Molecular Interactions between the Specialist HerbivoreManduca sexta (Lepidoptera, Sphingidae) and Its Natural Host Nicotiana attenuata. II. Accumulation of Plant mRNAs in Response to Insect-Derived Cues

Abstract

The transcriptional changes in Nicotiana attenuata Torr. ex Wats. elicited by attack from Manduca sexta larvae were previously characterized by mRNA differential display (D. Hermsmeier, U. Schittko, I.T. Baldwin [2001] Plant Physiol 125: 683-700). Because herbivore attack causes wounding, we disentangled wound-induced changes from those elicited by M. sexta oral secretions and regurgitant (R) with a northern analysis of a subset of the differentially expressed transcripts encoding threonine deaminase, pathogen-induced oxygenase, a photosystem II light-harvesting protein, a retrotransposon homolog, and three unknown genes. R extensively modified wound-induced responses by suppressing wound-induced transcripts (type I) or amplifying the wound-induced response (type II) further down-regulating wound-suppressed transcripts (type IIa) or up-regulating wound-induced transcripts (type IIb). It is interesting that although all seven genes displayed their R-specific patterns in the treated tissues largely independently of the leaf or plant developmental stage, only the type I genes displayed strong systemic induction. Ethylene was not responsible for any of the specific patterns of expression. R collected from different tobacco feeding insects, M. sexta, Manduca quinquemaculata, and Heliothis virescens, as well as from different instars of M. sexta were equally active. The active components of M. sexta R were heat stable and active in minute amounts, comparable with real transfer rates during larval feeding. Specific expression patterns may indicate that the plant is adjusting its wound response to efficiently fend off M. sexta, but may also be advantageous to the larvae, especially when R suppress wound-induced plant responses.

Molecular Interactions between the Specialist HerbivoreManduca sexta (Lepidoptera, Sphingidae) and Its Natural Host Nicotiana attenuata. I. Large-Scale Changes in the Accumulation of Growth- and Defense-Related Plant mRNAs

“…The analysis provided evidence for exclusively insectresponsive promotors (in pDH25.4 and pDH14.2). The response of these genes in addition to five additional insect-elicited transcripts are characterized more fully in a second companion paper (Schittko et al, 2001) and the active components responsible for the insect-specific elicitation are described in a third companion paper (Halitschke et al, 2001). Insectresponsive promoters will not only allow researchers to engineer insect-resistance, but also to analyze the contribution of individual transgenes to the Darwinian fitness of natural plant populations exposed to herbivory.…”

“…Among the genes presented in this work, TD showed the strongest and most specific response to insect attack: transcripts encoding TD strongly accumulated after herbivory and application of MeJA to leaves, weakly in response to low concentrations of airborne MeJA and wounding, and not at all after inoculation with TMV, A. tumefaciens, or exposure to ABA, ethylene, and MSA (pDH 14.2; Figs. 1 and 3; see also Schittko et al, 2001). Local induction of TD transcript accumulation after wounding or application of ABA or JA has been reported for potato and tomato, but data on systemic responses are contradictory (Hildmann et al, 1992;Pena-Cortez et al, 1993;Dammann et al, 1997).…”

Molecular Interactions between the Specialist HerbivoreManduca 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

“…In 1/20th of the insect-responsive transcriptome, 27 genes displayed altered expression patterns (Hermsmeier et al, 2001). A subset of seven genes was found to differentially respond to R as compared with mechanical damage.…”

“…A subset of seven genes was found to differentially respond to R as compared with mechanical damage. Larval R of M. sexta and Manduca quinquemaculata antagonistically (type I genes) or synergistically (type II genes) modified wound-induced transcriptional responses of these seven genes (Schittko et al, 2001). Given that chemical attributes of larval feeding mediate extensive changes in transcript accumulation and phenotypic responses, characterization of active components of R is of great interest.…”

Transcriptional Regulation of Sorghum Defense Determinants against a Phloem-Feeding Aphid

“…Insect chewing also accelerated accumulation of woundinduced transcripts in potato (Solanum tuberosum) leaves (Korth and Dixon, 1997). Furthermore, unique to insect feeding, plants are able to initiate indirect defense by synthesizing specific blends of volatiles that attract natural enemies of the herbivores (Alborn et al, 1997;Pare and Tumlinson, 1997;Schittko et al, 2001), and by forming neoplasmic tissues that impede larval entry into the plant tissue (Doss et al, 2000). Discrimination between mechanical wounding and insect herbivory is thought to be due to recognition of insect-derived elicitors by plant cells (Alborn et al, 1997;Korth and Dixon, 1997;Halitschke et al, 2001).…”