Microbiome-Assisted Breeding: Engineering the Holobiont in Horticultural Crops
Abstract
Horticultural crop improvement is moving from a plant-centred model toward a soil-plant-microbiome framework in which host genotype, root-zone biology and the production environment are considered together. Microbiome-assisted breeding (MAB) aims to select plant genotypes that recruit, accommodate or respond to microbial communities capable of improving nutrient acquisition, soil fertility, disease suppression, abiotic-stress resilience, fruit quality and post-harvest performance. This review synthesizes the current basis of holobiont engineering with a primary focus on soil and plant-associated microbes of horticultural crops. The rhizosphere, rhizoplane, root endosphere, seed, flower and fruit compartments are considered as connected but functionally distinct microbial habitats. Important microbial groups include arbuscular mycorrhizal fungi, plant-growth-promoting rhizobacteria, diazotrophs, phosphate-solubilizing bacteria and fungi, actinobacteria, Trichoderma, endophytes, yeasts and defined synthetic communities. Recent literature highlights three developments: regulation of rhizosphere microbiomes by host traits and management, microbiome-interactive traits as potential breeding targets, and rhizosphere hybridization or microbiome engineering to build climate-smart and disease-suppressive soils. However, microbial abundance alone is not evidence of function, and inoculants frequently perform inconsistently when they cannot establish within a compatible native community. A practical MAB pipeline should combine host genotyping, soil physicochemical analysis, 16S/ITS or shotgun sequencing, culturomics, metabolomics, causal inoculation, synthetic-community testing and multi-environment validation. The review proposes priority research pathways for fruit, vegetable, spice, ornamental and underutilized crops and emphasizes that plant genotype × microbiome × soil management interactions must be measured explicitly. MAB should therefore complement—not replace—conventional breeding, crop management, conservation and farmer knowledge.
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Introduction
Horticultural crops are expected to produce high yield, nutritional quality, flavour, appearance and shelf life while facing heat, drought, salinity, soil degradation, emerging pathogens, declining biodiversity and restrictions on agrochemical use. Conventional breeding has delivered major gains, but it generally evaluates the plant phenotype while treating the microbial environment as background. That assumption is increasingly difficult to defend. Roots release carbon compounds, organic acids, amino acids, sugars and signalling molecules that structure the rhizosphere, while soil microorganisms transform nutrients, modify root development, antagonize pathogens and influence plant immunity. The plant is therefore not an isolated genetic entity but a host embedded in a dynamic soil-plant-microbe system [1], [2].
The term holobiont is useful as a systems concept when it describes the interacting host and its microbiota; it should not automatically be interpreted as a single evolutionary unit in every crop or environment. The phytomicrobiome concept places microbial partners at the centre of plant nutrition, resistance and environmental adaptation. Microbiome-assisted breeding extends this view by asking whether a plant genotype can recruit a stable, beneficial and context-compatible microbial community, and whether that host-microbe association remains useful across soils and seasons [3], [4].
Early proposals for microbiome selection suggested reciprocal soil transplantation, artificial ecosystem selection and co-propagation of beneficial microbiota. Recent frameworks have developed this idea toward measurable microbiome-interactive traits, climate-smart crops and plant-microbiome breeding roadmaps. The goal is not simply to add a commercial microbe to soil; it is to select host genotypes and microbial communities that work together under realistic management [5], [6].
This review synthesizes the current state of knowledge on MAB in horticulture, covering soil-plant-microbiome architecture, important microbial groups, mechanisms linking microbes to horticultural traits, breeding frameworks, crop-specific priorities, and challenges for implementation.
Conclusion
Microbiome-assisted breeding provides a practical bridge between plant genetics, soil health and microbial ecology. Its strongest promise lies in selecting horticultural genotypes that recruit and respond to beneficial communities for nutrient-use efficiency, disease suppression, climate resilience, fruit quality and post-harvest stability. The central unit of selection is not necessarily a fixed list of microbes, but a repeatable host-microbiome function that performs under a defined soil and management context [37], [38].
For the next decade, research should prioritize standardized soil metadata, voucher-linked host genotypes, strain-resolved functional assays, causal synthetic communities, rootstock-scion-microbiome interactions and multi-location validation. By 2050, successful horticultural systems may combine genomic selection, microbiome-interactive traits, AI-assisted community design and regenerative soil management. The central test will remain whether a host-microbiome combination provides a safe, stable and economically useful benefit in real fields. MAB should therefore be advanced as a complementary layer of precision breeding and soil stewardship [39], [40].
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