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Plant Physiol, April 2001, Vol. 125, pp. 2189-2202
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
Transcripts1,2
Robert A.
Winz and
Ian T.
Baldwin*
Department of Molecular Ecology, Max Planck Institute for Chemical
Ecology, Carl Zeiss Promenade 10, D-07745 Jena, Germany
Attack by the specialist herbivore, Manduca sexta,
on its native host Nicotiana attenuata Torr. ex Wats.
produces a dramatic ethylene release, a jasmonate burst, and a
suppression of the nicotine accumulation that results from careful
simulations of the herbivore's damage. Methyl-jasmonate (MeJA)
treatment induces nicotine biosynthesis. However, this induction can be
suppressed by ethylene as pretreatment of plants with
1-methylcyclopropene (1-MCP), a competitive inhibitor of ethylene
receptors, restores the full MeJA-induced nicotine response in
herbivore attacked plants (J. Kahl, D.H. Siemens, R.J. Aerts, R. Gäbler, F. Kühnemann, C.A. Preston, I.T. Baldwin [2000]
Planta 210: 336-342). To understand whether this herbivore-induced
signal cross-talk occurs at the level of transcript accumulation, we
cloned the putrescine methyltransferase genes (NaPMT1 and NaPMT2) of
N. attenuata, which are thought to represent the rate
limiting step in nicotine biosynthesis, and measured transcript
accumulations by northern analysis after various jasmonate, 1-MCP,
ethephon, and herbivory treatments. Transcripts of both root putrescine
N-methyltransferase (PMT) genes and nicotine accumulation increased dramatically within 10 h of shoot MeJA treatment and immediately after root treatments. Root ethephon treatments suppressed this response, which could be reversed by 1-MCP
pretreatment. Moreover, 1-MCP pretreatment dramatically amplified the
transcript accumulation resulting from both wounding and M.
sexta herbivory. We conclude that attack from this
nicotine-tolerant specialist insect causes N. attenuata
to produce ethylene, which directly suppresses the nitrogen-intensive
biosynthesis of nicotine.
1
This work was supported by the Max Planck Gesellschaft.
2
Part III in the series is: Halitschke R, Schittko U,
Pohnert G, Boland W, Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera,
Sphingidae) and its natural host Nicotiana attenuata:
III. Fatty acid-amino acid conjugates in herbivore oral secretions are
necessary and sufficient for herbivore-specific plant responses. Plant
Physiol 125: 711-717.
*
Corresponding author; e-mail baldwin{at}ice.mpg.de; fax
49-0-3641-643653.
© 2001 American Society of Plant Physiologists
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