Engineering plant holobionts for climate-resilient agriculture

Abstract

The plant holobiont - an integrated unit of the host and its microbiome - has co-evolved through ecological and genetic interactions. Microbiome engineering offers a promising route to enhance resilience in response to climate stress, soil degradation, and yield stagnation. This review presents an integrated framework combining microbial ecology, synthetic biology, and computational modeling to rationally design synthetic microbial communities (SynComs) for agriculture. We outline ecological principles - priority effects, keystone taxa, and functional redundancy - that shape microbiome assembly and guide SynCom design. Strategies like CRISPR interference, biosensor circuits, and quorum-sensing modules enable programmable microbial functions. We also highlight the predictive potential of in silico modeling - including genome-scale metabolic models, dynamic flux balance analysis, and machine learning - to simulate interactions, optimize SynCom composition, and enhance design accuracy. To bridge lab and field, we discuss native microbial chassis, encapsulation, and precision delivery as tools for scalable, ecosystem-integrated deployment. We introduce the concept of the programmable holobiont: an engineered plant-microbe partnership capable of dynamic feedback, interkingdom signaling, and ecological memory. This systems-level perspective reframes plants as designable ecosystems. By synthesizing cross-disciplinary advances, we offer a roadmap for climate-resilient agriculture, where engineered microbiomes improve sustainability, yield stability, and environmental adaptation.