Herbivory and Soil Water Availability Induce Changes in Arbuscular Mycorrhizal Fungal Abundance and Composition.

We tested the prediction that abundance and composition of arbuscular mycorrhizal fungi (AMF) in Ipomopsis aggregata roots and soils are influenced by ungulate herbivory and drought conditions by examining the effects in a field setting over two years. We used a multi-metric approach to quantify AMF root colonization, AMF reproduction, and AMF community composition in roots and soils. We incorporated complimentary community characterization assays by morphologically identifying spores from trap cultures and the use of terminal restriction fragment length polymorphism (T-RFLP) fingerprinting. Herbivory caused a twofold increase in spore production, an increase in AMF taxa diversity in roots, and a shift in AMF species composition in rhizosphere soils. The impact of herbivory was dependent on water availability, which differed in the two contrasting years. This study demonstrates that both soil water availability and herbivory shape arbuscular mycorrhizal fungi communities. The changes to mycorrhizal communities may help in understanding mycorrhizal function in changing climates.

Belowground fungal associations and water interact to influence the compensatory response of Ipomopsis aggregata.

Although the concept that some plants benefit from being eaten is counterintuitive, there is now considerable evidence demonstrating enhanced fitness following herbivory. It has been assumed that plants growing in high resource conditions are the ones best able to compensate for herbivory. However, just the opposite has been found for dicotyledonous plants exhibiting patterns of overcompensation, with most occurring in resource-poor conditions. Long-term studies of the monocarpic biennial, scarlet gilia, Ipomopsis aggregata growing in resource-poor conditions have shown that ungulate herbivory by mule deer and elk can result in a threefold increase in plant fitness over uneaten controls. These observations led us to hypothesize that fungal associations would facilitate the compensatory response most commonly observed in this Arizona population of scarlet gilia; perhaps mutualistic associations with fungi, such as arbuscular mycorrhizal fungi, would explain the phenomenon of overcompensation altogether. Fungal removal experiments, using Captan®, a commercially available fungicide, showed that a reduction in fungal abundance altered the compensatory response following ungulate herbivory, particularly in years in which water was limited, increasing fitness compensation from equal compensation to overcompensation. A multifactorial experiment revealed that the interactive effects of water and fungicide maximized fruit production following herbivory. Our results are counter to the "modification of tolerance hypothesis" in which plants associating with mycorrhizal fungi will have higher tolerance to herbivory. It is likely that arbuscular mycorrhizal fungi and dark septate endophytes compete with plants for photosynthates following herbivory, thereby limiting the magnitude of compensation. Thus, fungi appear to be parasitic on scarlet gilia following ungulate herbivory.

Shifting microbial communities can enhance tree tolerance to changing climates.

Climate change is pushing species outside of their evolved tolerances. Plant populations must acclimate, adapt, or migrate to avoid extinction. However, because plants associate with diverse microbial communities that shape their phenotypes, shifts in microbial associations may provide an alternative source of climate tolerance. Here, we show that tree seedlings inoculated with microbial communities sourced from drier, warmer, or colder sites displayed higher survival when faced with drought, heat, or cold stress, respectively. Microbially mediated drought tolerance was associated with increased diversity of arbuscular mycorrhizal fungi, whereas cold tolerance was associated with lower fungal richness, likely reflecting a reduced burden of nonadapted fungal taxa. Understanding microbially mediated climate tolerance may enhance our ability to predict and manage the adaptability of forest ecosystems to changing climates.

Genome-Wide Association Studies across Environmental and Genetic Contexts Reveal Complex Genetic Architecture of Symbiotic Extended Phenotypes.

A goal of modern biology is to develop the genotype-phenotype (G→P) map, a predictive understanding of how genomic information generates trait variation that forms the basis of both natural and managed communities. As microbiome research advances, however, it has become clear that many of these traits are symbiotic extended phenotypes, being governed by genetic variation encoded not only by the host's own genome, but also by the genomes of myriad cryptic symbionts. Building a reliable G→P map therefore requires accounting for the multitude of interacting genes and even genomes involved in symbiosis. Here, we use naturally occurring genetic variation in 191 strains of the model microbial symbiont Sinorhizobium meliloti paired with two genotypes of the host Medicago truncatula in four genome-wide association studies (GWAS) to determine the genomic architecture of a key symbiotic extended phenotype-partner quality, or the fitness benefit conferred to a host by a particular symbiont genotype, within and across environmental contexts and host genotypes. We define three novel categories of loci in rhizobium genomes that must be accounted for if we want to build a reliable G→P map of partner quality; namely, (i) loci whose identities depend on the environment, (ii) those that depend on the host genotype with which rhizobia interact, and (iii) universal loci that are likely important in all or most environments. IMPORTANCE Given the rapid rise of research on how microbiomes can be harnessed to improve host health, understanding the contribution of microbial genetic variation to host phenotypic variation is pressing, and will better enable us to predict the evolution of (and select more precisely for) symbiotic extended phenotypes that impact host health. We uncover extensive context-dependency in both the identity and functions of symbiont loci that control host growth, which makes predicting the genes and pathways important for determining symbiotic outcomes under different conditions more challenging. Despite this context-dependency, we also resolve a core set of universal loci that are likely important in all or most environments, and thus, serve as excellent targets both for genetic engineering and future coevolutionary studies of symbiosis.