Defense responses of arbuscular mycorrhizal fungus-colonized poplar seedlings against gypsy moth larvae: a multiomics study

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.

Mycorrhizal Inoculation Enhances Nutrient Absorption and Induces Insect-Resistant Defense of Elymus nutans

“…It has been commonly reported in both laboratory and field experiments that plant inoculation with AMF promote growth and increase biomass, a phenomenon considered as the positive mycorrhizal growth response (MGR) ( Bernaola et al, 2018 ; Zhang et al, 2019 ). Positive MGR was previously found to be due to the improved uptake and transfer of nutrients (usually phosphorus and nitrogen) ( Jiang et al, 2021 ), which is consistent with the findings of this study. E. nutans inoculated with F. mosseae significantly increased plant biomass compared to the non-inoculated treatment, in addition to increasing the uptake of nitrogen and phosphorus.…”

“…Mycorrhizal symbiosis as a potential pest control strategy may be an effective alternative to some chemical pesticides in contemporary agriculture ( Jiang et al, 2021 ). However, the applicability of this insect resistance mechanism in alpine forage plants is unknown.…”

“…AMF are obligate biotrophs that ingest plant photosynthetic products ( Dowarah et al, 2021 ) and lipids to support their life cycle ( Jiang et al, 2017 ). AMF symbiosis can help plants to obtain essential nutrients from the soil, such as nitrogen, phosphorus, and potassium, absorb other trace nutrients from resource-deficient soils, and assist plant roots to take-up more water from the soil ( Kayama and Yamanaka, 2014 ; Bhantana et al, 2021 ; Jiang et al, 2021 ). In return, plants supply AMF with carbohydrates and lipids that can be used to develop extensive mycelial networks ( Bernaola et al, 2018 ).…”

“…Arbuscular mycorrhizal fungi confer benefits to their host plant in many ways, including enhancement in nutrient uptake and protection against stressors ( Dowarah et al, 2021 ). Most importantly, AMF inoculation is known to induce the activation of plant resistance and protect plants from phytopathogenic fungi, bacteria, viruses, and herbivores ( Hao et al, 2019 ; Miozzi et al, 2019 ; Jiang et al, 2021 ). Mycorrhizal symbiosis have been reported to respond variably to above-ground insect damage, including positive ( Babikova et al, 2013 ; Meier and Hunter, 2018 ), negative ( Bernaola et al, 2018 ; Bolin et al, 2018 ), and neutral ( Gehring and Bennett, 2009 ) effects on plant defense.…”

Mycorrhizal Symbiosis Triggers Local Resistance in Citrus Plants Against Spider Mites

“…Flavonoids and secondary metabolites have a strong impact on defense against pathogens because of their antimicrobial activity, but they also reduce plant quality to insects, thus reducing the range of hosts (Burghardt et al, 2001). Previous studies confirmed that oxylipins and JA-related responses are tightly regulated in mycorrhized plants (Sanchez-Bel et al, 2018;Jiang et al, 2021;Rivero et al, 2021). LOX and AOS upregulation in myco rrhized poplar is correlated with an increase in 4-coumarate-CoA ligase, chalcone isomerase, and other flavonoid-related genes.…”