Nicotine's Defensive Function in Nature

Abstract

Plants produce metabolites that directly decrease herbivore performance, and as a consequence, herbivores are selected for resistance to these metabolites. To determine whether these metabolites actually function as defenses requires measuring the performance of plants that are altered only in the production of a certain metabolite. To date, the defensive value of most plant resistance traits has not been demonstrated in nature. We transformed native tobacco(Nicotiana attenuata) with a consensus fragment of its two putrescine N-methyl transferase (pmt) genes in either antisense or inverted-repeat (IRpmt) orientations. Only the latter reduced (by greater than 95%) constitutive and inducible nicotine. With D4-nicotinic acid (NA), we demonstrate that silencing pmt inhibits nicotine production, while the excess NA dimerizes to form anatabine. Larvae of the nicotine-adapted herbivore Manduca sexta (tobacco hornworm) grew faster and, like the beetle Diabrotica undecimpunctata, preferred IRpmt plants in choice tests. When planted in their native habitat, IRpmt plants were attacked more frequently and, compared to wild-type plants, lost 3-fold more leaf area from a variety of native herbivores, of which the beet armyworm, Spodoptera exigua, and Trimerotropis spp. grasshoppers caused the most damage. These results provide strong evidence that nicotine functions as an efficient defense in nature and highlights the value of transgenic techniques for ecological research.

Natural history-driven, plant-mediated RNAi-based study reveals CYP6B46 ’s role in a nicotine-mediated antipredator herbivore defense

“…AF280402] N. attenuata plants (A-03-108-3), fully characterized in ref. 23, were used as a nicotine-free hostplant to feed M. sexta larvae. Previously characterized N. attenuata transgenic line irCYP (A-09-30-2) was used to silence M. sexta's CYP6B46 (MsCYP6B46 NCBI accession no.…”

A Comparison of Two Nicotiana attenuata Accessions Reveals Large Differences in Signaling Induced by Oral Secretions of the Specialist Herbivore Manduca sexta

“…In N. attenuata, these herbivore-induced defenses include nicotine and TPI (Steppuhn et al, 2004;Zavala et al, 2004b). Because AZ plants have lost their TPI defense mechanism (Wu et al, 2007b), we analyzed the levels of nicotine as well as two phenolic compounds, chlorogenic acid and rutin, which are putative antiherbivore defenses (Isman and Duffey, 1982;Bi et al, 1997) and may constitute part of N. attenuata's direct defense.…”

“…We found that AZ produces greater amounts of both nicotine and phenolic compounds (chlorogenic acid and rutin) than does UT. Nicotine is a potent chemical defense that has a strong negative effect on M. sexta and on many other herbivores and has been previously shown to be a critical component of JA-mediated direct defense in AZ as well as in UT (Steppuhn et al, 2004). Nicotine biosynthesis is both up-regulated by JA and down-regulated by OS-induced ET (Baldwin, 1998;Voelckel et al, 2001;von Dahl et al, 2007).…”

Multidrug and Toxic Compound Extrusion-Type Transporters Implicated in Vacuolar Sequestration of Nicotine in Tobacco Roots

“…Alkaloids are a chemically diverse group of lowmolecular weight, nitrogen-containing secondary metabolites with characteristic toxicity and pharmacological activity and may function in the chemical defense of plants against herbivores and pathogens (Facchini, 2001;Steppuhn et al, 2004). Natural hydrophilic products, including alkaloids, are usually stored in the vacuole, which appears to be especially adapted to the bulk storage of chemicals for defensive functions.…”