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Metagenome-enabled models improve genomic predictive ability and identification of herbivory-limiting genes in sweetpotato.

Alhagie K ChamAlison K AdamsPhillip A WadlMa Del Carmen Ojeda-ZacaríasWilliam B RutterD Michael JacksonD Dewayne ShoemakerG Craig YenchoBode A Olukolu
Published in: Horticulture research (2024)
Plant-insect interactions are often influenced by host- or insect-associated metagenomic community members. The relative abundance of insects and the microbes that modulate their interactions were obtained from sweetpotato ( Ipomoea batatas ) leaf-associated metagenomes using quantitative reduced representation sequencing and strain/species-level profiling with the Qmatey software. Positive correlations were found between whitefly ( Bemisia tabaci ) and its endosymbionts ( Candidatus Hamiltonella defensa , Candidatus Portiera aleyrodidarum , and Rickettsia spp . ) and negative correlations with nitrogen-fixing bacteria that implicate nitric oxide in sweetpotato-whitefly interaction. Genome-wide associations using 252 975 dosage-based markers, and metagenomes as a covariate to reduce false positive rates, implicated ethylene and cell wall modification in sweetpotato-whitefly interaction. The predictive abilities (PA) for whitefly and Ocypus olens abundance were high in both populations (68%-69% and 33.3%-35.8%, respectively) and 69.9% for Frankliniella occidentalis . The metagBLUP (gBLUP) prediction model, which fits the background metagenome-based Cao dissimilarity matrix instead of the marker-based relationship matrix (G-matrix), revealed moderate PA (35.3%-49.1%) except for O. olens (3%-10.1%). A significant gain in PA after modeling the metagenome as a covariate (gGBLUP, ≤11%) confirms quantification accuracy and that the metagenome modulates phenotypic expression and might account for the missing heritability problem. Significant gains in PA were also revealed after fitting allele dosage (≤17.4%) and dominance effects (≤4.6%). Pseudo-diploidized genotype data underperformed for dominance models. Including segregation-distorted loci (SDL) increased PA by 6%-17.1%, suggesting that traits associated with fitness cost might benefit from the inclusion of SDL. Our findings confirm the holobiont theory of host-metagenome co-evolution and underscore its potential for breeding within the context of G × G × E interactions.
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