Fungal endophytes can modulate plant invasion

Biol Rev Camb Philos Soc. 2024 Apr 17. doi: 10.1111/brv.13085. Online ahead of print.

Abstract

Symbiotic organisms may contribute to a host plant's success or failure to grow, its ability to maintain viable populations, and potentially, its probability of establishment and spread outside its native range. Intercellular and intracellular microbial symbionts that are asymptomatic in their plant host during some or all of their life cycle - endophytes - can form mutualistic, commensal, or pathogenic relationships, and sometimes novel associations with alien plants. Fungal endophytes are likely the most common endosymbiont infecting plants, with life-history, morphological, physiological, and plant-symbiotic traits that are distinct from other endophytic guilds. Here, we review the community dynamics of fungal endophytes during the process of plant invasion, and how their functional role may shift during the different stages of invasion: transport, introduction (colonisation), establishment, and spread. Each invasion stage presents distinct ecological filters that an alien plant must overcome to advance to the subsequent stage of invasion. Endophytes can alternately aid the host in overcoming stage-specific filters, or contribute to the barriers imposed by filters (e.g. biotic resistance), thereby affecting invasion pathways. A few fungi can be transported as seed endophytes from their native range and be vertically transmitted to future generations in the non-native range, especially in graminoids. In other plant groups, alien plants mostly acquire endophytes via horizontal transmission from the invaded plant community, and the host endophyte community is shaped by host filtering and biogeographic factors (e.g. dispersal limitation, environmental filtering). Endophytes infecting alien plants (both those transported with their host and those accumulated in the non-native range) may influence invasion success by affecting plant growth, reproduction, environmental tolerance, and pathogen and herbivory defences; however, the direction and magnitude of these effects can be contingent upon the host identity, life stage, ecological conditions, and invasion stage. This context dependence may cause endophytic fungi to shift to a non-endophytic (e.g. pathogenic) functional life stage in the same or different hosts, which can modify alien-native plant community dynamics. We conclude by identifying paths in which alien hosts can exploit the context dependency of endophyte function in novel abiotic and biotic conditions and at the different stages of invasion.

Keywords: biocontrol; community assembly; disease‐mediated invasions; enemy release; fungal endophytes; fungal pathogens; invasive plants; plant–fungal interactions.