Holobiont-based genetic analysis reveals new plant and microbial markers for resistance against a root rot pathogen complex in pea

The pea root rot complex is caused by various soil-borne pathogens that likely reinforce each other, influencing the composition of the root microbiome and leading to significant yield reductions. Previous studies have shown variations in the abundance of key microbial taxa and differences in disease susceptibility among plant genotypes. To better understand this relationship between plant genetics and microbiome dynamics, we conducted genetic analyses focusing on plant health and frequency of microbial taxa. Two hundred fifty-two diverse pea lines were grown in naturally infested soil under controlled conditions, genotyped, assessed for their disease symptoms at the seedling stage, and analyzed the associated root microbial communities using amplicon sequencing. Genome-wide association studies (GWAS) revealed genomic loci that influence the abundance of various fungal and bacterial operational taxonomic units (OTUs). We identified 54 independent quantitative trait loci (QTLs) significantly linked to the abundance of 98 out of 1227 detected OTUs, while an additional 20 QTLs were associated with more than one OTU. The most significant region was found on chromosome 6, influencing 50 OTUs across 10 distinct QTLs. When comparing genomic markers and microbial OTUs as predictors in a genomic prediction model for root rot resistance and seedling emergence, we found that the abundance of specific microbial groups provided a significantly better predictive ability than QTLs. The abundance of Fusarium species was correlated with increased infection levels, while others, such as those linked to Dactylonectria and Chaetomiaceae, positively correlated with resistance to root rot. These findings were validated by specific QTLs and high genetic heritability for OTU abundance. The results highlight two key points: (1) the presence and abundance of certain microbial groups in the pea root are influenced by distinct QTLs and, thus, determined by the plant genotype, and (2) these microbial communities show heritable correlations with the plant resistance to root rot. By combining plant and microbiome genetic markers—using a “holobiont” approach—we can improve predictions of root rot resistance compared to predictions based on plant genetics alone. These findings set a foundation for practical applications in breeding programs aimed at enhancing disease resistance through microbiome-assisted approaches.