Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. IV. Insect-induced ethylene reduces jasmonate-induced nicotine accumulation by regulating putrescine N-methyltransferase transcripts

Attack by the specialist herbivore, Manduca sexta, on its native host Nicot iana attenuata Torr. ex Wats. produces a dramatic ethylene release, a jasmo nate burst, and a suppression of the nicotine accumulation that results fro m careful simulations of the herbivore's damage. Methyl-jasmonate (MeJA) tr eatment induces nicotine biosynthesis. However, this induction can be suppr essed by ethylene as pretreatment of plants with 1-methylcyclopropene (1-MC P), a competitive inhibitor of ethylene receptors, restores the full MeJA-i nduced nicotine response in herbivore attacked plants (J. Kahl, D.H. Siemen s, R.J. Aerts, R. Gabler, F. Kuhnemann, C.A. Preston, I.T. Baldwin [2000] P lanta 210: 336-342). To understand whether this herbivore-induced signal cr oss-talk occurs at the level of transcript accumulation, we cloned the putr escine methyltransferase genes (NaPMT1 and NaPMT2) of N. attenuata, which a re thought to represent the rate limiting step in nicotine biosynthesis, an d measured transcript accumulations by northern analysis after various jasm onate, 1-MCP, ethephon, and herbivory treatments. Transcripts of both root putrescine N-methyltransferase (PMT) genes and nicotine accumulation increa sed dramatically within 10 h of shoot MeJA treatment and immediately after root treatments. Root ethephon treatments suppressed this response, which c ould be reversed by 1-MCP pretreatment. Moreover, 1-MCP pretreatment dramat ically amplified the transcript accumulation resulting from both wounding a nd M. sexta herbivory. We conclude that attack from this nicotinetolerant s pecialist insect causes N. attenuata to produce ethylene, which directly su ppresses the nitrogen-intensive biosynthesis of nicotine.