Morphogenesis and metabolomics reveal the compatible relationship among Suillus bovinus , Phialocephala fortinii , and their co-host, Pinus massoniana

Abstract

Ectomycorrhizal (ECM) fungi and dark septate endophytes (DSEs) can both form a symbiotic relationship with the same host plant. However, the interactions that occur among these two types of fungi and their co-hosts are largely unknown. Here, we investigated interactions that occur among the ECM fungus Suillus bovinus , the DSE Phialocephala fortinii , and their co-host Pinus massoniana . We used both scanning electron microscopy and optical microscopy to characterize the morphogenesis of the two symbionts and employed the ultra-high-performance liquid chromatography–tandem mass spectrometry technique to assess the effects of fungal inoculation on the root metabolome. Under pure culture conditions, no synergistic or antagonistic effects were observed between Phi. fortinii and S. bovinus . Generally, S. bovinus and Phi. fortinii can simultaneously colonize P. massoniana roots without affecting each other’s symbiotic processes. S. bovinus can colonize the root locus where Phi. fortinii has already invaded but not vice versa, which may be due to the physical barrier effect of the mantle. Both fungi can significantly promote the growth of P. massoniana , and they have a synergistic effect on host N and K uptake. Metabolite accumulation patterns in roots inoculated with Phi. fortinii and/or S. bovinus were greatly altered, especially with respect to organic acids, flavonoids, lipids, and phenolic acids. S. bovinus inoculation significantly enhanced root flavonoid biosynthesis, whereas Phi. fortinii and dual-inoculation treatments mainly induced phenylpropanoid biosynthesis. These findings reveal compatible relationships among P. massoniana , S. bovinus , and Phi. fortinii , and suggest a theoretical basis for ECM fungi and DSE co-application when cultivating seedlings. IMPORTANCE The prevalence of both ectomycorrhizal fungi and dark septate endophytes in the roots of a wide spectrum of tree species is well recognized. In this study, we investigated the interactions that occur among the ECM fungus S. bovinus , the DSE Phi. fortinii , and their co-host, P. massoniana . The two fungi can simultaneously colonize P. massoniana roots without affecting each other’s symbiotic processes. S. bovinus appears to be superior to Phi. fortinii in microniche competition, which may be due to the physical barrier effect of the mantle. The two fungi have different effects on root metabolite accumulation patterns. S. bovinus inoculation significantly enhanced root flavonoid biosynthesis, whereas Phi. fortinii and dual-inoculation treatments mainly induced phenylpropanoid biosynthesis. This is the first study revealing the morphological and metabolic mechanisms that contribute to the compatible relationship among ECM fungi, DSEs, and their co-host.

Mycorrhizal and endophytic fungi structure contrasting but interdependent assembly processes in forest below-ground symbiosis

“…Such priority effects (Fukami, 2015) may be stronger in ectomycorrhizal fungal communities (Kennedy, 2010) than in arbuscular mycorrhizal fungal communities (Werner and Kiers, 2015) potentially because ectomycorrhizal fungi can defend their territories by forming dense hyphal structures (mantles) surrounding host roots (Smith and Read, 2008). Potentially due to the defensive abilities of ectomycorrhizal fungi, the inferred negative interations between ectomycorrhizal fungi and fungi in other ecological guilds (Table 3) may be asymmetric (Sun et al, 2023). Indeed, an experimental study has shown that ectomycorrhizal fungi can impose asymmetric suppressive impacts on root-endophytic fungi (Reininger & Sieber, 2012).…”

Bioassay-guided isolation of three new alkaloids from Suillus bovinus and preliminary mechanism against ginseng root rot

“…Suillus bovinus , an edible mushroom belonging to the Suillus genus, is broadly distributed across various regions globally ( Feng et al, 2022 ). In recent years, research about S. bovinus focus mainly on the mechanisms related to symbiotic interactions with trees ( Sun et al, 2023 ). Additionally, the pharmacological studies indicated that S. bovinus possessed the effect of inhibiting CYP enzymes ( Huang et al, 2009 ).…”

Chromosome-Level Assembly and Comparative Genomic Analysis of Suillus bovinus Provides Insights into the Mechanism of Mycorrhizal Symbiosis

“…It also contains anticancer substances, with antitumor, antioxidant, and anti-inflammatory effects, thus providing both medicinal and edible benefits [ 4 , 5 ]. However, with unique growth and development characteristics, the domestication and artificial cultivation of this fungus remain challenging [ 6 , 7 ]. Thus, there is growing interest in understanding the mycorrhizal formation process of S. bovinus , as well as the underlying molecular mechanisms to facilitate strategies for the effective cultivation of this ECM fungus.…”