Potential and challenges for application of microbiomes in agriculture

The plant microbiome can promote plant health and productivity through a multitude of mechanisms. Our understanding of plant microbiome interaction relies on descriptive natural surveys and experiments performed under simplified laboratory environments. While reductionist approaches are essential to understand mechanisms of plant-microbiome interactions, they risk missing emergent community properties seen in nature. To bridge the gap between basic research and real-world deployment of the microbiome for translational application, one has to consider both functional association as well as ecological principles governing interspecies and interkingdom interactions. In this review, we discuss the beneficial potential of plant microbiomes to enhance plant growth, nutrition, stress tolerance, pathogen protection and commercial value through the modulation of taste and flavors, using examples from both model plants and agriculturally important crops. We then discuss how microbial invasion and persistence in standing communities, tradeoffs under multiple stressors and community instability under host- and environment-imposed modulation should be considered in the rational design of microbial inocula, followed by a scrutiny of the method of microbial delivery. We synthesize ideas on how multiomic data including genomics, transcriptomes and metabolomics can be leveraged to identify strains or target genes of interest for functional studies, and how machine learning algorithms can be incorporated to enable prediction of plant microbiome interactions. Microbiome-based strategies hold promise for improvements in agriculture. Despite the intrinsic complexity of the underlying interactions, interdisciplinary approaches are constantly providing insight into microbiome functioning and assembly principles, which is key towards knowledge-based engineering of the microbiome for increased and sustainable crop performance.