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Integrated transcriptomics and metabolomics decipher differences in the resistance of pedunculate oak to the herbivore Tortrix viridana L.

Kersten B, Ghirardo A, Schnitzler JP, Kanawati B, Schmitt-Kopplin P, Fladung M, Schroeder H - BMC Genomics (2013)

Bottom Line: Next generation RNA sequencing revealed hundreds of genes that exhibited constitutive and/or inducible differential expression in the resistant oak compared to the susceptible oak.We conclude that the resistant oak type seem to prefer a strategy of constitutive defence responses in contrast to more induced defence responses of the susceptible oaks triggered by feeding.These results pave the way for the development of biomarkers for an early determination of potentially green oak leaf roller-resistant genotypes in natural pedunculate oak populations in Europe.

View Article: PubMed Central - HTML - PubMed

Affiliation: Thünen Institute of Forest Genetics, Sieker Landstrasse 2, D-22927, Grosshansdorf, Germany. hilke.schroeder@ti.bund.de.

ABSTRACT

Background: The interaction between insect pests and their host plants is a never-ending race of evolutionary adaption. Plants have developed an armament against insect herbivore attacks, and attackers continuously learn how to address it. Using a combined transcriptomic and metabolomic approach, we investigated the molecular and biochemical differences between Quercus robur L. trees that resisted (defined as resistant oak type) or were susceptible (defined as susceptible oak type) to infestation by the major oak pest, Tortrix viridana L.

Results: Next generation RNA sequencing revealed hundreds of genes that exhibited constitutive and/or inducible differential expression in the resistant oak compared to the susceptible oak. Distinct differences were found in the transcript levels and the metabolic content with regard to tannins, flavonoids, and terpenoids, which are compounds involved in the defence against insect pests. The results of our transcriptomic and metabolomic analyses are in agreement with those of a previous study in which we showed that female moths prefer susceptible oaks due to their specific profile of herbivore-induced volatiles. These data therefore define two oak genotypes that clearly differ on the transcriptomic and metabolomic levels, as reflected by their specific defensive compound profiles.

Conclusions: We conclude that the resistant oak type seem to prefer a strategy of constitutive defence responses in contrast to more induced defence responses of the susceptible oaks triggered by feeding. These results pave the way for the development of biomarkers for an early determination of potentially green oak leaf roller-resistant genotypes in natural pedunculate oak populations in Europe.

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Model of a signalling cascade for oak’s constitutive and induced defence response. The model of the cascade is derived from a model recently published by Arimura et al.[32]. A: In the unfed control, the cascade is expected to be triggered by some 'damaged-self’ oligosaccharids (OS; grey circles) acting as elicitors activated by constitutively expressed cell wall degrading enzymes (CWDE; higher expressed in T-oaks than in S-oaks). B: Feeding by the leaf chewing insect T. viridana induces the release of herbivore-derived OS (green circles; elicitors) as well as of 'damaged-self’ OS and therefore initiates the cascade. The cascade itself is the same for the constitutive and induced defence response with different expression of transcripts in T- and S-oaks. Red squares represent transcripts stronger expressed in T-oaks and blue squares represent transcripts with higher expression in S-oaks. Transcripts assigned to the following MapMan BINs are presented: cellulases and beta -1,4-glucanases (CWDEs) belonging to cell wall degradation, jasmonate (JAs) related to hormone metabolism, proteasome (Proteasome) belonging to protein degradation, isoprenoids (Terpenes) and flavonoids (Flavonoids) related to secondary metabolism, ERF transcription factor family (ERF, ethylene-responsive factors), WRKY transcription factors (WRKY) belonging to regulation of transcription, histone (Histone) related to DNA synthesis/chromatin structure. Abbreviations: ACS, 1-aminocyclopropane-1-carboxylate; JAZ, jasmonate ZIM-domain; OS, oligosaccharids (elicitors); ROS, reactive oxygen species; SCF, SCF-type E3 ubiquitin ligase SCFCOI1.
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Figure 10: Model of a signalling cascade for oak’s constitutive and induced defence response. The model of the cascade is derived from a model recently published by Arimura et al.[32]. A: In the unfed control, the cascade is expected to be triggered by some 'damaged-self’ oligosaccharids (OS; grey circles) acting as elicitors activated by constitutively expressed cell wall degrading enzymes (CWDE; higher expressed in T-oaks than in S-oaks). B: Feeding by the leaf chewing insect T. viridana induces the release of herbivore-derived OS (green circles; elicitors) as well as of 'damaged-self’ OS and therefore initiates the cascade. The cascade itself is the same for the constitutive and induced defence response with different expression of transcripts in T- and S-oaks. Red squares represent transcripts stronger expressed in T-oaks and blue squares represent transcripts with higher expression in S-oaks. Transcripts assigned to the following MapMan BINs are presented: cellulases and beta -1,4-glucanases (CWDEs) belonging to cell wall degradation, jasmonate (JAs) related to hormone metabolism, proteasome (Proteasome) belonging to protein degradation, isoprenoids (Terpenes) and flavonoids (Flavonoids) related to secondary metabolism, ERF transcription factor family (ERF, ethylene-responsive factors), WRKY transcription factors (WRKY) belonging to regulation of transcription, histone (Histone) related to DNA synthesis/chromatin structure. Abbreviations: ACS, 1-aminocyclopropane-1-carboxylate; JAZ, jasmonate ZIM-domain; OS, oligosaccharids (elicitors); ROS, reactive oxygen species; SCF, SCF-type E3 ubiquitin ligase SCFCOI1.

Mentions: Plant defence responses to herbivory are driven by both herbivore-induced factors (e.g., elicitors, effectors, wounding) and plant signalling (e.g., phytohormones and plant volatiles; Figure 10) [32]. Figure 10 summarizes the constitutive and induced transcriptomic and metabolomic differences in T- and S-oaks responding to green oak leaf roller herbivory. The transcript levels of cell wall degrading enzymes (CWDE) are constitutively high in T-oaks (Figure 10A) but were found to be more inducible in S-oaks (Figure 10B). Changes in hormone signalling are likely to occur via the CDPK (Ca2+-dependent protein kinases) and MAPK (mitogen-activated protein kinase) cascades. Moreover, transcriptional changes at transcription factor genes are most likely responsible for the eventual activation of several defence response genes, such as those involved in the synthesis of volatiles and pathogen-related genes (Figure 10). The activated cascade results in a different response in T- and S-oaks mainly characterised by transcriptomic and metabolomic differences in the biosynthesis of tannins, flavonoids and terpenes (which is discussed in detail below).


Integrated transcriptomics and metabolomics decipher differences in the resistance of pedunculate oak to the herbivore Tortrix viridana L.

Kersten B, Ghirardo A, Schnitzler JP, Kanawati B, Schmitt-Kopplin P, Fladung M, Schroeder H - BMC Genomics (2013)

Model of a signalling cascade for oak’s constitutive and induced defence response. The model of the cascade is derived from a model recently published by Arimura et al.[32]. A: In the unfed control, the cascade is expected to be triggered by some 'damaged-self’ oligosaccharids (OS; grey circles) acting as elicitors activated by constitutively expressed cell wall degrading enzymes (CWDE; higher expressed in T-oaks than in S-oaks). B: Feeding by the leaf chewing insect T. viridana induces the release of herbivore-derived OS (green circles; elicitors) as well as of 'damaged-self’ OS and therefore initiates the cascade. The cascade itself is the same for the constitutive and induced defence response with different expression of transcripts in T- and S-oaks. Red squares represent transcripts stronger expressed in T-oaks and blue squares represent transcripts with higher expression in S-oaks. Transcripts assigned to the following MapMan BINs are presented: cellulases and beta -1,4-glucanases (CWDEs) belonging to cell wall degradation, jasmonate (JAs) related to hormone metabolism, proteasome (Proteasome) belonging to protein degradation, isoprenoids (Terpenes) and flavonoids (Flavonoids) related to secondary metabolism, ERF transcription factor family (ERF, ethylene-responsive factors), WRKY transcription factors (WRKY) belonging to regulation of transcription, histone (Histone) related to DNA synthesis/chromatin structure. Abbreviations: ACS, 1-aminocyclopropane-1-carboxylate; JAZ, jasmonate ZIM-domain; OS, oligosaccharids (elicitors); ROS, reactive oxygen species; SCF, SCF-type E3 ubiquitin ligase SCFCOI1.
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Figure 10: Model of a signalling cascade for oak’s constitutive and induced defence response. The model of the cascade is derived from a model recently published by Arimura et al.[32]. A: In the unfed control, the cascade is expected to be triggered by some 'damaged-self’ oligosaccharids (OS; grey circles) acting as elicitors activated by constitutively expressed cell wall degrading enzymes (CWDE; higher expressed in T-oaks than in S-oaks). B: Feeding by the leaf chewing insect T. viridana induces the release of herbivore-derived OS (green circles; elicitors) as well as of 'damaged-self’ OS and therefore initiates the cascade. The cascade itself is the same for the constitutive and induced defence response with different expression of transcripts in T- and S-oaks. Red squares represent transcripts stronger expressed in T-oaks and blue squares represent transcripts with higher expression in S-oaks. Transcripts assigned to the following MapMan BINs are presented: cellulases and beta -1,4-glucanases (CWDEs) belonging to cell wall degradation, jasmonate (JAs) related to hormone metabolism, proteasome (Proteasome) belonging to protein degradation, isoprenoids (Terpenes) and flavonoids (Flavonoids) related to secondary metabolism, ERF transcription factor family (ERF, ethylene-responsive factors), WRKY transcription factors (WRKY) belonging to regulation of transcription, histone (Histone) related to DNA synthesis/chromatin structure. Abbreviations: ACS, 1-aminocyclopropane-1-carboxylate; JAZ, jasmonate ZIM-domain; OS, oligosaccharids (elicitors); ROS, reactive oxygen species; SCF, SCF-type E3 ubiquitin ligase SCFCOI1.
Mentions: Plant defence responses to herbivory are driven by both herbivore-induced factors (e.g., elicitors, effectors, wounding) and plant signalling (e.g., phytohormones and plant volatiles; Figure 10) [32]. Figure 10 summarizes the constitutive and induced transcriptomic and metabolomic differences in T- and S-oaks responding to green oak leaf roller herbivory. The transcript levels of cell wall degrading enzymes (CWDE) are constitutively high in T-oaks (Figure 10A) but were found to be more inducible in S-oaks (Figure 10B). Changes in hormone signalling are likely to occur via the CDPK (Ca2+-dependent protein kinases) and MAPK (mitogen-activated protein kinase) cascades. Moreover, transcriptional changes at transcription factor genes are most likely responsible for the eventual activation of several defence response genes, such as those involved in the synthesis of volatiles and pathogen-related genes (Figure 10). The activated cascade results in a different response in T- and S-oaks mainly characterised by transcriptomic and metabolomic differences in the biosynthesis of tannins, flavonoids and terpenes (which is discussed in detail below).

Bottom Line: Next generation RNA sequencing revealed hundreds of genes that exhibited constitutive and/or inducible differential expression in the resistant oak compared to the susceptible oak.We conclude that the resistant oak type seem to prefer a strategy of constitutive defence responses in contrast to more induced defence responses of the susceptible oaks triggered by feeding.These results pave the way for the development of biomarkers for an early determination of potentially green oak leaf roller-resistant genotypes in natural pedunculate oak populations in Europe.

View Article: PubMed Central - HTML - PubMed

Affiliation: Thünen Institute of Forest Genetics, Sieker Landstrasse 2, D-22927, Grosshansdorf, Germany. hilke.schroeder@ti.bund.de.

ABSTRACT

Background: The interaction between insect pests and their host plants is a never-ending race of evolutionary adaption. Plants have developed an armament against insect herbivore attacks, and attackers continuously learn how to address it. Using a combined transcriptomic and metabolomic approach, we investigated the molecular and biochemical differences between Quercus robur L. trees that resisted (defined as resistant oak type) or were susceptible (defined as susceptible oak type) to infestation by the major oak pest, Tortrix viridana L.

Results: Next generation RNA sequencing revealed hundreds of genes that exhibited constitutive and/or inducible differential expression in the resistant oak compared to the susceptible oak. Distinct differences were found in the transcript levels and the metabolic content with regard to tannins, flavonoids, and terpenoids, which are compounds involved in the defence against insect pests. The results of our transcriptomic and metabolomic analyses are in agreement with those of a previous study in which we showed that female moths prefer susceptible oaks due to their specific profile of herbivore-induced volatiles. These data therefore define two oak genotypes that clearly differ on the transcriptomic and metabolomic levels, as reflected by their specific defensive compound profiles.

Conclusions: We conclude that the resistant oak type seem to prefer a strategy of constitutive defence responses in contrast to more induced defence responses of the susceptible oaks triggered by feeding. These results pave the way for the development of biomarkers for an early determination of potentially green oak leaf roller-resistant genotypes in natural pedunculate oak populations in Europe.

Show MeSH
Related in: MedlinePlus