Jasmonate-induced responses of Nicotiana sylvestris results in fitness costs due to impaired competitive ability for nitrogen

We present the first evidence for a fitness cost of an inducible response t hat is detectable in a nitrogen (N) currency. Nicotine is an induced defens e in Nicotiana sylvestris that can utilize 5-8% of the plant's total N, an investment that apparently cannot be recouped by metabolism Induced nicotin e production is endogenously regulated by jasmonic acid (JA), and we treate d leaves with the methyl ester of this wound hormone (MeJA) in quantities ( 0, 25, 250 mu g) known to elicit changes in endogenous JA and subsequent ni cotine responses comparable to those elicited by mechanical wounding and he rbivory in this species. We grew plants in competition chambers (CCs) in wh ich three same-sized plants could compete for a communal but fixed pool of (NO3)-N-15 to quantify the outcome of competition for this fitness-limiting resource that is used both in defense and seed production. Competition pro foundly increased all measures of growth and reproductive performance measu red per milligram of N acquired. While plants acquired all the N supplied t o them in the hydroponic solution, plants grown in CCs (as compared those g rown in individual chambers-ICs) retained more of this N and produced more biomass, had larger nicotine contents, allocated less of their N to nicotin e, 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 di fference in seed viability. MeJA treatment increased nicotine concentrations in proportion to the amoun t applied and significantly reduced growth (13-23%) and reproductive (31-44 %) performance for plants grown with uninduced competitors, reflecting a la rge 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 [N-15]KNO3 (reducing uptake by 9.5% and 23.7% for 25- and 250-mu g MeJA-tr eated plants, respectively); no reductions in N acquisition were found in I C grown plants treated with MeJA. This impairment of competitive ability co uld account for 41-47% of the jasmonate-induced reductions in biomass by th e day 15 harvest and 12-20% of the reductions in seed set and, in addition, created by "opportunity benefit" for neighboring uninduced plants, which g rew larger, aborted fewer flowers, and matured more seed (a 28% increase) t han did uninduced plants competing with similarly uninduced plants. Competition dramatically increased plant growth and reproductive performanc e, and MeJA treatment of these high-performing plants significantly reduced their competitive ability, which translated into opportunity costs for ind uced plants and opportunity benefits for neighboring uninduced plants. indu ced plants minimized these fitness costs by reducing their use of recently acquired N for nicotine biosynthesis when growing with competitors. MeJA tr eatments also altered stalk length, flower production, flower abortion, and allocation to seed mass. In spite of all this plasticity, induced response s incur large fitness costs, costs that could be in part attributed to redu ctions in competitive ability for N. We conclude that inducibility function s to minimize these costs.