Fungal Endophytes: Common Host Plant Symbionts but Uncommon Mutualists1

SYNOPSIS. Fungal endophytes are extremely common and highly diverse microorganisms that live within plant tissues, but usually remain asymptomatic. Endophytes traditionally have been considered plant mutualists, mainly by reducing herbivory via production of mycotoxins, such as alkaloids. However, the vast majority of endophytes, especially horizontally-transmitted ones commonly found in woody plants, apparently have little or no effect on herbivores. For the systemic, vertically-transmitted endophytes of grasses, mutualistic interactions via increased resistance to herbivores and pathogens are more common, as predicted by evolutionary theory. However, even in these obligate symbioses, endophytes are often neutral or even pathogenic to the host grass, depending on endophyte and plant genotype and environmental conditions. We present a graphical model based upon variation in nitrogen flux in the host plant. Nitrogen is a common currency in endophyte/host and plant/herbivore interactions in terms of limitations to host plant growth, enhanced uptake by endophytes, demand for synthesis of nitrogen-rich alkaloids, and herbivore preference and performance. Our graphical model predicts that low alkaloid-producing endophytes should persist in populations when soil nutrients and herbivory are low. Alternatively, high alkaloid endophytes are favored under increasing herbivory and increasing soil nitrogen, at least to some point. At very high soil nitrogen levels, uninfected plants may be favored over either type of infected plants. These predictions are supported by patterns of infection and alkaloid production in nature, as well by a manipulative field experiment. However, plant genotype and other environmental factors, such as available water, interact with the presence of the endophyte to influence host plant performance.