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Tree planting and natural regeneration contribute to the ongoing effort to restore Earth's forests. Our review addresses how the plant microbiome can enhance the survival of planted and naturally regenerating seedlings and serve in long-term forest carbon capture and the conservation of biodiversity. We focus on fungal leaf endophytes, ubiquitous defensive symbionts that protect against pathogens. We first show that fungal and oomycetous pathogen richness varies greatly for tree species native to the United States ( n = 0–876 known pathogens per US tree species), with nearly half of tree species either without pathogens in these major groups or with unknown pathogens. Endophytes are insurance against the poorly known and changing threat of tree pathogens. Next, we review studies of plant phyllosphere feedback, but knowledge gaps prevent us from evaluating whether adding conspecific leaf litter to planted seedlings promotes defensive symbiosis, analogous to adding soil to promote positive feedback. Finally, we discuss research priorities for integrating the plant microbiome into efforts to expand Earth's forests. 

Closely related species are expected to have similar functional traits due to shared ancestry and phylogenetic inertia. However, few tests of this hypothesis are available for plant‐associated fungal symbionts. Fungal leaf endophytes occur in all land plants and can protect their host plant from disease by a variety of mechanisms, including by parasitizing pathogens (e.g., mycoparasitism). Here, we tested whether phylogenetic relatedness among species ofCladosporium, a widespread genus that includes mycoparasitic species, predicts the effect of this endophyte on the severity of leaf rust disease. First, we used congruence among different marker sequences (i.e., genealogical concordance phylogenetic species recognition criterion) to delimit species ofCladosporium. Next, in a controlled experiment, we quantified both mycoparasitism and disease modification for the selectedCladosporiumspecies. We identified 17 species ofCladosporium; all the species reduced rust disease severity in our experiment.Cladosporiumphylogeny was a significant predictor of mycoparasitism. However, we did not observe a phylogenetic effect on disease severity overall, indicating that other mechanism/s operating independently of shared ancestry also contributed to endophyte effects on disease severity. Indeed, a second experiment showed thatCladosporiumendophyte exudates (no live organism) from divergent species groups equally reduced disease severity. Our results reveal that multiple mechanisms contribute to the protective effects of an endophyte against a plant pathogen, but not all traits underlying these mechanisms are phylogenetically conserved.

 

Plant defense against pathogens includes a range of mechanisms, including, but not limited to, genetic resistance, pathogen‐antagonizing endophytes, and pathogen competitors. The relative importance of each mechanism can be expressed in a hierarchical view of defense. Several recent studies have shown that pathogen antagonism is inconsistently expressed within the plant defense hierarchy. Our hypothesis is that the hierarchy is governed by contingency rules that determine when and where antagonists reduce plant disease severity.

Here, we investigated whether pathogen competition influences pathogen antagonism usingPopulusas a model system. In three independent field experiments, we asked whether competition for leaf mesophyll cells between aMelampsorarust pathogen and a microscopic, eriophyid mite affects rust pathogen antagonism by fungal leaf endophytes. The rust pathogen has an annual, phenological disadvantage in competition with the mite because the rust pathogen must infect its secondary host in spring before infectingPopulus. We varied mite–rust competition by utilizingPopulusgenotypes characterized by differential genetic resistance to the two organisms. We inoculated plants with endophytes and allowed mites and rust to infect plants naturally.

Two contingency rules emerged from the three field experiments: (a) Pathogen antagonism by endophytes can be preempted by host genes for resistance that suppress pathogen development, and (b) pathogen antagonism by endophytes can secondarily be preempted by competitive exclusion of the rust by the mite.

Synthesis: Our results point to aPopulusdefense hierarchy with resistance genes on top, followed by pathogen competition, and finally pathogen antagonism by endophytes. We expect these rules will help to explain the variation in pathogen antagonism that is currently attributed to context dependency.

 

Foliar fungi – pathogens, endophytes, epiphytes – form taxonomically diverse communities that affect plant health and productivity. The composition of foliar fungal communities is variable at spatial scales both small (e.g. individual plants) and large (e.g. continents), yet few studies have attempted to tease apart spatial from climatic factors influencing these communities. Moreover, few studies have sampled in more than 1 year to gauge interannual variation in community structure.

The Pacific Northwest of western North America.

Foliar fungi associated with the deciduous treePopulus trichocarpa.

In two consecutive years, we used DNA metabarcoding to characterize foliar fungal communities ofPopulus trichocarpaacross its geographic range, which encompasses a sharp climatic transition as it crosses the Cascade Mountain Range. We used multivariate analyses to (a) test for and differentiate spatial and environmental factors affecting community composition and (b) test for temporal variation in community composition across spatial and environmental gradients.

In both study years, we found that foliar fungal community composition varied among sites and between regions (east vs. west of the Cascades). We found that climate explained more variation in community composition than geographic distance, although the majority of variation explained by each was shared. We also found that interannual variation in community composition depended on environmental context: communities located in the dry, eastern portion of the tree's geographic range varied more between study years than those located in the wet, western portion of the tree's range.

Our results suggest that the environment plays a greater role in structuring foliar fungal communities than dispersal limitation.

 

Free‐air CO₂enrichment (FACE) experiments have elucidated how climate change affects plant physiology and production. However, we lack a predictive understanding of how climate change alters interactions between plants and endophytes, critical microbial mediators of plant physiology and ecology. We leveraged the SoyFACE facility to examine how elevated [CO₂] affected soybean (Glycine max)leaf endophyte communities in the field. Endophyte community composition changed under elevated [CO₂], including a decrease in the abundance of a common endophyte,Methylobacteriumsp. Moreover,Methylobacteriumabundance was negatively correlated with co‐occurring fungal endophytes. We then assessed howMethylobacteriumaffected the growth of co‐occurring endophytic fungi in vitro.Methylobacteriumantagonized most co‐occurring fungal endophytes in vitro, particularly when it was more established in culture before fungal introduction. Variation in fungal response toMethylobacteriumwithin a single fungal operational taxonomic unit (OTU) was comparable to inter‐OTU variation. Finally, fungi isolated from elevated vs. ambient [CO₂] plots differed in colony growth and response toMethylobacterium, suggesting that increasing [CO₂] may affect fungal traits and interactions within the microbiome. By combining in situ and in vitro studies, we show that elevated [CO₂] decreases the abundance of a common bacterial endophyte that interacts strongly with co‐occurring fungal endophytes. We suggest that endophyte responses to global climate change will have important but largely unexplored implications for both agricultural and natural systems.

 

Fungi play many essential roles in ecosystems. They facilitate plant access to nutrients and water, serve as decay agents that cycle carbon and nutrients through the soil, water and atmosphere, and are major regulators of macro‐organismal populations. Although technological advances are improving the detection and identification of fungi, there still exist key gaps in our ecological knowledge of this kingdom, especially related to function.Trait‐based approaches have been instrumental in strengthening our understanding of plant functional ecology and, as such, provide excellent models for deepening our understanding of fungal functional ecology in ways that complement insights gained from traditional and ‐omics‐based techniques. In this review, we synthesize current knowledge of fungal functional ecology, taxonomy and systematics and introduce a novel database of fungal functional traits (Fun^Fun). Fun^Funis built to interface with other databases to explore and predict how fungal functional diversity varies by taxonomy, guild, and other evolutionary or ecological grouping variables. To highlight how a quantitative trait‐based approach can provide new insights, we describe multiple targeted examples and end by suggesting next steps in the rapidly growing field of fungal functional ecology.