Engineering plant microbiomes by integrating eco-evolutionary principles into current strategies

Engineering plant microbiomes has the potential to improve plant health in a rapid and sustainable way. Rapidly changing climates and relatively long timelines for plant breeding make microbiome engineering an appealing approach to improving food security. However, approaches that have shown promise in the lab have not resulted in wide-scale implementation in the field. Here, we suggest the use of an integrated approach, combining mechanistic molecular and genetic knowledge, with ecological and evolutionary theory, to target knowledge gaps in plant microbiome engineering that may facilitate translatability of approaches into the field. We highlight examples where understanding microbial community ecology is essential for a holistic understanding of the efficacy and consequences of microbiome engineering. We also review examples where understanding plant–microbe evolution could facilitate the design of plants able to recruit specific microbial communities. Finally, we discuss possible trade-offs in plant–microbiome interactions that should be considered during microbiome engineering efforts so as not to introduce off-target negative effects. We include classic and emergent approaches, ranging from microbial inoculants to plant breeding to host-driven microbiome engineering, and address areas that would benefit from multidisciplinary approaches.