Plasticity in allocation of nicotine to reproductive parts inNicotiana attenuata

Abstract

Although little is known about the patterns of chemical defense allocation in reproductive tissues, optimal defense theory predicts a high constitutive allocation due to the tissues' high fitness value. To examine this prediction, we quantified the short- and long-term changes in the nicotine pools of reproductive tissues in response to both floral and leaf damage. Recently opened flowers (stage 5 capsules) do not alter their nicotine pools within a day in response to herbivory byManduca sexta larvae or mechanical damage to the corolla. Similarly, leaf damage during both vegetative and reproductive growth does not influence the nicotine pools of the first three stage-5 capsules produced. However, the nicotine pools of capsules produced later in reproductive growth were significantly larger (1.2- to 1.9-fold) on plants with leaf damage. These differences in floral nicotine pools were a result of both increases in nicotine pools of capsules on damaged plants and decreases in the nicotine pools of capsules on undamaged plants during reproductive growth. Leaf damage did not affect the rate of capsule maturation or the mass of stage-5 capsules at any time during reproductive growth. An allometric analysis of nicotine pools and biomass of reproductive parts in all stages of development from damaged and undamaged plants demonstrates that damaged plants allocated a significantly larger quantity of nicotine to reproductive parts in all stages of development than did undamaged plants. Given that nicotine is thought to be synthesized in the roots and transported to leaves and reproductive parts, nicotine could be allocated to reproductive parts in proportion to the number of developing capsules on a plant. We excised the first 27 stage-5 capsules on plants with and without leaf damage, with the expectation that plants with fewer capsules would allocate a larger amount of nicotine to the remaining capsules. In contrast to the prediction of this passive allocation model, floral excision did not affect nicotine pools on plants with or without leaf damage. These results demonstrate that the allocation of nicotine to reproductive parts is more strongly influenced by damage to vegetative rather than reproductive tissues. Reproductive parts are constitutively defended over the short term, but the set points for defense allocation are apparently increased by damage to vegetative tissues during reproductive growth. The decrease in allocation of nicotine to reproductive parts in undamaged plants during reproductive growth suggests an optimization of resource allocation as plants realize their potential fitness.

Tobacco nicotine uptake permease (NUP1) affects alkaloid metabolism

“…Thus, NUP1 seems to be at a physiological nexus between root nicotine metabolism and root growth. In this light, the establishment and/or monitoring of apoplastic root nicotine levels by NUP1-mediated nicotine uptake might be important for maintaining well-documented-but poorly understood-whole-plant nicotine allometric set points (20,21).…”

“…Nicotine is not appreciably degraded in planta (19), and whole-plant nicotine levels are held at MeJA-responsive allometric set points (20,21). Nicotine exhibits differential shoot accumulations over the course of plant development and seems to be mobilized by source-sink movement in the phloem (22,23).…”

Jasmonate-induced responses are costly but benefit plants under attack in native populations

“…Nicotiana attenuata, like its congener N. sylvestris, synthesizes the toxic alkaloid nicotine in its roots and dramatically increases its rate of nicotine synthesis after leaf wounding or herbivory, which in turn, results in a systemic increase in nicotine concentrations in above-ground vegetative and reproductive tissues (12)(13)(14)(15). In laboratory feeding trials, induced levels of nicotine protect plants against nicotinetolerant herbivores (16), but these herbivores may suffer lower rates of parasitism when feeding on plants with high nicotine concentrations (17), indicating that this induced defense may have both ecological benefits and costs.…”

Within‐plant relationships among wounding, jasmonic acid, and nicotine implications for defence in Nicotiana sylvestris

“…Although a defence response might be a local (Jongsma et al, 1994;Zangerl & Berenbaum, 1995) or systemic (Baldwin, 1989;Farmer & Ryan, 1992;Pena-Cortes, Fisahn & Willmitzer, 1995) phenomenon, the individual underlying components of the signal-transduction pathway might operate independently of that level, ln order to disentangle local and systemic responses, we damage a single tobacco leaf and quantify JA in the damaged leaf, as well as in single leaves phylotactically one position above and one position below the damaged leaf; we also quantify JA m leaves at those positions on undamaged plants. We find that damage to a single leaf does not significantly alter the amount of J A in phylotactically adjacent leaves.…”

“…The within-plant distribution, fitness cost, then these metabolites should be distri-as well as the inducibility, of a number of secondary buted within a plant so as to optimize the plant's metabolites, including nicotine (Baldwin, 1989; Darwinian fitness. Optimal defence (OD) theory Baldwin & Karb, 1995), furanocoumarins (Zangeri (McKey, 1974, 1979Rhoades, 1979) formalizes & Bazzaz, 1992;Zangeri & Rutledge, 1996), pyrrolithese arguments and predicts that tissues with high zidine alkaloids (van Dam, Verpoorte & van der Meijden, 1994;van Dame/a/., 1995),andproteinase inhibitors (Wolfson, 1991) are consistent with this * To whom correspondence should be addressed.…”