Despite their ubiquitous distribution and significant ecological roles, soil microorganisms have long been neglected in investigations addressing parasitic plant-host interactions. Because nutrient deprivation is a primary cause of host damage by parasitic plants, we hypothesized that beneficial soil microorganisms conferring nutrient benefits to parasitized hosts may play important roles in alleviating damage. We conducted a pot cultivation experiment to test the inoculation effect of an arbuscular mycorrhizal fungus (Glomus mosseae), a rhizobium (Rhizobium leguminosarum) and their interactive effects, on alleviation of damage to a legume host (Trifolium repens) by two root hemiparasitic plants with different nutrient requirements (N-demanding Pedicularis rex and P-demanding P. tricolor). Strong interactive effects between inoculation regimes and hemiparasite identity were observed. The relative benefits of microbial inoculation were related to hemiparasite nutrient requirements. Dual inoculation with the rhizobium strongly enhanced promotional arbuscular mycorrhizal effects on hosts parasitized by P. rex, but reduced the arbuscular mycorrhizal promotion on hosts parasitized by P. tricolor. Our results demonstrate substantial contribution of arbuscular mycorrhizal and rhizobial symbioses to alleviating damage to the legume host by root hemiparasites, and suggest that soil microorganisms are critical factors regulating host-parasite interactions and should be taken into account in future studies.

In nature, most plants parasitized by root hemiparasites are also colonized by mutualistic arbuscular mycorrhizal (AM) fungi, highlighting the prevalence of this tripartite interaction. AM colonization is generally found to improve the growth of parasitized legumes but has little impact on grass hosts parasitized by root hemiparasites, and the underlying mechanisms are still unclear. In this study, we conducted a pot experiment to test the influence of AM fungus (Glomus mosseae) on the growth and photosynthesis of leguminous Trifolium repens and gramineous Elymus nutans in the presence of a root hemiparasitic plant (Pedicularis kansuensis). The results showed that inoculation with AM fungi significantly improved the growth performance of parasitized legumes via enhancing their nutrient status and photosynthetic capacity, even though a larger P. kansuensis parasitized the legume host in the AM treatment. In contrast, AM colonization slightly improved the shoot DW of grass hosts by suppressing haustoria formation and the growth of P. kansuensis. Our results demonstrated that legume hosts benefit more from AM inoculation than grass hosts in the presence of hemiparasitic plants, and set out the various mechanisms. This study provides new clues for parsing the tritrophic interaction of AM fungi, parasitic plants, and host plants.

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