Akiyama Ryota, Kawano Yui, Shimizu Kosuke, Makino Soichiro, Akanuma Karen, Nagatomo Haru, Hirai Masami Yokota, Sugimoto Yukihiro, Kushida Atsuhiko, Tanino Keiji, Mizutani Masaharu
Graduate School of Agricultural Science, Kobe University, Rokkodai 1-1, Nada, Kobe, Hyogo, 657-8501, Japan.
RIKEN Center for Sustainable Resource Science, Suehiro-cho 1-7-22, Tsurumi-ku, Yokohama, Kanagawa, 230-0045, Japan.
New Phytol. 2025 Aug;247(3):1370-1381. doi: 10.1111/nph.70252. Epub 2025 May 26.
Eclepins are root-secreted compounds that induce the hatching of cyst nematodes. Solanoeclepin A (SEA) and B (SEB) have been isolated as potent hatching factors for potato cyst nematodes (PCNs). SEB is biosynthesized in roots, released into the rhizosphere, and converted into SEA by soil microorganisms. However, given that SEB and SEA exhibit comparable hatching-inducing activity toward PCNs, the ecological significance of microbial solanoeclepin metabolism in eclepin-mediated communication remains unclear. In this study, we identified solanoeclepin C (SEC), a previously unrecognized solanoeclepin secreted by tomato and potato roots. Structural analysis revealed that SEC is an acetylated derivative of SEB. Soil incubation experiments demonstrated that SEC is converted into SEB and subsequently into SEA. SEC exhibits 10 000-fold lower hatching-inducing activity than SEA. Gene expression analysis in hydroponically grown tomatoes showed that solanoeclepin biosynthesis is upregulated under nitrogen and phosphorus deficiencies, with nitrogen starvation having the strongest effect. Our results demonstrate that although SEC itself exhibits low hatching-inducing activity, it is converted by soil microorganisms into SEB and SEA, which are then exploited by PCNs to trigger their hatching. These findings reveal a previously unrecognized three-way interaction among plants, soil microbes, and nematodes mediated by solanoeclepins.
独脚金内酯是根部分泌的化合物,可诱导孢囊线虫孵化。已分离出独脚金内酯A(SEA)和B(SEB)作为马铃薯孢囊线虫(PCN)的有效孵化因子。SEB在根部生物合成,释放到根际,并被土壤微生物转化为SEA。然而,鉴于SEB和SEA对PCN表现出相当的孵化诱导活性,独脚金内酯介导的通讯中微生物对独脚金内酯的代谢的生态意义仍不清楚。在本研究中,我们鉴定了独脚金内酯C(SEC),一种以前未被识别的由番茄和马铃薯根部分泌的独脚金内酯。结构分析表明,SEC是SEB的乙酰化衍生物。土壤培养实验表明,SEC被转化为SEB,随后又转化为SEA。SEC的孵化诱导活性比SEA低10000倍。水培番茄的基因表达分析表明,在氮和磷缺乏的情况下,独脚金内酯的生物合成上调,其中氮饥饿的影响最强。我们的结果表明,尽管SEC本身的孵化诱导活性较低,但它被土壤微生物转化为SEB和SEA,然后被PCN利用来触发它们的孵化。这些发现揭示了一种以前未被识别的由独脚金内酯介导的植物、土壤微生物和线虫之间的三方相互作用。