal membrane and are mediated by protein families that are widely distributed in the fungal kingdom. We present a spatial and temporal model on how these mechanisms jointly confer tolerance to saponins and discuss the repercussions of these findings for other plant pathogenic fungi, as well as human pathogens.
皂素是一种植物次生代谢产物，由糖苷化三萜类、甾体或甾体生物碱组成，对微生物病原体和害虫具有广谱毒性，有助于植物对生物攻击的基础防御。迄今为止，唯一被报道的机制是分泌糖苷水解酶，将皂素转化为毒性较低的产物，从而使真菌病原体能够定殖其含有皂素的宿主植物。我们研究了真菌 Botrytis cinerea 利用哪些机制来耐受番茄和毛地黄中具有良好特征的、结构相关的皂素。通过基因表达研究、比较基因组学、酶测定以及对大量真菌（敲除和互补）突变体的测试，我们揭示了四个不同的细胞机制，这些机制参与减轻这些皂素的毒性活性，并在产生皂素的宿主植物上发挥毒性作用。我们鉴定的酶解糖化作用是新颖的，且仅存在于这种真菌-皂素组合中。其他三种耐受机制在真菌膜中起作用，由在真菌界广泛分布的蛋白质家族介导。我们提出了一个关于这些机制如何共同赋予对皂素的耐受性的时空模型，并讨论了这些发现对其他植物病原真菌以及人类病原体的影响。
