Fungal endophytes relieve the growth-defence trade-off of their plant hosts through the production of bioactive alkaloids.

A central paradigm in plant biology is that there is a trade-off between growth and defence. We propose that Epichloë fungal endophytes relieve this trade-off in plants by the fungal-derived production of antiherbivore alkaloids. Lolium perenne plants without (nil) and with Epichloë LpTG-3 sp. strain AR37 able (wild type (wt), ΔidtA) and unable (ΔidtM) to produce bioactive indole diterpene alkaloids were subjected to an exogenous application of gibberellin (GA) hormone followed by a challenge with Rhopalosiphum padi aphids. The GA-derived plant growth promotion increased the susceptibility to aphids in both nil plants and ΔidtM-associated plants but did not affect the aphid resistance in either wt- or ΔidtA-associated plants. GA treatment changed the composition of AR37-derived alkaloids, reduced the concentration of AR37-derived epoxyjanthitrem alkaloids in wt-associated plants and reduced the amount of mycelial biomass of AR37 variants. GA treatment generally increased expression of plant genes related to abscisic acid (ABA), auxin, cell division, cell wall and GA (e.g., YUCCA2, GA2ox3), reduced expression of photosynthesis-related genes (e.g., RBCS1), and had mixed effects on the expression of plant immunity-related genes (e.g., PR-1). GA treatment increased concentrations of ABA, salicylic acid, and jasmonic acid, and did not affect auxin concentrations. Additionally, soil derived from GA-treated plants showed increased abundance of putative bacterial taxa that included plant growth-promoting members (e.g., Bryobacter). Our findings demonstrate that the AR37-derived production of indole diterpene alkaloids was the key mechanism that relieved the growth-defence trade-off of plants.