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Different transcript patterns in response to specialist and generalist herbivores in the wild Arabidopsis relative Boechera divaricarpa.

ABSTRACT: BACKGROUND: Plants defend themselves against herbivorous insects, utilizing both constitutive and inducible defenses. Induced defenses are controlled by several phytohormone-mediated signaling pathways. Here, we analyze transcriptional changes in the North American Arabidopsis relative Boechera divaricarpa in response to larval herbivory by the crucifer specialist lepidopteran Plutella xylostella (diamondback moth) and by the generalist lepidopteran Trichoplusia ni (cabbage semilooper), and compare them to wounding and exogenous phytohormone application. METHODOLOGY/PRINCIPAL FINDINGS: We use a custom macroarray constructed from B. divaricarpa herbivory-regulated cDNAs identified by suppression subtractive hybridization and from known stress-responsive A. thaliana genes for transcript profiling after insect herbivory, wounding and in response to jasmonate, salicylate and ethylene. In addition, we introduce path analysis as a novel approach to analyze transcript profiles. Path analyses reveal that transcriptional responses to the crucifer specialist P. xylostella are primarily determined by direct effects of the ethylene and salicylate pathways, whereas responses to the generalist T. ni are influenced by the ethylene and jasmonate pathways. Wound-induced transcriptional changes are influenced by all three pathways, with jasmonate having the strongest effect. CONCLUSIONS/SIGNIFICANCE: Our results show that insect herbivory is distinct from simple mechanical plant damage, and that different lepidopteran herbivores elicit different transcriptional responses.

SUBMITTER: Vogel H

PROVIDER: S-EPMC2031921 | biostudies-literature | 2007

REPOSITORIES: biostudies-literature

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Different transcript patterns in response to specialist and generalist herbivores in the wild Arabidopsis relative Boechera divaricarpa.

Vogel Heiko H Kroymann Juergen J Mitchell-Olds Thomas T

PloS one 20071024 10

<h4>Background</h4>Plants defend themselves against herbivorous insects, utilizing both constitutive and inducible defenses. Induced defenses are controlled by several phytohormone-mediated signaling pathways. Here, we analyze transcriptional changes in the North American Arabidopsis relative Boechera divaricarpa in response to larval herbivory by the crucifer specialist lepidopteran Plutella xylostella (diamondback moth) and by the generalist lepidopteran Trichoplusia ni (cabbage semilooper), a ...[more]

PMID: 17957263

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Project description:Through artificial selection, domesticated plants often contain modified levels of primary and secondary metabolites compared to their wild progenitors. It is hypothesized that the changed chemistry of cultivated plants will affect the performance of insects associated with these plants. In this paper, the development of several specialist and generalist herbivores and their endoparasitoids were compared when reared on a wild and cultivated population of cabbage, Brassica oleracea, and a recently established feral Brassica species. Irrespective of insect species or the degree of dietary specialization, herbivores and parasitoids developed most poorly on the wild population. For the specialists, plant population influenced only development time and adult body mass, whereas for the generalists, plant populations also affected egg-to-adult survival. Two parasitoid species, a generalist (Diadegma fenestrale) and a specialist (D. semiclausum), were reared from the same host (Plutella xylostella). Performance of D. semiclausum was closely linked to that of its host, whereas the correlation between survival of D. fenestrale and host performance was less clear. Plants in the Brassicaceae characteristically produce defense-related glucosinolates (GS). Levels of GS in leaves of undamaged plants were significantly higher in plants from the wild population than from the domesticated populations. Moreover, total GS concentrations increased significantly in wild plants after herbivory, but not in domesticated or feral plants. The results of this study reveal that a cabbage cultivar and plants from a wild cabbage population exhibit significant differences in quality in terms of their effects on the growth and development of insect herbivores and their natural enemies. Although cultivated plants have proved to be model systems in agroecology, we argue that some caution should be applied to evolutionary explanations derived from studies on domesticated plants, unless some knowledge exists on the history of the system under investigation.

Project description:BackgroundHerbivore feeding elicits dramatic increases in defenses, most of which require jasmonate (JA) signaling, and against which specialist herbivores are thought to be better adapted than generalist herbivores. Unbiased transcriptional analyses of how neonate larvae cope with these induced plant defenses are lacking.Methodology/principal findingsWe created cDNA microarrays for Manduca sexta and Heliothis virescens separately, by spotting normalized midgut-specific cDNA libraries created from larvae that fed for 24 hours on MeJA-elicited wild-type (WT) Nicotiana attenuata plants. These microarrays were hybridized with labeled probes from neonates that fed for 24 hours on WT and isogenic plants progressively silenced in JA-mediated defenses (N: nicotine; N/PI: N and trypsin protease inhibitors; JA: all JA-mediated defenses). H. virescens neonates regulated 16 times more genes than did M. sexta neonates when they fed on plants silenced in JA-mediated defenses, and for both species, the greater the number of defenses silenced in the host plant (JA > N/PI > N), the greater were the number of transcripts regulated in the larvae. M. sexta larvae tended to down-regulate while H. virescens larvae up- and down-regulated transcripts from the same functional categories of genes. M. sexta larvae regulated transcripts in a diet-specific manner, while H. virescens larvae regulated a similar suite of transcripts across all diet types.Conclusions/significanceThe observations are consistent with the expectation that specialists are better adapted than generalist herbivores to the defense responses elicited in their host plants by their feeding. While M. sexta larvae appear to be better adapted to N. attenuata's defenses, some of the elicited responses remain effective defenses against both herbivore species. The regulated genes provide novel insights into larval adaptations to N. attenuata's induced defenses, and represent potential targets for plant-mediated RNAi to falsify hypotheses about the process of adaptation.

Dataset Information

Different transcript patterns in response to specialist and generalist herbivores in the wild Arabidopsis relative Boechera divaricarpa.

Publications

Different transcript patterns in response to specialist and generalist herbivores in the wild Arabidopsis relative Boechera divaricarpa.

Similar Datasets

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