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• Phytobiome management in horticultural systems: beyond the rhizosphere toward whole-plant microbiome optimization

  85-101.

  Mohammad Ahmad

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  The plant microbiome is not confined to the soil. Across every anatomical compartment, the rhizosphere, phyllosphere, endosphere, anthosphere, spermosphere, and carposphere, structurally distinct and functionally specialized microbial communities orchestrate processes fundamental to plant health, productivity, and resilience. Yet horticultural science has remained disproportionately anchored to the rhizosphere, leaving the vast microbial landscape inhabiting aerial, floral, seed, and fruit tissues largely unexplored and unmanaged. This blind spot carries profound consequences at a time when global horticultural production confronts an unprecedented convergence of pressures: accelerating climate instability, stringent restrictions on synthetic agrochemicals, mounting soil degradation, and escalating consumer demand for sustainably produced, chemical-free, premium-quality produce. The biological potential embedded within the whole-plant phytobiome to address these intersecting crises remains critically underutilized. A fundamental barrier to progress is the absence of a unifying scientific framework. Existing reviews address plant-associated microbiomes in disciplinary silos, focusing narrowly on rhizosphere bacteria, individual crop species, or single microbial kingdoms, without synthesizing the full cross-compartment, cross-kingdom phytobiome in the horticultural context. No comprehensive framework has yet integrated microbial community dynamics spanning bacteria, fungi, archaea, and viruses across fruit, vegetable, and ornamental crops within a single, coherent, and practically applicable model. This review addresses that gap directly. Through critical synthesis of compartment-resolved phytobiome research across major horticultural systems, we characterize the taxonomic composition, ecological assembly drivers, and agronomic functional roles of microbial communities inhabiting each plant compartment. We demonstrate that phyllosphere microbiomes confer photoprotection and pathogen exclusion; endophytic communities directly modulate secondary metabolite profiles and systemic immunity; anthosphere microbiomes influence pollinator attraction and fruit set; spermosphere communities determine seedling establishment success through vertical microbial inheritance; and carposphere microbiomes govern post-harvest storability and food safety outcomes. We further establish how host genotype, crop developmental stage, management-induced dysbiosis, and climate-driven perturbations collectively shape phytobiome assembly and functional integrity across compartments. Building on this synthesis, proposing to introduce the Whole-Plant Phytobiome Optimization (WPPO) framework, the first integrative, three-tier conceptual model designed specifically for horticultural systems. WPPO encompasses whole-plant phytobiome profiling using multi-omics platforms, identification of functional microbial modules linked to target agronomic traits, and precision compartment-targeted intervention through synthetic microbial communities (SynComs), encapsulated biostimulants, and digitally guided delivery systems integrated with IoT sensor networks and machine learning decision-support tools. Applied across the full crop life cycle, from spermosphere conditioning at seed priming to carposphere biopreservation at post-harvest, WPPO offers a scalable, evidence-based, and technologically integrated roadmap toward substantially reduced agrochemical dependence, enhanced crop resilience, superior produce quality, and the deployment of ecologically precise next-generation biocontrol and biostimulant strategies.