Genomic basis of biodiversity effect in cultivar mixture of natural and crop plant species

Conserving biodiversity while ensuring food security is a critical global challenge and a core component of the United Nations Sustainable Development Goals. Although chemical pesticides substantially contribute to crop protection, their negative effects on insect biodiversity highlight the need for more sustainable approaches. Associational resistance, which is reduced herbivore or pathogen damage achieved through specific combinations of plant genotypes through a positive biodiversity effect, may help balance productive agriculture with ecological conservation.

To identify genotype combinations that promote associational resistance to herbivory and fungal diseases, we developed “Neighbor GWAS,” a genome-wide association method that incorporates spatial interactions among individuals to evaluate neighbor effects at the genetic level using Ising model. We quantified the interactions using 199 genotypes of the model plant species Arabiodpsis thaliana in two years of open-field experiments in Switzerland and Japan. Machine-learning analyses predicted that 823 of 19,701 possible genotype pairs could enhance resistance in mixed plantings. Experimental validation using three selected pairs showed 18–30% reductions in herbivore damage in mixtures compared with monocultures, supporting the genomic prediction using the Neighbor GWAS approach. Furthermore, LASSO regression suggested that the genetic pathway of the volatile plant hormone jasmonic acid may be involved in the plant-plant communication in the associational resistance.

We here applied Neighbor GWAS to disease phenotypes in a crop species barley. We compiled the CIMMYT Australia ICARDA Germplasm Evaluation (CAIGE) data. Neighbor genotypic identity explained 10–30% of phenotypic variation in three fungal disease traits. In addition, two significant or marginal loci were identified on chromosome 7H, where allelic mixtures were associated with reduced severity of net form net blotch and scald. These findings indicate that specific allelic combinations can contribute to disease resistance through positive neighbor-mediated interactions.

Together, this work highlights associational resistance as a practical and ecologically grounded strategy to improve pest and disease management while reducing reliance on pesticides. Because Neighbor GWAS is compatible with existing genomic resources for many crop species, it provides a promising tool for designing genotype mixtures that simultaneously sustain agricultural productivity and contribute to biodiversity conservation.