The mycorrhizal-induced growth promotion and insect resistance reduction in Populus alba × P. berolinensis seedlings: a multi-omics study

Abstract Arbuscular mycorrhizal (AM) fungi are an alternative to chemical insecticides or fertilizers, and there is an urgent need to extend the application of AM fungi to woody plants. This study aims to investigate the growth and resistance against the gypsy moth larvae (Lymantria dispar) in Glomus intraradices-colonized Populus alba × P. berolinensis seedlings, and to unravel the transcriptome and metabolome phenotypes recruited by AM fungus colonization that affect plant growth and insect resistance. Our results showed a positive mycorrhizal growth response, i.e., growth and biomass of mycorrhizal seedlings were enhanced. However, AM fungus inoculation reduced the resistance of poplar to gypsy moth larvae, as evidenced by the decreased carbon/nitrogen ratio in leaves, as well as the increased larval growth and shortened larval developmental duration. Transcriptome analysis revealed that in both auxin and gibberellin signaling transductions, all nodes were responsive to AM symbiosis and most differentially expressed genes belonging to effectors were up-regulated in mycorrhizal seedlings. Furthermore, the two key enzymes (4-coumarate-CoA ligase and trans-cinnamate 4-monooxygenase) involved in the synthesis of p-Coumaroyl-CoA, an initial metabolite in flavonoid biosynthesis and the first rate-limiting enzyme (chalcone synthase) in flavonoid biosynthesis, were down-regulated at the transcriptional level. Consistent with the transcriptome results, metabolome analysis found that the amounts of all differentially accumulated flavonoid compounds (e.g., catechin and quercetin) identified in mycorrhizal seedlings were decreased. Taken together, these findings highlight the diverse outcomes of AM fungi–host plant–insect interaction and reveal the regulatory network of the positive mycorrhizal growth response and mycorrhizal-induced reduction of insect resistance in poplar.