<p>Drought is a major constraint to global crop productivity, underscoring the need to understand how plant molecular responses, root morphological traits, and microbiome functions jointly confer stress resilience. This review synthesizes advances from 2015 to 2025, integrating transcription factor (TF) networks, root hair dynamics, exudate chemistry, microbial metabolism, and emerging SynCom design frameworks. Literature was systematically surveyed across multi-omics, physiological, and microbiome engineering studies, focusing on transcriptomics, metabolomics, metagenomics, and controlled perturbation assays. Findings reveal that drought resilience arises from coordinated plant–microbe interactions governed by TF families such as DREB, NAC, MYB, and WRKY and mediated through ABA-, JA-, and SA-dependent signaling. These pathways regulate root hair proliferation and exudate release and structure microbial recruitment. Microbes including actinomycetes, Bacillus spp., and arbuscular mycorrhizal fungi contribute through osmolyte production, exopolysaccharides, ACC deaminase activity, and stress-responsive metabolic pathways. Microbiome feedback loops further reinforce water-use efficiency, oxidative balance, and nutrient acquisition. Discussion highlights three mechanistic themes: (1) bidirectional host–microbe signaling shaping exudate composition and microbial functional shifts; (2) stress-driven reorganization of rhizosphere ecological networks; and (3) metabolic integration within the holobiont supporting drought recovery. Knowledge gaps remain concerning causal inference, microbiome ecological memory, and the predictability of genotype × microbiome × environment (G×M×E) interactions. The review concludes that progress depends on embedding mechanistic insights into explicit design rules for microbiome-informed breeding and SynCom engineering. Recommendations include standardized multi-omics workflows, causal validation through SynCom perturbation, and long-term field trials to test durability. These steps form a translational pipeline toward developing climate-resilient crop holobionts.</p> Graphical abstract <p></p>

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Plant-microbiota interactions under drought stress: genetic and ecological mechanisms shaping drought-resistant rhizospheres

  • Zhe Wang,
  • Huanqing Huang,
  • Haifang Liu,
  • Chenyu Guo,
  • Jianmin Fan,
  • Lihua Xie,
  • Shiping Cheng

摘要

Drought is a major constraint to global crop productivity, underscoring the need to understand how plant molecular responses, root morphological traits, and microbiome functions jointly confer stress resilience. This review synthesizes advances from 2015 to 2025, integrating transcription factor (TF) networks, root hair dynamics, exudate chemistry, microbial metabolism, and emerging SynCom design frameworks. Literature was systematically surveyed across multi-omics, physiological, and microbiome engineering studies, focusing on transcriptomics, metabolomics, metagenomics, and controlled perturbation assays. Findings reveal that drought resilience arises from coordinated plant–microbe interactions governed by TF families such as DREB, NAC, MYB, and WRKY and mediated through ABA-, JA-, and SA-dependent signaling. These pathways regulate root hair proliferation and exudate release and structure microbial recruitment. Microbes including actinomycetes, Bacillus spp., and arbuscular mycorrhizal fungi contribute through osmolyte production, exopolysaccharides, ACC deaminase activity, and stress-responsive metabolic pathways. Microbiome feedback loops further reinforce water-use efficiency, oxidative balance, and nutrient acquisition. Discussion highlights three mechanistic themes: (1) bidirectional host–microbe signaling shaping exudate composition and microbial functional shifts; (2) stress-driven reorganization of rhizosphere ecological networks; and (3) metabolic integration within the holobiont supporting drought recovery. Knowledge gaps remain concerning causal inference, microbiome ecological memory, and the predictability of genotype × microbiome × environment (G×M×E) interactions. The review concludes that progress depends on embedding mechanistic insights into explicit design rules for microbiome-informed breeding and SynCom engineering. Recommendations include standardized multi-omics workflows, causal validation through SynCom perturbation, and long-term field trials to test durability. These steps form a translational pipeline toward developing climate-resilient crop holobionts.

Graphical abstract