Journal of Chemical Ecology

, Volume 26, Issue 4, pp 915–952

Jasmonate-Induced Responses of Nicotiana sylvestris Results in Fitness Costs Due to Impaired Competitive Ability for Nitrogen

  • Ian T. Baldwin
  • William HamiltonIII
Article
  • 164 Downloads

Abstract

We present the first evidence for a fitness cost of an inducible response that is detectable in a nitrogen (N) currency. Nicotine is an induced defense in Nicotiana sylvestris that can utilize 5–8% of the plant's total N, an investment that apparently cannot be recouped by metabolism. Induced nicotine production is endogenously regulated by jasmonic acid (JA), and we treated leaves with the methyl ester of this wound hormone (MeJA) in quantities (0, 25, 250 μg) known to elicit changes in endogenous JA and subsequent nicotine responses comparable to those elicited by mechanical wounding and herbivory in this species. We grew plants in competition chambers (CCs) in which three same-sized plants could compete for a communal but fixed pool of 15NO3 to quantify the outcome of competition for this fitness-limiting resource that is used both in defense and seed production. Competition profoundly increased all measures of growth and reproductive performance measured per milligram of N acquired. While plants acquired all the N supplied to them in the hydroponic solution, plants grown in CCs (as compared those grown in individual chambers—ICs) retained more of this N and produced more biomass, had larger nicotine contents, allocated less of their N to nicotine, produced larger floral stalks with more flowers, aborted fewer flowers, matured more capsules, and produced a greater mass of seed. Plants grown in ICs produced heavier seed, but this difference did not translate into a difference in seed viability.

MeJA treatment increased nicotine concentrations in proportion to the amount applied and significantly reduced growth (13–23%) and reproductive (31–44%) performance for plants grown with uninduced competitors, reflecting a large opportunity cost of induction. The effects of MeJA treatment on growth and reproduction were significantly less pronounced for plants grown in ICs. MeJA treatment significantly reduced the ability of plants to compete for [15N]KNO3 (reducing uptake by 9.5% and 23.7% for 25- and 250-μg MeJA-treated plants, respectively); no reductions in N acquisition were found in IC grown plants treated with MeJA. This impairment of competitive ability could account for 41–47% of the jasmonate-induced reductions in biomass by the day 15 harvest and 12–20% of the reductions in seed set and, in addition, created by "opportunity benefit" for neighboring uninduced plants, which grew larger, aborted fewer flowers, and matured more seed (a 28% increase) than did uninduced plants competing with similarly uninduced plants.

Competition dramatically increased plant growth and reproductive performance, and MeJA treatment of these high-performing plants significantly reduced their competitive ability, which translated into opportunity costs for induced plants and opportunity benefits for neighboring uninduced plants. Induced plants minimized these fitness costs by reducing their use of recently acquired N for nicotine biosynthesis when growing with competitors. MeJA treatments also altered stalk length, flower production, flower abortion, and allocation to seed mass. In spite of all this plasticity, induced responses incur large fitness costs, costs that could be in part attributed to reductions in competitive ability for N. We conclude that inducibility functions to minimize these costs.

Nicotiana sylvestris nitrogen nicotine allocation growth reproduction induced defenses costs of defense 

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Copyright information

© Plenum Publishing Corporation 2000

Authors and Affiliations

  • Ian T. Baldwin
    • 1
    • 2
  • William HamiltonIII
    • 2
  1. 1.Max-Planck-Institut für Chemische ÖkologieJenaGermany
  2. 2.Department of Biological Sciences, SUNYUniversity of BuffaloBuffalo

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