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

Abstract

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. Author Summary