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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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The number of genes regulated by both Ms and Hv larvae correlated with the number of defense traits that had been silenced in the larval host plants, but more genes were regulated in Hv than in Ms larvae.A) Venn diagrams depicting the number and percentage of genes significantly up- (ER>1.5) or down-regulated (ER<−1.5) by Ms and Hv larvae according to which defense compound was silenced in the plants they fed on. When the generalist Hv larvae fed on JA-, N/PI-, or N-silenced N. attenuata plants 17-, 33- and 38-fold more genes were regulated compared to when the specialist, Ms larvae fed on the same plants. Values in parentheses denote the percentage of regulated genes. For both species, the number of genes and the percentage of regulated genes correlated with the number of different direct defenses that had been silenced in the plants: more genes were found to be regulated in larvae that fed on JA-silenced plants than in larvae that fed on N/PI- and N-silenced plants. B) In Ms larvae, the percentage of genes coding for enzymes, transporters and metabolism was highly regulated; in Hv larvae, the percentage of genes coding for genetic information followed by cellular processes and environmental information processing was highly regulated.
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pone-0008735-g002: The number of genes regulated by both Ms and Hv larvae correlated with the number of defense traits that had been silenced in the larval host plants, but more genes were regulated in Hv than in Ms larvae.A) Venn diagrams depicting the number and percentage of genes significantly up- (ER>1.5) or down-regulated (ER<−1.5) by Ms and Hv larvae according to which defense compound was silenced in the plants they fed on. When the generalist Hv larvae fed on JA-, N/PI-, or N-silenced N. attenuata plants 17-, 33- and 38-fold more genes were regulated compared to when the specialist, Ms larvae fed on the same plants. Values in parentheses denote the percentage of regulated genes. For both species, the number of genes and the percentage of regulated genes correlated with the number of different direct defenses that had been silenced in the plants: more genes were found to be regulated in larvae that fed on JA-silenced plants than in larvae that fed on N/PI- and N-silenced plants. B) In Ms larvae, the percentage of genes coding for enzymes, transporters and metabolism was highly regulated; in Hv larvae, the percentage of genes coding for genetic information followed by cellular processes and environmental information processing was highly regulated.

Mentions: While Hv larvae regulated more transcripts than did Ms larvae, the overall pattern of regulation in both species tracked the number of defenses that were silenced in the host: the greater the number of defenses silenced in the host plant (JA>N/PI>N), the greater the number of transcripts that were differentially regulated in larvae feeding on these silenced host plants in comparison to larvae that fed on wild-type (WT) plants (Figure 2A). Moreover, the type of regulation differed between the two species: Ms larvae down-regulated 2–5 times more transcripts than they up-regulated, but in Hv larvae, an equal number of genes were up- and down-regulated. Hence, Ms larvae that fed on N-silenced plants regulated 24 transcripts of which 8 were up-regulated and 16 were down-regulated; when they fed on N/PI-silenced plants, they regulated 30 transcripts of which 5 were up-regulated and 25 were down-regulated; and on JA-silenced plants, they regulated 73 transcripts of which 22 were up-regulated and 51 were down-regulated. Hv larvae that fed on N-, N/PI- and JA-silenced plants regulated 914 transcripts (493 up-regulated and 421 down-regulated), 1006 transcripts (567 up-regulated and 439 down-regulated) and 1228 transcripts (716 up-regulated and 512 down-regulated), respectively (Figure 2A).


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)

The number of genes regulated by both Ms and Hv larvae correlated with the number of defense traits that had been silenced in the larval host plants, but more genes were regulated in Hv than in Ms larvae.A) Venn diagrams depicting the number and percentage of genes significantly up- (ER>1.5) or down-regulated (ER<−1.5) by Ms and Hv larvae according to which defense compound was silenced in the plants they fed on. When the generalist Hv larvae fed on JA-, N/PI-, or N-silenced N. attenuata plants 17-, 33- and 38-fold more genes were regulated compared to when the specialist, Ms larvae fed on the same plants. Values in parentheses denote the percentage of regulated genes. For both species, the number of genes and the percentage of regulated genes correlated with the number of different direct defenses that had been silenced in the plants: more genes were found to be regulated in larvae that fed on JA-silenced plants than in larvae that fed on N/PI- and N-silenced plants. B) In Ms larvae, the percentage of genes coding for enzymes, transporters and metabolism was highly regulated; in Hv larvae, the percentage of genes coding for genetic information followed by cellular processes and environmental information processing was highly regulated.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2806910&req=5

pone-0008735-g002: The number of genes regulated by both Ms and Hv larvae correlated with the number of defense traits that had been silenced in the larval host plants, but more genes were regulated in Hv than in Ms larvae.A) Venn diagrams depicting the number and percentage of genes significantly up- (ER>1.5) or down-regulated (ER<−1.5) by Ms and Hv larvae according to which defense compound was silenced in the plants they fed on. When the generalist Hv larvae fed on JA-, N/PI-, or N-silenced N. attenuata plants 17-, 33- and 38-fold more genes were regulated compared to when the specialist, Ms larvae fed on the same plants. Values in parentheses denote the percentage of regulated genes. For both species, the number of genes and the percentage of regulated genes correlated with the number of different direct defenses that had been silenced in the plants: more genes were found to be regulated in larvae that fed on JA-silenced plants than in larvae that fed on N/PI- and N-silenced plants. B) In Ms larvae, the percentage of genes coding for enzymes, transporters and metabolism was highly regulated; in Hv larvae, the percentage of genes coding for genetic information followed by cellular processes and environmental information processing was highly regulated.
Mentions: While Hv larvae regulated more transcripts than did Ms larvae, the overall pattern of regulation in both species tracked the number of defenses that were silenced in the host: the greater the number of defenses silenced in the host plant (JA>N/PI>N), the greater the number of transcripts that were differentially regulated in larvae feeding on these silenced host plants in comparison to larvae that fed on wild-type (WT) plants (Figure 2A). Moreover, the type of regulation differed between the two species: Ms larvae down-regulated 2–5 times more transcripts than they up-regulated, but in Hv larvae, an equal number of genes were up- and down-regulated. Hence, Ms larvae that fed on N-silenced plants regulated 24 transcripts of which 8 were up-regulated and 16 were down-regulated; when they fed on N/PI-silenced plants, they regulated 30 transcripts of which 5 were up-regulated and 25 were down-regulated; and on JA-silenced plants, they regulated 73 transcripts of which 22 were up-regulated and 51 were down-regulated. Hv larvae that fed on N-, N/PI- and JA-silenced plants regulated 914 transcripts (493 up-regulated and 421 down-regulated), 1006 transcripts (567 up-regulated and 439 down-regulated) and 1228 transcripts (716 up-regulated and 512 down-regulated), respectively (Figure 2A).

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