COS 219-6 - Genotype, mycorrhizae, and herbivory interactively shape plant functional traits and the floral microbiome

Background/Question/Methods

Arbuscular mycorrhizal fungi and herbivores are ubiquitous biotic agents affecting plant fitness and are known to influence plant functional trait expression. However, little is known about how these species interact to influence phenotypic plasticity in plants, especially the emissions of phytochemicals such as floral volatile organic compounds (VOCs). Any shifts in the expression of plant traits could potentially influence interactions with additional species, such as floral microbiota and pollinators. We conducted a field-based experiment in which three strawberry (Fragaria x ananassa) genotypes were subjected to mycorrhizal inoculation of roots, above-ground herbivory, and the combined factors in a fully-crossed factorial design. We measured plant physiological, growth, reproductive, and floral volatile emission responses to treatments. A subset of strawberry plants was used to assess how genotype and treatments influenced the bidirectional relationships between floral volatile organic compounds (VOCs) and the floral microbiome using structural equation modeling. We hypothesized that mycorrhizae would mitigate negative herbivore effects on trait expression and that genotypic variation would influence functional trait responses to these biotic agents. Additionally, we hypothesized that genotype and biotic interactions would influence floral microbiome assembly directly and indirectly via floral trait variation.

Results/Conclusions

Mycorrhizal inoculation, herbivory, and genotype were all key determinants of phenotypic variation. Inoculation increased flower and fruit number across herbivory treatments, and enhanced fruit biomass in one genotype by 30-40% depending on herbivory. Inoculation increased total leaf area, but only in plants that received no herbivory. While herbivory altered floral volatile profiles and increased total terpenoid emissions, plant genotype more strongly shaped floral VOC profiles. Genotypic variation in flower abundance and size influenced the emission of floral VOCs, especially terpenes (e.g. α-and β-pinene, ocimene isomers) and benzenoids (e.g., p-anisaldehyde, benzaldehyde), which in turn altered floral bacterial and fungal communities. While the effects of biotic interactions on floral traits were weak, mycorrhizae treatments (mycorrhizae and herbivory + mycorrhizae) affected the fungal community composition in flowers. Here we provide the first evidence that biotic interactions above and below ground can influence the floral microbiome. These findings improve our understanding of how genotype and multitrophic interactions shape trait expression, floral VOC emissions, and in turn, the floral microbiome. Because floral emissions and microbiomes can alter pollinator and natural enemy attraction, and deter herbivores, the documented changes to floral environment have important implications for pollination success and plant fitness.