Plant holobionts in a changing climate: Genome–microbiome integration for sustainable food systems

Achieving global food security under accelerating climate change remains one of the greatest challenges to sustainable agriculture and is central to the United Nations Sustainable Development Goal 2 (Zero Hunger). Although, conventional crop improvement has primarily focused on host genetics, increasing evidence indicates that plants function as holobionts, in which the host and its associated microbiome collectively influence plant growth, nutrient acquisition, stress tolerance, disease resistance and overall productivity. Harnessing these interactions offers new opportunities for developing climate-resilient crops. This review synthesizes recent advances in integrating genome-wide association studies (GWAS) with plant microbiome research to elucidate the genetic basis of host–microbe interactions. We discuss microbiome-mediated GWAS (mGWAS), metagenome-wide association studies (MWAS), and complementary multi-omics approaches that extend classical GWAS by incorporating microbial taxa, functional genes, metabolites and community traits as quantitative phenotypes. These integrative frameworks enable the identification of microbiome-associated host genes (M genes) that regulate microbial recruitment, assembly and function, thereby linking host genetics with complex agronomic traits. We further summarize evidence from cereals, legumes, and oilseed crops demonstrating that often. Particular emphasis is placed on the transition from statistical association to biological causation through CRISPR-based functional validation, synthetic microbial communities (SynComs), and artificial intelligence-assisted multi-omics analyses. Together, these advances establish the microbiome as a heritable and selectable component of crop improvement. Integrating host genetics with beneficial microbial communities through holobiont-aware breeding and designer microbiomes represents a transformative strategy for enhancing crop productivity, resilience, and sustainability under changing climatic conditions.