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Genome-Wide Characterization of ISR Induced in Arabidopsis thaliana by Trichoderma hamatum T382 Against Botrytis cinerea Infection.

Mathys J, De Cremer K, Timmermans P, Van Kerckhove S, Lievens B, Vanhaecke M, Cammue BP, De Coninck B - Front Plant Sci (2012)

Bottom Line: Treatment with T. hamatum T382 primes the plant (ISR-prime), resulting in an accelerated activation of the defense response against B. cinerea during ISR-boost and a subsequent moderation of the B. cinerea induced defense response.Microarray results were validated for representative genes by qRT-PCR.Combined with additional anthocyanin analysis data these results all point to the involvement of the phenylpropanoid pathway in T. hamatum T382-induced ISR.

View Article: PubMed Central - PubMed

Affiliation: Centre of Microbial and Plant Genetics, Katholieke Universiteit Leuven Heverlee, Belgium.

ABSTRACT
In this study, the molecular basis of the induced systemic resistance (ISR) in Arabidopsis thaliana by the biocontrol fungus Trichoderma hamatum T382 against the phytopathogen Botrytis cinerea B05-10 was unraveled by microarray analysis both before (ISR-prime) and after (ISR-boost) additional pathogen inoculation. The observed high numbers of differentially expressed genes allowed us to classify them according to the biological pathways in which they are involved. By focusing on pathways instead of genes, a holistic picture of the mechanisms underlying ISR emerged. In general, a close resemblance is observed between ISR-prime and systemic acquired resistance, the systemic defense response that is triggered in plants upon pathogen infection leading to increased resistance toward secondary infections. Treatment with T. hamatum T382 primes the plant (ISR-prime), resulting in an accelerated activation of the defense response against B. cinerea during ISR-boost and a subsequent moderation of the B. cinerea induced defense response. Microarray results were validated for representative genes by qRT-PCR. The involvement of various defense-related pathways was confirmed by phenotypic analysis of mutants affected in these pathways, thereby proving the validity of our approach. Combined with additional anthocyanin analysis data these results all point to the involvement of the phenylpropanoid pathway in T. hamatum T382-induced ISR.

No MeSH data available.


Related in: MedlinePlus

Overview of modulation of expression of genes in four defense-related pathways as a result of ISR and BIDR. Selected pathways include those involved in MAMP-triggered defense and subsequent ROS-production (A) (based on Asai et al., 2002; Kaupp and Seifert, 2002; Mittler et al., 2004; Wan et al., 2004; Kotchoni and Gachomo, 2006; Pitzschke et al., 2006; Tsuda et al., 2008; Van Breusegem et al., 2008; Li et al., 2009; Christensen et al., 2010; Foyer and Noctor, 2011; Ranf et al., 2011), those mediated by SA (B) (based on Shah, 2003; Dong, 2004; Katagiri, 2004; Glazebrook, 2005; Wang et al., 2006; Krinke et al., 2007; van Leeuwen et al., 2007), or JA (C) (based on Sasaki et al., 2001; Stintzi et al., 2001; Glazebrook et al., 2003; Delker et al., 2006; Ndamukong et al., 2007; van Leeuwen et al., 2007; Wasternack, 2007; Chico et al., 2008; Koornneef et al., 2008; Mueller et al., 2008; Lee et al., 2009; Fonseca et al., 2010) and the phenylpropanoid pathway leading to the production of lignin, flavonoids, and anthocyanins (D) (based on Winkel-Shirley, 2002; Routaboul et al., 2006; Ferrer et al., 2008). For each pathway except for the JA-pathway three panels can be distinguished: Upper panel: overview of modulated gene expression during ISR-prime in plants 2 days post-inoculation with T. hamatum T382 vs. mock-treated control plants. Middle panel: overview of modulated gene expression during BIDR in plants 2 days post-inoculation with B. cinerea vs. mock-treated control plants. Lower panel: overview of modulated gene expression during ISR-boost in plants pretreated with T. hamatum T382 vs. mock-treated control plants, both 2 days post-inoculation with B. cinerea. For the JA-pathway five panels can be distinguished because both 1 and 2 days post-inoculation with B. cinerea are shown for ISR-boost and BIDR. Up- and downregulated genes are shown in red and green respectively. Gene names are in conformity with TAIR annotation.
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Figure 6: Overview of modulation of expression of genes in four defense-related pathways as a result of ISR and BIDR. Selected pathways include those involved in MAMP-triggered defense and subsequent ROS-production (A) (based on Asai et al., 2002; Kaupp and Seifert, 2002; Mittler et al., 2004; Wan et al., 2004; Kotchoni and Gachomo, 2006; Pitzschke et al., 2006; Tsuda et al., 2008; Van Breusegem et al., 2008; Li et al., 2009; Christensen et al., 2010; Foyer and Noctor, 2011; Ranf et al., 2011), those mediated by SA (B) (based on Shah, 2003; Dong, 2004; Katagiri, 2004; Glazebrook, 2005; Wang et al., 2006; Krinke et al., 2007; van Leeuwen et al., 2007), or JA (C) (based on Sasaki et al., 2001; Stintzi et al., 2001; Glazebrook et al., 2003; Delker et al., 2006; Ndamukong et al., 2007; van Leeuwen et al., 2007; Wasternack, 2007; Chico et al., 2008; Koornneef et al., 2008; Mueller et al., 2008; Lee et al., 2009; Fonseca et al., 2010) and the phenylpropanoid pathway leading to the production of lignin, flavonoids, and anthocyanins (D) (based on Winkel-Shirley, 2002; Routaboul et al., 2006; Ferrer et al., 2008). For each pathway except for the JA-pathway three panels can be distinguished: Upper panel: overview of modulated gene expression during ISR-prime in plants 2 days post-inoculation with T. hamatum T382 vs. mock-treated control plants. Middle panel: overview of modulated gene expression during BIDR in plants 2 days post-inoculation with B. cinerea vs. mock-treated control plants. Lower panel: overview of modulated gene expression during ISR-boost in plants pretreated with T. hamatum T382 vs. mock-treated control plants, both 2 days post-inoculation with B. cinerea. For the JA-pathway five panels can be distinguished because both 1 and 2 days post-inoculation with B. cinerea are shown for ISR-boost and BIDR. Up- and downregulated genes are shown in red and green respectively. Gene names are in conformity with TAIR annotation.

Mentions: In this study we demonstrated that application of T. hamatum T382 to the roots of A. thaliana results in an increased resistance to subsequent leaf infections by the necrotrophic pathogen B. cinerea, characterized by a significant reduction in symptom development. This tripartite model allowed a genome-wide analysis of ISR-related gene expression using microarrays. More specifically, gene expression was characterized both before (ISR-prime) and after (ISR-boost) additional B. cinerea inoculation in T. hamatum T382-pretreated plants as compared to mock-pretreated controls. To allow further comparison with the regular defense response induced by this pathogen, further mentioned as BIDR, we also compared B. cinerea infected plants without T. hamatum T382-pretreatment with uninfected controls. Aiming at a holistic view on ISR, we classified the ISR- and BIDR-related genes into the standard biological processes, as defined by the Gene Ontology Consortium (2000), that were significantly induced or downregulated (Table 2). However, since (i) not all relevant biological processes are represented in Gene Ontology (e.g. MAMP-triggered defense is as such not present), and (ii) the analysis of enriched biological processes might miss small differences between ISR and BIDR, we opted to perform an additional reverse analysis process by starting from the structure of a pathway and identifying the differentially expressed genes in that pathway. We focused on pathways with a relatively well-known structure on different reported levels of the plant’s defense response including (i) early processes related to MAMP-triggered defense and the subsequent production of reactive oxygen species (ROS; Figure 6A), (ii) downstream signaling [e.g. mediated by SA (Figure 6B) and JA (Figure 6C)] leading to the production of defense-related components (e.g. different types of PR proteins), and (iii) general stress responses such as those occurring via the phenyl propanoid pathway (Figure 6D). The induction or downregulation of genes was visualized in Figure 6 by red and green boxes, respectively, allowing visual comparison of general gene modulation during ISR-prime, ISR-boost and BIDR. By combining this overview with results shown earlier in this manuscript the following overall conclusions can be drawn.


Genome-Wide Characterization of ISR Induced in Arabidopsis thaliana by Trichoderma hamatum T382 Against Botrytis cinerea Infection.

Mathys J, De Cremer K, Timmermans P, Van Kerckhove S, Lievens B, Vanhaecke M, Cammue BP, De Coninck B - Front Plant Sci (2012)

Overview of modulation of expression of genes in four defense-related pathways as a result of ISR and BIDR. Selected pathways include those involved in MAMP-triggered defense and subsequent ROS-production (A) (based on Asai et al., 2002; Kaupp and Seifert, 2002; Mittler et al., 2004; Wan et al., 2004; Kotchoni and Gachomo, 2006; Pitzschke et al., 2006; Tsuda et al., 2008; Van Breusegem et al., 2008; Li et al., 2009; Christensen et al., 2010; Foyer and Noctor, 2011; Ranf et al., 2011), those mediated by SA (B) (based on Shah, 2003; Dong, 2004; Katagiri, 2004; Glazebrook, 2005; Wang et al., 2006; Krinke et al., 2007; van Leeuwen et al., 2007), or JA (C) (based on Sasaki et al., 2001; Stintzi et al., 2001; Glazebrook et al., 2003; Delker et al., 2006; Ndamukong et al., 2007; van Leeuwen et al., 2007; Wasternack, 2007; Chico et al., 2008; Koornneef et al., 2008; Mueller et al., 2008; Lee et al., 2009; Fonseca et al., 2010) and the phenylpropanoid pathway leading to the production of lignin, flavonoids, and anthocyanins (D) (based on Winkel-Shirley, 2002; Routaboul et al., 2006; Ferrer et al., 2008). For each pathway except for the JA-pathway three panels can be distinguished: Upper panel: overview of modulated gene expression during ISR-prime in plants 2 days post-inoculation with T. hamatum T382 vs. mock-treated control plants. Middle panel: overview of modulated gene expression during BIDR in plants 2 days post-inoculation with B. cinerea vs. mock-treated control plants. Lower panel: overview of modulated gene expression during ISR-boost in plants pretreated with T. hamatum T382 vs. mock-treated control plants, both 2 days post-inoculation with B. cinerea. For the JA-pathway five panels can be distinguished because both 1 and 2 days post-inoculation with B. cinerea are shown for ISR-boost and BIDR. Up- and downregulated genes are shown in red and green respectively. Gene names are in conformity with TAIR annotation.
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Related In: Results  -  Collection

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Figure 6: Overview of modulation of expression of genes in four defense-related pathways as a result of ISR and BIDR. Selected pathways include those involved in MAMP-triggered defense and subsequent ROS-production (A) (based on Asai et al., 2002; Kaupp and Seifert, 2002; Mittler et al., 2004; Wan et al., 2004; Kotchoni and Gachomo, 2006; Pitzschke et al., 2006; Tsuda et al., 2008; Van Breusegem et al., 2008; Li et al., 2009; Christensen et al., 2010; Foyer and Noctor, 2011; Ranf et al., 2011), those mediated by SA (B) (based on Shah, 2003; Dong, 2004; Katagiri, 2004; Glazebrook, 2005; Wang et al., 2006; Krinke et al., 2007; van Leeuwen et al., 2007), or JA (C) (based on Sasaki et al., 2001; Stintzi et al., 2001; Glazebrook et al., 2003; Delker et al., 2006; Ndamukong et al., 2007; van Leeuwen et al., 2007; Wasternack, 2007; Chico et al., 2008; Koornneef et al., 2008; Mueller et al., 2008; Lee et al., 2009; Fonseca et al., 2010) and the phenylpropanoid pathway leading to the production of lignin, flavonoids, and anthocyanins (D) (based on Winkel-Shirley, 2002; Routaboul et al., 2006; Ferrer et al., 2008). For each pathway except for the JA-pathway three panels can be distinguished: Upper panel: overview of modulated gene expression during ISR-prime in plants 2 days post-inoculation with T. hamatum T382 vs. mock-treated control plants. Middle panel: overview of modulated gene expression during BIDR in plants 2 days post-inoculation with B. cinerea vs. mock-treated control plants. Lower panel: overview of modulated gene expression during ISR-boost in plants pretreated with T. hamatum T382 vs. mock-treated control plants, both 2 days post-inoculation with B. cinerea. For the JA-pathway five panels can be distinguished because both 1 and 2 days post-inoculation with B. cinerea are shown for ISR-boost and BIDR. Up- and downregulated genes are shown in red and green respectively. Gene names are in conformity with TAIR annotation.
Mentions: In this study we demonstrated that application of T. hamatum T382 to the roots of A. thaliana results in an increased resistance to subsequent leaf infections by the necrotrophic pathogen B. cinerea, characterized by a significant reduction in symptom development. This tripartite model allowed a genome-wide analysis of ISR-related gene expression using microarrays. More specifically, gene expression was characterized both before (ISR-prime) and after (ISR-boost) additional B. cinerea inoculation in T. hamatum T382-pretreated plants as compared to mock-pretreated controls. To allow further comparison with the regular defense response induced by this pathogen, further mentioned as BIDR, we also compared B. cinerea infected plants without T. hamatum T382-pretreatment with uninfected controls. Aiming at a holistic view on ISR, we classified the ISR- and BIDR-related genes into the standard biological processes, as defined by the Gene Ontology Consortium (2000), that were significantly induced or downregulated (Table 2). However, since (i) not all relevant biological processes are represented in Gene Ontology (e.g. MAMP-triggered defense is as such not present), and (ii) the analysis of enriched biological processes might miss small differences between ISR and BIDR, we opted to perform an additional reverse analysis process by starting from the structure of a pathway and identifying the differentially expressed genes in that pathway. We focused on pathways with a relatively well-known structure on different reported levels of the plant’s defense response including (i) early processes related to MAMP-triggered defense and the subsequent production of reactive oxygen species (ROS; Figure 6A), (ii) downstream signaling [e.g. mediated by SA (Figure 6B) and JA (Figure 6C)] leading to the production of defense-related components (e.g. different types of PR proteins), and (iii) general stress responses such as those occurring via the phenyl propanoid pathway (Figure 6D). The induction or downregulation of genes was visualized in Figure 6 by red and green boxes, respectively, allowing visual comparison of general gene modulation during ISR-prime, ISR-boost and BIDR. By combining this overview with results shown earlier in this manuscript the following overall conclusions can be drawn.

Bottom Line: Treatment with T. hamatum T382 primes the plant (ISR-prime), resulting in an accelerated activation of the defense response against B. cinerea during ISR-boost and a subsequent moderation of the B. cinerea induced defense response.Microarray results were validated for representative genes by qRT-PCR.Combined with additional anthocyanin analysis data these results all point to the involvement of the phenylpropanoid pathway in T. hamatum T382-induced ISR.

View Article: PubMed Central - PubMed

Affiliation: Centre of Microbial and Plant Genetics, Katholieke Universiteit Leuven Heverlee, Belgium.

ABSTRACT
In this study, the molecular basis of the induced systemic resistance (ISR) in Arabidopsis thaliana by the biocontrol fungus Trichoderma hamatum T382 against the phytopathogen Botrytis cinerea B05-10 was unraveled by microarray analysis both before (ISR-prime) and after (ISR-boost) additional pathogen inoculation. The observed high numbers of differentially expressed genes allowed us to classify them according to the biological pathways in which they are involved. By focusing on pathways instead of genes, a holistic picture of the mechanisms underlying ISR emerged. In general, a close resemblance is observed between ISR-prime and systemic acquired resistance, the systemic defense response that is triggered in plants upon pathogen infection leading to increased resistance toward secondary infections. Treatment with T. hamatum T382 primes the plant (ISR-prime), resulting in an accelerated activation of the defense response against B. cinerea during ISR-boost and a subsequent moderation of the B. cinerea induced defense response. Microarray results were validated for representative genes by qRT-PCR. The involvement of various defense-related pathways was confirmed by phenotypic analysis of mutants affected in these pathways, thereby proving the validity of our approach. Combined with additional anthocyanin analysis data these results all point to the involvement of the phenylpropanoid pathway in T. hamatum T382-induced ISR.

No MeSH data available.


Related in: MedlinePlus