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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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Both Ms and Hv larvae regulated more genes related to primary and secondary metabolism when they fed on JA-silenced plants than when they fed on N/PI- or N-silenced plants.In Ms larvae, these genes were mainly down-regulated while in Hv larvae, they were both up- and down-regulated. A) Various functional categories of genes related to primary metabolism were highly regulated in Hv larvae, while only a few were regulated in Ms larvae; however, Ms larvae that fed on JA-silenced plants regulated 1.9-fold more genes than did Hv larvae that fed on the same plants. B) In Ms larvae, most genes related to secondary metabolism were down-regulated (with percentages down-regulated in larvae fed on JA-silenced plants being the highest followed by N/PI- and N-silenced plants), while in Hv larvae, these genes were both up- and down-regulated. Ms larvae that fed on JA-silenced plants regulated 4.4-fold more genes than did Hv larvae that fed on the same plants. Open bars: up-regulated (ER>1.5); black bars: down-regulated (ER<−1.5). Inset: Venn diagrams depicting the percentage of genes regulated by larvae in response to JA-, N/PI or N-silenced diets; Ms (upper panel) and Hv (lower panel) for primary (A) and secondary (B) metabolism.
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pone-0008735-g003: Both Ms and Hv larvae regulated more genes related to primary and secondary metabolism when they fed on JA-silenced plants than when they fed on N/PI- or N-silenced plants.In Ms larvae, these genes were mainly down-regulated while in Hv larvae, they were both up- and down-regulated. A) Various functional categories of genes related to primary metabolism were highly regulated in Hv larvae, while only a few were regulated in Ms larvae; however, Ms larvae that fed on JA-silenced plants regulated 1.9-fold more genes than did Hv larvae that fed on the same plants. B) In Ms larvae, most genes related to secondary metabolism were down-regulated (with percentages down-regulated in larvae fed on JA-silenced plants being the highest followed by N/PI- and N-silenced plants), while in Hv larvae, these genes were both up- and down-regulated. Ms larvae that fed on JA-silenced plants regulated 4.4-fold more genes than did Hv larvae that fed on the same plants. Open bars: up-regulated (ER>1.5); black bars: down-regulated (ER<−1.5). Inset: Venn diagrams depicting the percentage of genes regulated by larvae in response to JA-, N/PI or N-silenced diets; Ms (upper panel) and Hv (lower panel) for primary (A) and secondary (B) metabolism.

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)

Both Ms and Hv larvae regulated more genes related to primary and secondary metabolism when they fed on JA-silenced plants than when they fed on N/PI- or N-silenced plants.In Ms larvae, these genes were mainly down-regulated while in Hv larvae, they were both up- and down-regulated. A) Various functional categories of genes related to primary metabolism were highly regulated in Hv larvae, while only a few were regulated in Ms larvae; however, Ms larvae that fed on JA-silenced plants regulated 1.9-fold more genes than did Hv larvae that fed on the same plants. B) In Ms larvae, most genes related to secondary metabolism were down-regulated (with percentages down-regulated in larvae fed on JA-silenced plants being the highest followed by N/PI- and N-silenced plants), while in Hv larvae, these genes were both up- and down-regulated. Ms larvae that fed on JA-silenced plants regulated 4.4-fold more genes than did Hv larvae that fed on the same plants. Open bars: up-regulated (ER>1.5); black bars: down-regulated (ER<−1.5). Inset: Venn diagrams depicting the percentage of genes regulated by larvae in response to JA-, N/PI or N-silenced diets; Ms (upper panel) and Hv (lower panel) for primary (A) and secondary (B) metabolism.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2806910&req=5

pone-0008735-g003: Both Ms and Hv larvae regulated more genes related to primary and secondary metabolism when they fed on JA-silenced plants than when they fed on N/PI- or N-silenced plants.In Ms larvae, these genes were mainly down-regulated while in Hv larvae, they were both up- and down-regulated. A) Various functional categories of genes related to primary metabolism were highly regulated in Hv larvae, while only a few were regulated in Ms larvae; however, Ms larvae that fed on JA-silenced plants regulated 1.9-fold more genes than did Hv larvae that fed on the same plants. B) In Ms larvae, most genes related to secondary metabolism were down-regulated (with percentages down-regulated in larvae fed on JA-silenced plants being the highest followed by N/PI- and N-silenced plants), while in Hv larvae, these genes were both up- and down-regulated. Ms larvae that fed on JA-silenced plants regulated 4.4-fold more genes than did Hv larvae that fed on the same plants. Open bars: up-regulated (ER>1.5); black bars: down-regulated (ER<−1.5). Inset: Venn diagrams depicting the percentage of genes regulated by larvae in response to JA-, N/PI or N-silenced diets; Ms (upper panel) and Hv (lower panel) for primary (A) and secondary (B) metabolism.
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