Abstract
Arbuscular mycorrhizal (AM) fungi may help protect plants against herbivores; however, their use for the pest control of woody plants requires further study. Here, we investigated the effect of Glomus mosseae colonization on the interactions between gypsy moth larvae and Populus alba × P. berolinensis seedlings and deciphered the regulatory mechanisms underlying the mycorrhizal-induced resistance in the leaves of mycorrhizal poplar using RNA-seq and nontargeted metabolomics. The resistance assay showed that AM fungus inoculation protected poplar seedlings against gypsy moth larvae, as evidenced by the decreased larval growth and reduced larval survival. A transcriptome analysis revealed that differentially expressed genes (DEGs) were involved in jasmonic acid biosynthesis (lipoxygenase, hydroperoxide dehydratase, and allene oxide cyclase) and signal transduction (jasmonate-ZIM domain and transcription factor MYC2) and identified the genes that were upregulated in mycorrhizal seedlings. Except for chalcone synthase and anthocyanidin synthase, which were downregulated in mycorrhizal seedlings, all DEGs related to flavonoid biosynthesis were upregulated, including 4-coumarate-CoA ligase, chalcone isomerase, flavanone 3-hydroxylase, flavonol synthase, and leucoanthocyanidin reductase. The metabolome analysis showed that several metabolites with insecticidal properties, including coumarin, stachydrine, artocarpin, norizalpinin, abietic acid, 6-formylumbelliferone, and vanillic acid, were significantly accumulated in the mycorrhizal seedlings. These findings suggest the potential of mycorrhiza-induced resistance for use in pest management of woody plants and demonstrate that the priming of JA-dependent responses in poplar seedlings contributes to mycorrhiza-induced resistance to insect pests.
Highlights
Arbuscular mycorrhizal (AM) fungi (AMF) that belong to the subphylum Glomeromycotina occur in soil and are widely distributed in agroforestry ecosystems
To study the resistance of woody plants that were colonized with AM fungus to insects, we analyzed the growth and survival of gypsy moth larvae that fed on the leaves of P. alba × P. berolinensis seedlings in which the roots were colonized with G. mosseae or control leaves from plants without mycorrhizal colonization
We investigated the outcome of insect–plant–microbe interactions with a focus on P. alba × P. berolinensis seedlings, gypsy moth larvae, and G. mossae
Summary
Arbuscular mycorrhizal (AM) fungi (AMF) that belong to the subphylum Glomeromycotina occur in soil and are widely distributed in agroforestry ecosystems. AM symbiosis triggers a systemic effect on underground and epigeous portions of plants beyond nutritional benefits, including improving photosynthetic processes, promoting changes in primary and secondary metabolism, enhancing reactive oxygen scavenging ability, and maintaining water uptake, osmotic potential and cell membrane integrity[6,7] These alterations imply that root colonization by AMF affects plant growth but can regulate plant responses to biotic (e.g., bacterial pathogens and nematodes) or abiotic stress (e.g., climatic changes, water deficit, and heavy metal pollution)[8]. During their lengthy interaction with phytophagous insects, plants have evolved defense mechanisms to reduce herbivore damage. It appears that the outcome of the mycorrhizal plant-herbivore interaction may vary with the AMF, host plant, and insect species involved as well as environmental factors
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