Plants

Sustainable improvement of crop performance requires integrative approaches that link genomic variation to phenotypic expression through intermediate molecular pathways. Here, we present Reciprocal Best Linear Unbiased Prediction (Reciprocal BLUP), a predictability-guided multi-omics framework that quantifies the cross-layer relationships among the genome, metabolome, and microbiome to enhance phenotype prediction. Using a panel of 198 soybean accessions grown under well-watered and drought conditions, we first evaluated four direction-specific prediction models (genome → microbiome, genome → metabolome, metabolome → microbiome, and microbiome → metabolome) to estimate the predictability of individual omics features. We evaluated whether subsets of features with high cross-omics predictability improved phenotype prediction. These cross-layer models identify features that play physiologically meaningful roles within multi-omics systems, enabling the prioritization of variables that capture coherent biological signals enriched with phenotype-relevant information. Consequently, metabolome features were highly predictable from microbiome data, whereas microbiome predictability from metabolomic data was weaker and more environmentally dependent, revealing an asymmetric relationship between these layers. In the subsequent phenotype prediction analysis, the model incorporating predictability-based feature selection substantially outperformed models using randomly selected features and achieved prediction accuracies comparable to those of the full-feature model. Under drought conditions, the phenotype prediction models based on metabolomic or microbiomic kernels (MetBLUP or MicroBLUP) outperformed the genomic baseline (GBLUP) for several biomass-related traits, indicating that the environment-responsive omics layers captured phenotypic variations that were not explained by additive genetic effects. Our results highlight the hierarchical interactions among genomic, metabolic, and microbial systems, with the metabolome functioning as an integrative mediator linking the genotype, environment, and microbiome composition. The Reciprocal BLUP framework provides a biologically interpretable and practical approach for integrating multi-omics data, improving phenotype prediction, and guiding omics-based feature selection in plant breeding.

Plants are naturally exposed to various biotic stresses, including pathogen attacks and insect herbivory, which activate distinct signaling pathways as part of their defense responses. Inoculation with beneficial microorganisms, such as plant growth-promoting rhizobacteria (PGPR), can trigger induced systemic resistance (ISR) in plants, a defense response that resembles the one activated by herbivore attack in terms of signaling pathways and physiological effects. However, these interactions have typically been studied independently, limiting our understanding of their combined effects. In this study, we examined the effects of aphid (Acyrthosiphon pisum) herbivory on Ocimum basilicum plants and assessed how these responses are modulated when the plants are inoculated with the PGPR strain Bacillus amyloliquefaciens GB03, with a particular focus on biochemical and structural defense mechanisms. Aphid herbivory significantly increased total essential oil (EO) content and volatile organic compound (VOC) emission and induced a greater density of glandular trichomes while also modifying the phytohormone profile. In contrast, total phenolic content remained unchanged. When aphid herbivory occurred on GB03-inoculated plants, the effects on defense-related parameters became more pronounced. EO and eugenol contents were further increased compared with inoculated controls, jasmonates remained comparable to levels induced by either factor alone, and SA levels nearly doubled relative to aphid-infested plants. Feeding assays revealed that aphids preferred inoculated plants over controls, a response that may be explained by the increased emission of eugenol in inoculated basil. These results demonstrate that GB03 inoculation modifies several defenses-related responses in O. basilicum upon aphid herbivory, including by hormonal signaling, specialized metabolites accumulation, and structural barriers such as glandular trichomes. These findings suggest that PGPR may contribute to modulating plant responses to herbivory under certain conditions, highlighting their context-dependent influence within plant–microbe–insect interactions.

The interaction between plants and phytophagous insects is one of the most complex relationships in ecosystems. By acting as direct third-party participants, gut symbionts redefine this binary antagonistic relationship. This article reviews the roles of gut symbionts in the adaptive evolution of phytophagous insects, highlighting their important roles in degrading plant secondary metabolites, modulating plant defense responses, promoting insect nutrient absorption, and shaping immune phenotypes. Gut symbionts not only enhance the adaptability of insects by degrading plant defense compounds, but also significantly influence their physiological adaptation by manipulating plant defense signaling pathways, regulating the immune system of insects, and promoting their rapid adaptation to external stress. When insects are confronted with environmental changes or shifts of host plants, the dynamic plasticity of the gut symbionts provides them with evolutionary advantages. Reviewing the mechanism of action of intestinal symbiotic bacteria in the adaptive evolution of insects is helpful to deepen our understanding of the ecological interaction process between insects and plants.