Symbiosis and stress: how plant microbiomes affect host evolution

Existing paradigms for plant microevolution rarely acknowledge the potential impacts of diverse microbiomes on evolutionary processes. Many plant-associated microorganisms benefit the host via access to resources, protection from pathogens, or amelioration of abiotic stress. In doing so, they alter the plant's perception of the environment, potentially reducing the strength of selection acting on plant stress tolerance or defence traits or altering the traits that are the target of selection. We posit that the microbiome can affect plant microevolution via (1) manipulation of plant phenotypes in ways that increase plant fitness under stress and (2) direct microbial responses to the environment that benefit the plant. Both mechanisms might favour plant genotypes that attract or stimulate growth of the most responsive microbial populations or communities. We provide support for these scenarios using infectious disease and quantitative genetics models. Finally, we discuss how beneficial plant-microbiome associations can evolve if traditional mechanisms maintaining cooperation in pairwise symbioses, namely partner fidelity, partner choice and fitness alignment, also apply to the interactions between plants and diverse foliar and soil microbiomes. To understand the role of the plant microbiome in host evolution will require a broad ecological understanding of plant-microbe interactions across both space and time. This article is part of the theme issue 'The role of the microbiome in host evolution'.