Auxin Is Rapidly Induced by Herbivore Attack and Regulates a Subset of Systemic, Jasmonate-Dependent Defenses

Abstract

Plant responses to herbivore attack are regulated by phytohormonal networks. To date, the role of the auxin indole-3-acetic acid (IAA) in this context is not well understood. We quantified and manipulated the spatiotemporal patterns of IAA accumulation in herbivore-attacked Nicotiana attenuata plants to unravel its role in the regulation of plant secondary metabolism. We found that IAA is strongly, rapidly, and specifically induced by herbivore attack. IAA is elicited by herbivore oral secretions and fatty acid conjugate elicitors and is accompanied by a rapid transcriptional increase of auxin biosynthetic YUCCA-like genes. IAA accumulation starts 30 to 60 s after local induction and peaks within 5 min after induction, thereby preceding the jasmonate (JA) burst. IAA accumulation does not require JA signaling and spreads rapidly from the wound site to systemic tissues. Complementation and transport inhibition experiments reveal that IAA is required for the herbivore-specific, JA-dependent accumulation of anthocyanins and phenolamides in the stems. In contrast, IAA does not affect the accumulation of nicotine or 7-hydroxygeranyllinalool diterpene glycosides in the same tissue. Taken together, our results uncover IAA as a rapid and specific signal that regulates a subset of systemic, JA-dependent secondary metabolites in herbivore-attacked plants.

Auxin signalling of Arachis hypogaea activated by colonization of mutualistic fungus Phomopsis liquidambari enhances nodulation and N2 -fixation

“…protects tomato against the root nematode Meloidgyne incognita through local and systemic regulation of jasmonic acid (JA) and salicylic acid (SA) signalling and pathogenesis‐related gene expression. Additionally, herbivory Manduca sexta challenge induces IAA both locally and systemically in Nicotiana attenuata (Machado et al, ), regulating the JA‐dependent secondary metabolites. Thus, we speculate that secondary signals, such as electrical potentials, are induced in roots, following P. liquidambari inoculation, spread to the aerial parts of the plants, where it further activates auxin production.…”

“…This inevitably gives rise to the question whether and how fungal symbiosis affects another, especially rhizobial symbiosis. However, the interactions between symbioses from different members from the root microbiome have been largely neglected, with most studies testing the effects of plant symbionts against pathogen and herbivore attacks and environmental stresses (Cosme, Lu, Erb, Stout, & Wurst, ; Fernandez‐Conradi, Jactel, Robin, Tack, & Castagneyrol, ; Machado et al, ; Ruiz‐Lozano et al, ).…”

Aboveground herbivory induced jasmonates disproportionately reduce plant reproductive potential by facilitating root nematode infestation

“…Intact plants were harvested in a similar manner and used as controls. JA and JA‐Ile were quantified as previously described (Ferrieri et al, ; Machado, Robert, et al, ).…”

Flower-specific jasmonate signaling regulates constitutive floral defenses in wild tobacco

“…Therefore, other signaling systems in addition to JA might be involved in the regulation of the constitutive defenses of flowers. In leaves or stems of N. attenuata, ABA, ethylene, and IAA signaling have been shown to be involved in defense responses (72)(73)(74).…”