Domestication Compromised Microbiome-Mediated Resistance to Western Corn Rootworm in Maize

Western corn rootworm (WCR) ( Diabrotica virgifera virgifera ) represents a significant threat to global maize production, with annual costs exceeding $1 billion. While modern maize is highly susceptible, wild teosinte ( Zea mays ssp. parviglumis ) exhibits superior resistance through poorly understood mechanisms. This study investigated rhizosphere microbiome contributions to WCR resistance across the domestication gradient. We screened 23 accessions (15 wild teosinte accessions, 6 ancestral maize accessions, 2 modern maize accessions) for WCR resistance and analyzed rhizosphere microbiomes of selected resistant and susceptible accessions using Oxford Nanopore sequencing. Resistant accessions retained >80% of root structure (85.4% ± 3.2%) while supporting minimal larval survival (22.5% ± 4.8%) compared to susceptible accessions (46.7% ± 5.1% root retention, 78.6% ± 6.3% larval survival; P < 0.001). Resistant accessions recruited significantly more diverse bacterial communities under WCR pressure, with 28-31 enriched species versus 7-19 in susceptible accessions. Key enriched taxa included Pseudomonas putida (3.0-3.2-fold), Stenotrophomonas maltophilia (2.7-2.9-fold), and Bacillus subtilis , all possessing documented insecticidal properties. Functional analysis revealed enrichment of defense-related pathways in resistant accessions, including hydrogen cyanide production and antimicrobial compound synthesis. Wild teosinte showed the strongest responses, with significant diversity increases (P < 0.0001) and 31 enriched species under WCR herbivory. Modern maize exhibited attenuated responses regardless of resistance classification, suggesting domestication compromised plant-microbiome defensive interactions. These findings demonstrate that WCR resistance involves coordinated plant-microbiome networks and identify bacterial taxa with biocontrol potential for developing sustainable management strategies.

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