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Abstract

Arbuscular mycorrhizal fungi (AMF) establish symbiotic associations with a majority
of terrestrial plants to form underground common mycorrhizal networks (CMNs) that
connect neighbouring plants. Because Nicotiana attenuata plants do not respond to
herbivory‐elicited volatiles from neighbours, we used this ecological model system
to evaluate if CMNs function in interplant transmission of herbivory‐elicited
responses. A mesocosm system was designed to establish and remove CMNs linking
N. attenuata plants to examine the herbivory‐elicited metabolic and hormone
responses in CMNs‐connected “receiver” plants after the elicitation of “donor” plants
by wounding (W) treated with Manduca sexta larval oral secretions (OS). AMF colonization
increased constitutive jasmonate (JA and JA‐Ile) levels in N. attenuata roots but
did not affect well‐characterized JAs‐regulated defensive metabolites in systemic
leaves. Interestingly, larger JAs bursts, and higher levels of several amino acids and
particular sectors of hydroxygeranyllinalool diterpene glycoside metabolism were elevated
in the leaves of W + OS‐elicited “receivers” with CMN connections with
“donors” that had beenW + OS‐elicited 6 hr previously. Our results demonstrate that
AMF colonization alone does not enhance systemic defence responses but that sectors
of systemic responses in leaves can be primed by CMNs, suggesting that CMNs
can transmit and even filter defence signalling among connected plants.