Many recent studies have demonstrated that non-pathogenic fungi within plant microbiomes, i.e., endophytes ("endo" = within, "phyte" = plant), can significantly modify the expression of host plant disease. The rapid pace of advancement in endophyte ecology warrants a pause to synthesize our understanding of endophyte disease modification and to discuss future research directions. We reviewed recent literature on fungal endophyte disease modification, and here report on several emergent themes: (1) Fungal endophyte effects on plant disease span the full spectrum from pathogen antagonism to pathogen facilitation, with pathogen antagonism most commonly reported. (2) Agricultural plant pathosystems are the focus of research on endophyte disease modification. (3) A taxonomically diverse group of fungal endophytes can influence plant disease severity. And (4) Fungal endophyte effects on plant disease severity are context-dependent. Our review highlights the importance of fungal endophytes for plant disease across a broad range of plant pathosystems, yet simultaneously reveals that complexity within plant microbiomes presents a significant challenge to disentangling the biotic environmental factors affecting plant disease severity. Manipulative studies integrating eco-evolutionary approaches with emerging molecular tools will be poised to elucidate the functional importance of endophytes in natural plant pathosystems that are fundamental to biodiversity and conservation.

▪ Abstract  Interspecific hybridization can disrupt normal resistance of plant and animal species to their parasites. Resistance to parasites is affected by hybridization in the following ways: no difference between hybrids and parentals, additivity, hybrid susceptibility, and dominance to susceptibility. Similar patterns were seen across host taxa. Responses of different parasite species vary widely to the same hybrid host, which indicates diverse genetic effects of interspecific hybridization on resistance. Differences between field and common garden or laboratory studies suggest that environmental factors in hybrid zones influence the patterns seen in the field. Based on recent studies of hybrid-parasite interactions, three avenues of future research will provide a more complete understanding of the roles of hybrids and the roles of parasites in host evolution. First, the relationship between inheritance of putative resistance mechanisms of hosts and responses of parasites needs study using analyses of recombinant progenies. Second, the interaction among environmental variation in hybrid zones, resistance mechanisms, responses of parasites, and the impact of parasites on host fitness needs experimental analysis using reciprocal transplant experiments in hybrid zones. Finally, the role of hybrids in the community structure and interactions of parasites needs study.

The endophytic fungi of woody plants may be diverse as often claimed, and likewise, they may be functionally novel as demonstrated in a few studies. However, the endophyte taxa that are most frequently reported tend to belong to fungal groups composed of morphologically similar endophytes and parasites. Thus, it is plausible that endophytes are known (i.e., described) parasites in a latent phase within the host. If this null hypothesis were true, endophytes would represent neither additional fungal diversity distinct from parasite diversity nor a symbiont community likely to be novel ecologically. To be synonymous with parasites of the host, endophytes should at least be most closely related to those same parasites. Here we report that seven distinct parasites of Pinus monticola do not occur as endophytes. The majority of endophytes of P. monticola (90% of 2,019 cultures) belonged to one fungal family, the Rhytismataceae. However, not a single rhytismataceous endophyte was found to be most closely related by sequence homology to the three known rhytismataceous parasites of P. monticola. Similarly, neither endophytic Mycosphaerella nor endophytic Rhizosphaera isolates were most closely related to known parasites of P. monticola. Morphologically, the endophytes of P. monticola can be confounded with the parasites of the same host. However, they are actually most closely related to, but distinct from, parasites of other species of Pinus. If endophytes are generally unknown species, then estimates of 1 million endophytes (i.e., approximately 1 in 14 of all species of life) seem reasonable.

Summary Nonpathogenic foliar fungi (i.e. endophytes and epiphytes) can modify plant disease severity in controlled experiments. However, experiments have not been combined with ecological studies in wild plant pathosystems to determine whether disease‐modifying fungi are common enough to be ecologically important. We used culture‐based methods and DNA sequencing to characterize the abundance and distribution of foliar fungi of Populus trichocarpa in wild populations across its native range (Pacific Northwest, USA). We conducted complementary, manipulative experiments to test how foliar fungi commonly isolated from those populations influence the severity of Melampsora leaf rust disease. Finally, we examined correlative relationships between the abundance of disease‐modifying foliar fungi and disease severity in wild trees. A taxonomically and geographically diverse group of common foliar fungi significantly modified disease severity in experiments, either increasing or decreasing disease severity. Spatial patterns in the abundance of some of these foliar fungi were significantly correlated (in predicted directions) with disease severity in wild trees. Our study reveals that disease modification is an ecological function shared by common foliar fungal symbionts of P. trichocarpa. This finding raises new questions about plant disease ecology and plant biodiversity, and has applied potential for disease management.

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Fungal endophytes are important in plant ecology and common in plants. We attempted to test cointroduction and host-jumping hypotheses on a community basis by comparing endophytes isolated from invasive spotted knapweed (Centaurea stoebe, Asteraceae) in its native and invaded ranges. Of 92 combined, sequence-based haplotypes representing eight classes of Fungi, 78 occurred in only one of the two ranges. In the native range of C. stoebe, one haplotype of Alternaria alternata was clearly dominant, whereas in the invaded range, no haplotype was dominant. Many haplotypes were closely related to one another and novel. For example, six putative, new species of Botrytis were discovered as endophytes of C. stoebe, which has never been reported to have Botrytis spp.. Apparent differences between the two communities of endophytes were significant according to an analysis of similarity, but phylogenetic community structure did not differ significantly between the ranges. Both host-jumping and cointroduction of fungal endophytes likely took place during the spotted knapweed invasion.

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