Reciprocal interactions between the sorghum root microbiome and the parasitic weed Striga hermonthica

The soil microbiome can protect plants against fungal and bacterial pathogens, nematodes, and insect pests. However, the impact of the soil microbiome on interactions between plants and parasitic weeds remains largely elusive. Here, susceptible sorghum accession was grown in 22 field soils infested with the root parasitic weed Striga hermonthica seeds. Significant variation in Striga incidence was observed across these soils. Gamma-irradiation of the most Striga-suppressive soil led to a considerable increase in Striga attachments, exemplifying the importance of the soil microbiome in disrupting the parasite's infection cycle. In the presence of the soil microbiome, the Striga susceptible sorghum genotype showed comparable performance to three Striga-resistant sorghum genotypes. This phenotype was lost upon elimination of the soil microbiome by gamma-irradiation. Joint probabilistic model-based analysis revealed that Striga substantially impacts the sorghum rhizosphere microbiome and growth. The sorghum rhizosphere mycobiome and bacteriome members strongly correlated with Striga attachment. Further analyses revealed that some members of the mycobiome were detected in the sorghum rhizosphere only upon challenge with Striga seeds. Subsequent profiling of the Striga seed microbiome and cultivation-based fungal isolation and characterization indicated that most of these fungal taxa detected in the sorghum rhizosphere originated from the Striga seeds. Interestingly, these fungi are characterized as major sorghum pathogens suggesting a potential partnership between the root parasitic weed Striga and fungal pathogens to invade their shared host. In conclusion, our results showed that the soil microbiome affects Striga infection and sorghum performance in a genotype-dependent manner and that the microbiome of Striga seeds determines, at least in part, the sorghum rhizosphere microbiome composition.