From rhizosphere dialogue to holobiont resilience: The plant–microbiome interface as a model for drought adaptation

The concept of the plant holobiont, which encompasses the host plant along with associated microbial communities—such as bacteria, fungi, archaea, protists, algae, and viruses—marks a substantial shift in our understanding of how plants respond to drought. This review brings together current understanding of the molecular interactions between plants and their associated microbiomes that play a role in developing resilience to water scarcity. We explore the deep evolutionary roots of plant-microbe relationships, showing that drought tolerance is not just an intrinsic trait of plants but a co-evolved feature of the holobiont. At the rhizosphere interface, intricate signaling networks, like the "cry-for-help" strategy, orchestrate the assembly of the microbiome during times of stress. Beneficial microbes employ five distinct strategies for self-protection: forming biofilms with extracellular polymeric substances, producing osmoprotectants, utilizing antioxidants, modifying phytohormones (notably via ACC deaminase), and releasing signaling molecules. These components function collaboratively at various tiers, ranging from offering direct physical defence to preparing the entire system for optimal performance. The genetic structure of the host plays a significant role in the recruitment of the microbiome in a way that can be inherited, thereby supporting strategies for breeding that leverage the microbiome. Ecological factors, including legacy effects, land-use context, and meta-holobiont networks, significantly contribute to resilience. To implement these concepts effectively, we must employ a combination of synthetic consortia, bio stimulants, and responsible soil management. Other plant compartments, including the phyllosphere, endosphere, and spermosphere, contribute to the function of the holobiont. However, their roles in drought responses are less well defined, making them potential subjects for further study.