The beneficial root-colonizing fungus Colletotrichum tofieldiae mediates plant growth promotion (PGP) upon phosphate (Pi) starvation in Arabidopsis thaliana. This activity is dependent on the Trp metabolism of the host, including indole glucosinolate (IG) hydrolysis. Here, we show that C. tofieldiae resolves several Pi starvation-induced molecular processes in the host, one of which is the downregulation of auxin signaling in germ-free plants, which is restored in the presence of the fungus. Using CRISPR/Cas9 genome editing, we generated an Arabidopsis triple mutant lacking three homologous nitrilases (NIT1 to NIT3) that are thought to link IG-hydrolysis products with auxin biosynthesis. Retained C. tofieldiae-induced PGP in nit1/2/3 mutant plants demonstrated that this metabolic connection is dispensable for the beneficial activity of the fungus. This suggests that either there is an alternative metabolic link between IG-hydrolysis products and auxin biosynthesis, or C. tofieldiae restores auxin signaling independently of IG metabolism. We show that C. tofieldiae, similar to pathogenic microorganisms, triggers Arabidopsis immune pathways that rely on IG metabolism as well as salicylic acid and ethylene signaling. Analysis of IG-deficient myb mutants revealed that these metabolites are, indeed, important for control of in planta C. tofieldiae growth: however, enhanced C. tofieldiae biomass does not necessarily negatively correlate with PGP. We show that Pi deficiency enables more efficient colonization of Arabidopsis by C. tofieldiae, possibly due to the MYC2-mediated repression of ethylene signaling and changes in the constitutive IG composition in roots.

Copyright © 2021 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.

有益的根部定植真菌Colletotrichum tofieldiae在拟南芥中磷酸盐(Pi) 饥饿时介导植物生长促进(PGP) 。这种活性取决于宿主的色氨酸代谢，包括吲哚硫代葡萄糖苷 (IG) 水解。在这里，我们展示了C. tofieldiae解决了宿主中几个 Pi 饥饿诱导的分子过程，其中之一是无菌植物中生长素信号传导的下调，这种过程在真菌存在下得以恢复。使用 CRISPR/Cas9 基因组编辑，我们生成了一种缺乏三种同源腈水解酶（NIT1 到 NIT3）的拟南芥三重突变体，这些酶被认为将 IG 水解产物与生长素生物合成联系起来。保留的C. tofieldiae在nit1/2/3突变植物中诱导的 PGP证明这种代谢联系对于真菌的有益活动是可有可无的。这表明 IG 水解产物和生长素生物合成之间存在替代代谢联系，或者C. tofieldiae恢复独立于 IG 代谢的生长素信号。我们展示了与病原微生物相似的C. tofieldiae触发了依赖于 IG 代谢以及水杨酸和乙烯信号传导的拟南芥免疫通路。对缺乏 IG 的myb突变体的分析表明，这些代谢物确实对控制植物C. tofieldiae 的生长很重要：然而，增强C. tofieldiae生物量不一定与 PGP 呈负相关。我们表明，Pi 缺乏使拟南芥更有效地被C. tofieldiae 定植，这可能是由于 MYC2 介导的乙烯信号抑制和根中组成性 IG 组成的变化。

版权所有 © 2021 作者。这是在 CC BY-NC-ND 4.0 国际许可下分发的开放获取文章。