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Unbiased transcriptional comparisons of generalist and specialist herbivores feeding on progressively defenseless Nicotiana attenuata plants.

Govind G, Mittapalli O, Griebel T, Allmann S, Böcker S, Baldwin IT - PLoS ONE (2010)

Bottom Line: The 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.

View Article: PubMed Central - PubMed

Affiliation: Max Planck Institute for Chemical Ecology, Jena, Germany.

ABSTRACT

Background: Herbivore 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 findings: We 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/significance: The 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.

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In Ms larvae, a higher percentage of peptidases and hydrolases were down-regulated when they fed on plants silenced in JA compared to when they fed on plants silenced in N/PI, and this percentage of down-regulated enzymes was lowest in plants silenced in N; the regulation of these enzyme categories by Hv larvae did not follow a pattern organized by defense expression in the host plant.The percentage of genes regulated for A) peptidases was 2.4-fold greater and the B) hydrolases, 5.6-fold greater in Ms larvae that fed on plants silenced for JA compared to in Hv larvae that fed on the same plants. C) Oxidoreductases, transferases and isomerases (the category referred to as ‘other enzyme’) were regulated only in Hv larvae when these fed on JA-, N/PI- or N-silenced plants. Open bars: up-regulated (ER>1.5); solid bars: down-regulated (ER<−1.5). Inset: Venn diagrams depicting the percentage of genes regulated by Ms larvae (upper panel) and Hv larvae (lower panel) for peptidases (A), hydrolases (B) and other enzymes (C) in response to feeding on variously defenseless plants.
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pone-0008735-g004: In Ms larvae, a higher percentage of peptidases and hydrolases were down-regulated when they fed on plants silenced in JA compared to when they fed on plants silenced in N/PI, and this percentage of down-regulated enzymes was lowest in plants silenced in N; the regulation of these enzyme categories by Hv larvae did not follow a pattern organized by defense expression in the host plant.The percentage of genes regulated for A) peptidases was 2.4-fold greater and the B) hydrolases, 5.6-fold greater in Ms larvae that fed on plants silenced for JA compared to in Hv larvae that fed on the same plants. C) Oxidoreductases, transferases and isomerases (the category referred to as ‘other enzyme’) were regulated only in Hv larvae when these fed on JA-, N/PI- or N-silenced plants. Open bars: up-regulated (ER>1.5); solid bars: down-regulated (ER<−1.5). Inset: Venn diagrams depicting the percentage of genes regulated by Ms larvae (upper panel) and Hv larvae (lower panel) for peptidases (A), hydrolases (B) and other enzymes (C) in response to feeding on variously defenseless plants.

Mentions: In the following sections, we discuss the differences in the regulation of transcripts in the functional categories of primary and secondary metabolism, peptidase and hydrolases, transporters, and genetic information processing observed in Ms and Hv larvae that fed on defenseless plants. Two general patterns of regulation were observed. First, while Ms larvae down-regulated, Hv larvae up- and down-regulated transcripts from the same functional categories. Second, while Ms larvae regulated transcripts in a diet-specific manner, Hv larvae regulated a more similar suite of transcripts across all diet types (Figures 3, 4, 5, 6, upper and lower panels; Tables S1 and S2).


Unbiased transcriptional comparisons of generalist and specialist herbivores feeding on progressively defenseless Nicotiana attenuata plants.

Govind G, Mittapalli O, Griebel T, Allmann S, Böcker S, Baldwin IT - PLoS ONE (2010)

In Ms larvae, a higher percentage of peptidases and hydrolases were down-regulated when they fed on plants silenced in JA compared to when they fed on plants silenced in N/PI, and this percentage of down-regulated enzymes was lowest in plants silenced in N; the regulation of these enzyme categories by Hv larvae did not follow a pattern organized by defense expression in the host plant.The percentage of genes regulated for A) peptidases was 2.4-fold greater and the B) hydrolases, 5.6-fold greater in Ms larvae that fed on plants silenced for JA compared to in Hv larvae that fed on the same plants. C) Oxidoreductases, transferases and isomerases (the category referred to as ‘other enzyme’) were regulated only in Hv larvae when these fed on JA-, N/PI- or N-silenced plants. Open bars: up-regulated (ER>1.5); solid bars: down-regulated (ER<−1.5). Inset: Venn diagrams depicting the percentage of genes regulated by Ms larvae (upper panel) and Hv larvae (lower panel) for peptidases (A), hydrolases (B) and other enzymes (C) in response to feeding on variously defenseless plants.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2806910&req=5

pone-0008735-g004: In Ms larvae, a higher percentage of peptidases and hydrolases were down-regulated when they fed on plants silenced in JA compared to when they fed on plants silenced in N/PI, and this percentage of down-regulated enzymes was lowest in plants silenced in N; the regulation of these enzyme categories by Hv larvae did not follow a pattern organized by defense expression in the host plant.The percentage of genes regulated for A) peptidases was 2.4-fold greater and the B) hydrolases, 5.6-fold greater in Ms larvae that fed on plants silenced for JA compared to in Hv larvae that fed on the same plants. C) Oxidoreductases, transferases and isomerases (the category referred to as ‘other enzyme’) were regulated only in Hv larvae when these fed on JA-, N/PI- or N-silenced plants. Open bars: up-regulated (ER>1.5); solid bars: down-regulated (ER<−1.5). Inset: Venn diagrams depicting the percentage of genes regulated by Ms larvae (upper panel) and Hv larvae (lower panel) for peptidases (A), hydrolases (B) and other enzymes (C) in response to feeding on variously defenseless plants.
Mentions: In the following sections, we discuss the differences in the regulation of transcripts in the functional categories of primary and secondary metabolism, peptidase and hydrolases, transporters, and genetic information processing observed in Ms and Hv larvae that fed on defenseless plants. Two general patterns of regulation were observed. First, while Ms larvae down-regulated, Hv larvae up- and down-regulated transcripts from the same functional categories. Second, while Ms larvae regulated transcripts in a diet-specific manner, Hv larvae regulated a more similar suite of transcripts across all diet types (Figures 3, 4, 5, 6, upper and lower panels; Tables S1 and S2).

Bottom Line: The 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.

View Article: PubMed Central - PubMed

Affiliation: Max Planck Institute for Chemical Ecology, Jena, Germany.

ABSTRACT

Background: Herbivore 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 findings: We 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/significance: The 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.

Show MeSH
Related in: MedlinePlus