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.

Deciphering the mechanism about the mycorrhizal-induced resistance and susceptibility in Populus alba × P. berolinensis seedlings from the perspective of gypsy moth larvae

“…In some cases, this ecological speci city inhibits plant resistance and promotes the growth of harmful insects. In line with our previous studies, the present study revealed that GM and GI treatments respectively induced and decreased the resistance of P. alba × P. berolinensis seedlings to gypsy moth (Jiang et al 2021a;Jiang et al 2022). These results, together with the previous studies, demonstrated that speci c AMF colonization could induce alterations (either increase or decrease) in the plant resistance to insects.…”

“…The systematic investigation of AMF-induced plant resistance from the perspective of insects is still lacking. In our previous studies, we found that the inoculation with Glomus mossae (GM) improved the resistance to gypsy moth larvae in Populus alba × P. berolinensis seedlings, while inoculation with Glomus intraradices (GI) resulted in the opposite effect (Jiang et al 2021a;Jiang et al 2022). In the current study, leaves of P. alba × P. berolinensis inoculated with GM or GI were used to feed gypsy moth larvae, and the mechanism of mycorrhizal induced resistance/susceptibility was depicted at the microbial and metabolic level of gypsy moth larvae by combining the fat body metabolome and the gut microbiome.…”

Arbuscular mycorrhizal fungi inhibit necrotrophic, but not biotrophic, aboveground plant pathogens: a meta‐analysis and experimental study

“…However, there is evidence to suggest that the differential effects of AMF on biotrophic versus necrotrophic pathogens are achieved via similar mechanisms. For instance, in poplars, mycorrhizal fungi regulate flavonoid biosynthesis (Jiang et al ., 2022) and can induce distinct responses in jasmonic acid and salicylic acid pathways (Jiang et al ., 2021). Second, in the meta‐analysis, fewer publications were found for biotrophic pathogens than for necrotrophic pathogens.…”

A snapshot of the transcriptome ofMedicago truncatula(Fabales: Fabaceae) shoots and roots in response to an arbuscular mycorrhizal fungus and the pea aphid (Acyrthosiphon pisum) (Hemiptera: Aphididae)

“…In the study, they show that transcripts associated with JA-dependent defenses and metabolites with insecticidal properties increased in leaves of gypsy moth-damaged, mycorrhizal poplar seedlings (Jiang et al 2021). Contrastingly, in a separate study, they found that gypsy moth-damaged, mycorrhizal poplar seedlings accumulated biomass but had reduced resistance to gypsy moth larvae (Jiang et al 2022). Taken together, these findings highlight the complexity of tripartite interactions.…”