Pithy Protection: Nicotiana attenuata’s Jasmonic Acid-Mediated Defenses Are Required to Resist Stem-Boring Weevil Larvae    

Abstract

Folivory is the best studied plant-herbivore interaction, but it is unclear whether the signaling and resistance traits important for the defense of leaves are also important for other plant parts. Larvae of the tobacco stem weevil, Trichobaris mucorea, burrow into stems of Nicotiana attenuata and feed on the pith. Transgenic N. attenuata lines silenced in signaling and foliar defense traits were evaluated in a 2-year field study for resistance against attack by naturally occurring T. mucorea larva. Plants silenced in early jasmonic acid (JA) biosynthesis (antisense [as]-lipoxygenase3 [lox3]; inverted repeat [ir]-allene oxide cyclase), JA perception (as-coronatine insensitive1), proteinase inhibitors (ir-pi), and nicotine (ir-putrescine methyl-transferase) direct defenses and lignin (ir-cad) biosynthesis were infested more frequently than wild-type plants. Plants unable to emit C 6 aldehydes (as-hpl) had lower infestation rates, while plants silenced in late steps in JA biosynthesis (ir-acyl-coenzyme A oxidase, ir-opr) and silenced in diterpene glycoside production (ir-geranylgeranyl pyrophosphate synthase) did not differ from wild type. Pith choice assays revealed that ir-putrescine methyl-transferase, ir-coronatine insensitive1, and ir-lox3 pith, which all had diminished nicotine levels, were preferred by larvae compared to wild-type pith. The lack of preference for ir-lox2 and ir-cad piths, suggest that oviposition attraction and vascular defense, rather than pith palatability accounts for the higher attack rates observed for these plants. We conclude that traits that influence a plant's apparency, stem hardness, and pith direct defenses all contribute to resistance against this herbivore whose attack can be devastating to N. attenuata's fitness.

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

“…The stems of N. attenuata are often attacked by herbivores, including stem borers (Diezel et al, 2011b;Lee et al, 2016), and are very important for plant fitness (Machado et al, 2016). We observed a strong up-regulation of defensive secondary metabolites in the stems in response to M. sexta attack (Fig.…”

“…The stem of N. attenuata is vital for its reproduction and can be attacked by a wide variety of organisms, including vertebrates and invertebrate stem borers (Machado et al, 2016;Diezel et al, 2011b). We observed that real and simulated M. sexta attack induced anthocyanin accumulation in the stems, an effect that could not be reproduced by MeJA or IAA treatments alone, but by the combination of these two hormones.…”

“…unknown, jasmonate-dependent defenses (Diezel et al, 2011b;Lee et al, 2016). It is therefore possible that the IAA-triggered potentiation of jasmonate-dependent secondary metabolite accumulation in the stems may reduce the performance of stem feeders.…”

Phylogeography of specialist weevil Trichobaris soror: a seed predator of Datura stramonium

“…In fact, according to the geometric morphometric analysis, genetic analysis, and Barber's descriptions (1935), this group seems to belong to Trichobaris mucorea, a species reported parasitizing Datura wrightii and other solanaceous plants such as Nicotiana attenuata (Barber 1935;Diezel et al 2001). b Transformation grid of CV1 describe the shape of T. soror's aedeagi, whereas c CV2 describes the shape of weevils found in RC population Finally, this work is the first phylogeographic study of a species of the Trichobaris genus, which includes many species that are pests of potato, tomato, and tobacco crops.…”

Environmental Stresses of Field Growth Allow Cinnamyl Alcohol Dehydrogenase-Deficient Nicotiana attenuata Plants to Compensate for their Structural Deficiencies

“…We transformed N. attenuata plants using RNAi technology with an inverted-repeat (ir) sequence of their endogenous CAD gene to silence two stem-expressed NaCADs, referred to as ir-CAD plants. The ecological importance of lignification in N. attenuata-Trichobaris mucorea (tobacco stem weevil) interaction in the field has been reported recently using these NaCADsilenced plants (Diezel et al, 2011). Here, we addressed the following questions by conducting a series of experiments with N. attenuata ir-CAD plants grown in both the GH and the plant's native habitat in Utah.…”