Plant triterpenoid saponins function as susceptibility factors to promote the pathogenicity of Botrytis cinerea.

IF 17.1 1区 生物学 Q1 BIOCHEMISTRY & MOLECULAR BIOLOGY Molecular Plant Pub Date : 2024-07-01 Epub Date: 2024-05-27 DOI:10.1016/j.molp.2024.05.008
Francisco J Escaray, Amelia Felipo-Benavent, Cristian J Antonelli, Begoña Balaguer, Maria Pilar Lopez-Gresa, Pablo Vera
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Abstract

The gray mold fungus Botrytis cinerea is a necrotrophic pathogen that causes diseases in hundreds of plant species, including high-value crops. Its polyxenous nature and pathogenic success are due to its ability to perceive host signals in its favor. In this study, we found that laticifer cells of Euphorbia lathyris are a source of susceptibility factors required by B. cinerea to cause disease. Consequently, poor-in-latex (pil) mutants, which lack laticifer cells, show full resistance to this pathogen, whereas lot-of-latex mutants, which produce more laticifer cells, are hypersusceptible. These S factors are triterpenoid saponins, which are widely distributed natural products of vast structural diversity. The downregulation of laticifer-specific oxydosqualene cyclase genes, which encode the first committed step enzymes for triterpene and, therefore, saponin biosynthesis, conferred disease resistance to B. cinerea. Likewise, the Medicago truncatula lha-1 mutant, compromised in triterpenoid saponin biosynthesis, showed enhanced resistance. Interestingly, the application of different purified triterpenoid saponins pharmacologically complemented the disease-resistant phenotype of pil and hla-1 mutants and enhanced disease susceptibility in different plant species. We found that triterpenoid saponins function as plant cues that signal transcriptional reprogramming in B. cinerea, leading to a change in its growth habit and infection strategy, culminating in the abundant formation of infection cushions, the multicellular appressoria apparatus dedicated to plant penetration and biomass destruction in B. cinerea. Taken together, these results provide an explanation for how plant triterpenoid saponins function as disease susceptibility factors to promote B. cinerea pathogenicity.

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植物三萜皂苷作为易感因子可促进灰霉病菌的致病性。
灰霉病菌(Botrytis cinerea)是一种坏死性病原体,可导致数百种植物(包括高价值作物)发病。这种多腺性和致病性的成功是由于它能够感知寄主对其有利的信号。我们发现,Euphorbia lathyris 的小叶细胞是 B. cinerea 致病所需的易感因子(S)的来源。因此,缺乏鳞叶细胞的poor-in-latex(pil)突变体对这种病原体表现出完全的抗性,而产生更多鳞叶细胞的lot-of-latex(lol)突变体则易感。这些 S因子是三萜类皂苷,是分布广泛、结构多样的天然产物。下调拉蒂西弗特异性氧代喹啉环化酶(OSCs)基因(OSCs 编码三萜类生物合成的第一步酶,因此也是皂苷生物合成的第一步酶)可增强对 B. cinerea 的抗病性。同样,Medicago truncatula lha-1 突变体的三萜类皂苷生物合成受到影响,但其抗病性有所增强。有趣的是,不同纯化三萜类皂苷的药理应用补充了 pil 和 hla-1 突变体的抗病表型,并增强了不同植物物种对疾病的敏感性。我们发现,三萜类皂苷作为植物线索,可发出信号,对银环孢菌进行转录重编程,从而改变其生长习性和感染策略,最终大量形成感染垫(IC),这是银环孢菌专门用于植物穿透和生物量破坏的多细胞附生器。我们的研究结果解释了植物三萜类皂苷如何作为疾病易感性因子(S)促进 B. cinerea 的致病性。
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来源期刊
Molecular Plant
Molecular Plant 植物科学-生化与分子生物学
CiteScore
37.60
自引率
2.20%
发文量
1784
审稿时长
1 months
期刊介绍: Molecular Plant is dedicated to serving the plant science community by publishing novel and exciting findings with high significance in plant biology. The journal focuses broadly on cellular biology, physiology, biochemistry, molecular biology, genetics, development, plant-microbe interaction, genomics, bioinformatics, and molecular evolution. Molecular Plant publishes original research articles, reviews, Correspondence, and Spotlights on the most important developments in plant biology.
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