An Endophyte Constructs Fungicide-Containing Extracellular Barriers for Its Host Plant

Abstract

Surface cracks create sites for pathogen invasion. Yew trees (Taxus) hyperbranch from long-lived buds that lie underneath the bark [1], resulting in persistent bark cracking and deep air pockets, potentially allowing pathogens to enter the nutrient-rich vascular system (vertical phloem and inter-connected radial medullary rays [MR]). Yew is famous as the source of the anti-cancer diterpenoid drug Taxol. A mystery has been why both the tree and its resident non-pathogenic fungi (endophytes) synthesize Taxol, apparently redundantly [2-7]. These endophytes, as well as pure Taxol, suppress fungal pathogens including wood-decaying fungi (WDF) [8-11]. Here we show that a Taxol-producing fungal endophyte, Paraconiothyrium SSM001 [12], migrates to pathogen entry points including branch cracks. The fungus sequesters Taxol in intracellular hydrophobic bodies that are induced by WDF for release by exocytosis, after which the bodies can coalesce to form remarkable extracellular barriers, laced with the fungicide. We propose that microbial construction of fungicide-releasing hydrophobic barriers might be a novel plant defense mechanism. We further propose that the endophyte might be evolutionarily analogous to animal immune cells, in that it might expand plant immunity by acting as an autonomous, anti-pathogen sentinel that monitors the vascular system.

Root-hair endophyte stacking in finger millet creates a physicochemical barrier to trap the fungal pathogen Fusarium graminearum

“…These results show that an endophyte can create its own specialized killing microhabitat. M6 provides further support for our hypothesis 44 that plants have retained some endophytes because they are mobile hunters of host pathogens, analogous to immunity cells in animals, to protect plant cells, which are immobile. Indeed, RHESt is an inducible structure that only forms in the presence of Fusarium.…”

“…This study and earlier results 44 suggest that endophytes that show non-distinct localization under optimal conditions should be retested under native stress conditions. The discovery of RHESt suggests that other scientifically neglected, ancient crops may be worth exploring for microbiome-host interactions.…”

Six Key Traits of Fungi: Their Evolutionary Origins and Genetic Bases

“…Grass endophytes of Clavicipitaceae have long been studied for their antiherbivory toxins, which can increase fitness and dominance of infected plants (105). Surprisingly, some endophytes have been recently shown to produce the same SMs as their hosts and may compensate for reduced production of these SMs by the plants when they are allocating resources to, for example, reproduction (106). In general, endophytes are prolific producers of diverse metabolites and are considered "acquired immune systems" of the plants that benefit from them (107).…”

Molecular inter-kingdom interactions of endophytes isolated from Lychnophora ericoides

“…Following this rational, it is a promising endeavor to study the chemistry of interacting microorganisms to reveal molecules that are instrumental for the establishment of complex communities 23 . Studies into the chemistry of endophytes, combined with investigation of their involvement in microbial interactions, would contribute to our understanding of their role in natural environments 24, 25 .…”