Herbivore-induced ethylene suppresses a direct defense but not a putative indirect defense against an adapted herbivore

Herbivory induces both direct and indirect defenses in plants: however, som e combinations of these defenses may not be compatible. The jasmonate signa l cascade activated both direct (nicotine accumulations) and indirect (mono - and sesquiterpene emissions) whole-plant defense responses in the native tobacco Nicotiana attenuata Torr. Ex Wats. Nicotine accumulations were prop ortional to the amount of leaf wounding and the resulting increases in jasm onic acid (JA) concentrations. However. when larvae of the nicotine-toleran t herbivore. Manduca sexta, fed on plants or their oral secretions were app lied to leaf punctures, the normal wound response was dramatically altered, as evidenced by large (4- to 10-fold) increases in the release of (i) vola tile terpenoids and (ii) ethylene, (iii) increased (4- to 30-fold) accumula tions of endogenous JA pools, but (iv) decreased or unchanged nicotine accu mulations. The ethylene release, which was insensitive to inhibitors of ind uced JA accumulation, was sufficient to account for the attenuated nicotine response. Applications of ethylene and ethephon suppressed the induced nic otine response and pre-treatment of plants with a competitive inhibitor of ethylene receptors, 1-methylcyclopropene. restored the full nicotine respon se. This ethylene burst, however, did not inhibit the release of volatile t erpenoids. Because parasitoids of Manduca larvae are sensitive to the dieta ry intake of nicotine by their hosts, this ethylene-mediated switching from direct to a putative indirect defense may represent an adaptive tailoring of a plant's defense response.