microRNA390 modulates Nicotiana attenuata's tolerance response to Manduca sexta herbivory

Abstract miR390 is a highly conserved miRNA in plant lineages known to function in growth and development processes, such as lateral root development, and in responses to salt and metal stress. In the ecological model species, Nicotiana attenuata, miR390's biological function remains unknown, which we explore here with a gain‐of‐function analysis with plants over‐expressing (OE‐) N. attenuata miR390 (Na‐miR390) in glasshouse and natural environments. OEmiR390 plants showed normal developmental processes, including lateral root formation or reproductive output, in plants grown under standard conditions in the glasshouse. OEmiR390 plants did not have dramatically altered interactions with arbuscular mycorrhizal fungi (AMF), Fusarium pathogens, or herbivores. However, Na‐miR390 regulated the plant's tolerance of herbivory. Caterpillar feeding elicits the accumulation of a suite of phytohormones, including auxin and jasmonates, which further regulate host‐tolerance. The increase in Na‐miR390 abundance reduces the accumulation of auxin but does not influence levels of other phytohormones including jasmonates (JA, JA‐Ile), salicylic acid (SA), and abscisic acid (ABA). Na‐miR390 overexpression reduces reproductive output, quantified as capsule production, when plants are attacked by herbivores. Exogenous auxin treatments of herbivore‐attacked plants restored capsule production to wild‐type levels. During herbivory, Na‐miR390 transcript abundances are increased; its overexpression reduces the abundances of auxin biosynthesizing YUCCA and ARF (mainly ARF4) transcripts during herbivory. Furthermore, the accumulation of auxin‐regulated phenolamide secondary metabolites (caffeoylputrescine, dicaffeoylspermidine) is also reduced. In N. attenuata, miR390 functions in modulating tolerance responses of herbivore‐attacked plants.