Are endophytic fungi defensive plant mutualists?

Abstract

Endophytic fungi, especially asexual, systemic endophytes in grasses, are generally viewed as plant mutualists, mainly through the action of mycotoxins, such as alkaloids in infected grasses, which protect the host plant from herbivores. Most of the evidence for the defensive mutualism concept is derived from studies of agronomic grass cultivars, which may be atypical of many endophyte‐host interactions. I argue that endophytes in native plants, even asexual, seed‐borne ones, rarely act as defensive mutualists. In contrast to domesticated grasses where infection frequencies of highly toxic plants often approach 100%, natural grass populations are usually mosaics of uninfected and infected plants. The latter, however, usually vary enormously in alkaloid levels, from none to levels that may affect herbivores. This variation may result from diverse endophyte and host genotypic combinations that are maintained by changing selective pressures, such as competition, herbivory and abiotic factors. Other processes, such as spatial structuring of host populations and endophytes that act as reproductive parasites of their hosts, may maintain infection levels of seed‐borne endophytes in natural populations, without the endophyte acting as a mutualist.

Fungal grass endophytes and arthropod communities: lessons from plant defence theory and multitrophic interactions

“…We should expect that like plant-based alkaloids, endophytic alkaloids are also costly to produce in terms of tradeoffs with growth and reproduction (Faeth 2002). Maintenance of endophytic alkaloids in grasses may even decrease host fitness if herbivores are absent or if they are ineffective at deterring herbivory because uninfected plants or infected plants without alkaloids should be better competitors (Faeth 2002). The cost of endophyte infection and associated alkaloids are also difficult to detect because of the long-lived nature of the perennial grass hosts.…”

“…Many infected grasses produce either no alkaloids at all, or alkaloids at only very low levels. Very few produce the high levels found in cultivated grass cultivars (Faeth, 2002and Piano et al, 2005. Finally, when more complex, natural communities are considered, the effects of endophytes and their alkaloids become much less predictable.…”

“…PDT provides a long-standing and well-developed conceptual framework accompanied by a rich literature for explaining the ecology and evolution of plant-herbivore interactions. For unknown reasons, PDT has been, and still is (e.g., Clay 2009), largely ignored in explaining host endophyte-grass-herbivore interactions, despite early and repeated calls (e.g., Saikkonen et al, 1998, Faeth, 2002, Faeth and Bultman, 2002and Cheplick and Faeth, 2009) for applying existing ecological theory to endophyte-host grass interactions.…”

“…But in other studies, the frequency of endophyte infection does not increase with greater livestock (Bazely et al 1997, Rum and Benbecula islands) and native vertebrate (Rambo & Faeth 1999) grazing as predicted by DMH. In general, Faeth (2002) argued that relatively few grasses infected by seed borne endophytes are toxic to vertebrates. The few that are toxic have been well-studied relative to non-toxic endophytes because of their negative economic effects on livestock production.…”

Pathogen Competition and Coexistence and the Evolution of Virulence

“…A vertically transmitted parasite with no apparent horizontal transmission is the endophytic fungus Neotyphodium in the Arizona grass Festucca arizonica. So far, the persistence of this endophyte is a mystery, because its vertical transmission is not perfect and no competitive advantages have been found that it might give to infected plants [41,40,42]. Protection against a more virulent strain or a more virulent other parasite would be a possible explanation, but a candidate has been elusive so far.…”