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Conserved nematode signalling molecules elicit plant defenses and pathogen resistance.

Manosalva P, Manohar M, von Reuss SH, Chen S, Koch A, Kaplan F, Choe A, Micikas RJ, Wang X, Kogel KH, Sternberg PW, Williamson VM, Schroeder FC, Klessig DF - Nat Commun (2015)

Bottom Line: Plant-defense responses are triggered by perception of conserved microbe-associated molecular patterns (MAMPs), for example, flagellin or peptidoglycan.Picomolar to micromolar concentrations of ascr#18, the major ascaroside in plant-parasitic nematodes, induce hallmark defense responses including the expression of genes associated with MAMP-triggered immunity, activation of mitogen-activated protein kinases, as well as salicylic acid- and jasmonic acid-mediated defense signalling pathways.These results indicate that plants recognize ascarosides as a conserved molecular signature of nematodes.

View Article: PubMed Central - PubMed

Affiliation: 1] Boyce Thompson Institute for Plant Research, Ithaca, New York 14853, USA [2] Department of Plant Pathology and Microbiology, University of California Riverside, Riverside, California 92521, USA.

ABSTRACT
Plant-defense responses are triggered by perception of conserved microbe-associated molecular patterns (MAMPs), for example, flagellin or peptidoglycan. However, it remained unknown whether plants can detect conserved molecular patterns derived from plant-parasitic animals, including nematodes. Here we show that several genera of plant-parasitic nematodes produce small molecules called ascarosides, an evolutionarily conserved family of nematode pheromones. Picomolar to micromolar concentrations of ascr#18, the major ascaroside in plant-parasitic nematodes, induce hallmark defense responses including the expression of genes associated with MAMP-triggered immunity, activation of mitogen-activated protein kinases, as well as salicylic acid- and jasmonic acid-mediated defense signalling pathways. Ascr#18 perception increases resistance in Arabidopsis, tomato, potato and barley to viral, bacterial, oomycete, fungal and nematode infections. These results indicate that plants recognize ascarosides as a conserved molecular signature of nematodes. Using small-molecule signals such as ascarosides to activate plant immune responses has potential utility to improve economic and environmental sustainability of agriculture.

No MeSH data available.


Related in: MedlinePlus

Ascr#18 enhanced pathogen resistance and activated defense responses in Arabidopsis.(a) Enhanced resistance to virulent Pseudomonas syringae pv. tomato (Pst) DC3000 after root pretreatment for 24 h with ascr#18. Bacterial growth was assayed at 3 d.p.i. Data are averages±s.d. (n≥3). (b) Quantification of TCV CP in inoculated (local) and uninoculated (systemic) leaves of plants root pretreated for 24 h with ascr#18. Leaves were harvested at 2, 3 and 6 d.p.i. for immunoblot analysis with the anti-CP antibody. Coomassie blue staining (CB) served as loading control. (c) TCV-inoculated (local) leaves photographed at 6 d.p.i. (d) TCV-infected plants photographed at 6 d.p.i. (e) Transcript levels as measured by qRT-PCR of defense-gene markers in leaves from plants root pretreated with ascr#18 (1 μM). Gene-transcript levels were determined at 6 h.p.t. and 24 h.p.t. Data are average±s.d. (n=3). (f) Activation of MAPKs MPK3 and MPK6 in Arabidopsis 10 and 15 min after leaf pretreatment with ascr#18. CB served as loading control. (g) Induction of SA and JA marker genes PR-1 and PDF1.2, respectively, after syringe infiltration of leaves with ascr#18, as measured by qRT-PCR. β-tubulin was used as internal control. *P≤0.05; **P≤0.005; ***P≤0.0005, two-tailed t-test.
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f2: Ascr#18 enhanced pathogen resistance and activated defense responses in Arabidopsis.(a) Enhanced resistance to virulent Pseudomonas syringae pv. tomato (Pst) DC3000 after root pretreatment for 24 h with ascr#18. Bacterial growth was assayed at 3 d.p.i. Data are averages±s.d. (n≥3). (b) Quantification of TCV CP in inoculated (local) and uninoculated (systemic) leaves of plants root pretreated for 24 h with ascr#18. Leaves were harvested at 2, 3 and 6 d.p.i. for immunoblot analysis with the anti-CP antibody. Coomassie blue staining (CB) served as loading control. (c) TCV-inoculated (local) leaves photographed at 6 d.p.i. (d) TCV-infected plants photographed at 6 d.p.i. (e) Transcript levels as measured by qRT-PCR of defense-gene markers in leaves from plants root pretreated with ascr#18 (1 μM). Gene-transcript levels were determined at 6 h.p.t. and 24 h.p.t. Data are average±s.d. (n=3). (f) Activation of MAPKs MPK3 and MPK6 in Arabidopsis 10 and 15 min after leaf pretreatment with ascr#18. CB served as loading control. (g) Induction of SA and JA marker genes PR-1 and PDF1.2, respectively, after syringe infiltration of leaves with ascr#18, as measured by qRT-PCR. β-tubulin was used as internal control. *P≤0.05; **P≤0.005; ***P≤0.0005, two-tailed t-test.

Mentions: On the basis of the finding that ascr#18 is produced by all analyzed species of plant-parasitic nematodes, we asked whether this ascaroside is perceived by plants and affects plant-defense responses to diverse pathogens. Because ascarosides as the nematode signalling molecules may have direct effects on nematode pathogens that could confound detection of plant responses to ascr#18, we began by testing the effect of ascr#18 on defense responses of Arabidopsis to a bacterial (Pseudomonas syringae pv. tomato) and a viral pathogen (Turnip Crinkle Virus—TCV; Fig. 2). Since plants would naturally encounter nematodes via their roots, Arabidopsis roots were partially immersed in water containing different concentrations of ascr#18 for 24 h before leaves were inoculated with the pathogens. Root treatment with 1 μM ascr#18 reduced growth of virulent P. syringae, whereas a higher ascr#18 concentration (5 μM) was less effective (Fig. 2a). Root treatment with ascr#18 at 1 μM also enhanced resistance to virulent TCV (Fig. 2b–d, Supplementary Fig. 2.). Viral replication, as measured by the amount of viral coat protein (CP) in leaves (Fig. 2b), was reduced in both inoculated and distal leaves. Moreover, systemic spread of the virus was nearly abolished with only a trace of CP present in distal leaves of ascr#18-pretreated plants. Disease symptoms, including development of chlorosis on the inoculated leaves (Fig. 2c), leaf curling/crinkling and suppression of inflorescence development (Fig. 2d), were also reduced in ascr#18-pretreated plants.


Conserved nematode signalling molecules elicit plant defenses and pathogen resistance.

Manosalva P, Manohar M, von Reuss SH, Chen S, Koch A, Kaplan F, Choe A, Micikas RJ, Wang X, Kogel KH, Sternberg PW, Williamson VM, Schroeder FC, Klessig DF - Nat Commun (2015)

Ascr#18 enhanced pathogen resistance and activated defense responses in Arabidopsis.(a) Enhanced resistance to virulent Pseudomonas syringae pv. tomato (Pst) DC3000 after root pretreatment for 24 h with ascr#18. Bacterial growth was assayed at 3 d.p.i. Data are averages±s.d. (n≥3). (b) Quantification of TCV CP in inoculated (local) and uninoculated (systemic) leaves of plants root pretreated for 24 h with ascr#18. Leaves were harvested at 2, 3 and 6 d.p.i. for immunoblot analysis with the anti-CP antibody. Coomassie blue staining (CB) served as loading control. (c) TCV-inoculated (local) leaves photographed at 6 d.p.i. (d) TCV-infected plants photographed at 6 d.p.i. (e) Transcript levels as measured by qRT-PCR of defense-gene markers in leaves from plants root pretreated with ascr#18 (1 μM). Gene-transcript levels were determined at 6 h.p.t. and 24 h.p.t. Data are average±s.d. (n=3). (f) Activation of MAPKs MPK3 and MPK6 in Arabidopsis 10 and 15 min after leaf pretreatment with ascr#18. CB served as loading control. (g) Induction of SA and JA marker genes PR-1 and PDF1.2, respectively, after syringe infiltration of leaves with ascr#18, as measured by qRT-PCR. β-tubulin was used as internal control. *P≤0.05; **P≤0.005; ***P≤0.0005, two-tailed t-test.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4525156&req=5

f2: Ascr#18 enhanced pathogen resistance and activated defense responses in Arabidopsis.(a) Enhanced resistance to virulent Pseudomonas syringae pv. tomato (Pst) DC3000 after root pretreatment for 24 h with ascr#18. Bacterial growth was assayed at 3 d.p.i. Data are averages±s.d. (n≥3). (b) Quantification of TCV CP in inoculated (local) and uninoculated (systemic) leaves of plants root pretreated for 24 h with ascr#18. Leaves were harvested at 2, 3 and 6 d.p.i. for immunoblot analysis with the anti-CP antibody. Coomassie blue staining (CB) served as loading control. (c) TCV-inoculated (local) leaves photographed at 6 d.p.i. (d) TCV-infected plants photographed at 6 d.p.i. (e) Transcript levels as measured by qRT-PCR of defense-gene markers in leaves from plants root pretreated with ascr#18 (1 μM). Gene-transcript levels were determined at 6 h.p.t. and 24 h.p.t. Data are average±s.d. (n=3). (f) Activation of MAPKs MPK3 and MPK6 in Arabidopsis 10 and 15 min after leaf pretreatment with ascr#18. CB served as loading control. (g) Induction of SA and JA marker genes PR-1 and PDF1.2, respectively, after syringe infiltration of leaves with ascr#18, as measured by qRT-PCR. β-tubulin was used as internal control. *P≤0.05; **P≤0.005; ***P≤0.0005, two-tailed t-test.
Mentions: On the basis of the finding that ascr#18 is produced by all analyzed species of plant-parasitic nematodes, we asked whether this ascaroside is perceived by plants and affects plant-defense responses to diverse pathogens. Because ascarosides as the nematode signalling molecules may have direct effects on nematode pathogens that could confound detection of plant responses to ascr#18, we began by testing the effect of ascr#18 on defense responses of Arabidopsis to a bacterial (Pseudomonas syringae pv. tomato) and a viral pathogen (Turnip Crinkle Virus—TCV; Fig. 2). Since plants would naturally encounter nematodes via their roots, Arabidopsis roots were partially immersed in water containing different concentrations of ascr#18 for 24 h before leaves were inoculated with the pathogens. Root treatment with 1 μM ascr#18 reduced growth of virulent P. syringae, whereas a higher ascr#18 concentration (5 μM) was less effective (Fig. 2a). Root treatment with ascr#18 at 1 μM also enhanced resistance to virulent TCV (Fig. 2b–d, Supplementary Fig. 2.). Viral replication, as measured by the amount of viral coat protein (CP) in leaves (Fig. 2b), was reduced in both inoculated and distal leaves. Moreover, systemic spread of the virus was nearly abolished with only a trace of CP present in distal leaves of ascr#18-pretreated plants. Disease symptoms, including development of chlorosis on the inoculated leaves (Fig. 2c), leaf curling/crinkling and suppression of inflorescence development (Fig. 2d), were also reduced in ascr#18-pretreated plants.

Bottom Line: Plant-defense responses are triggered by perception of conserved microbe-associated molecular patterns (MAMPs), for example, flagellin or peptidoglycan.Picomolar to micromolar concentrations of ascr#18, the major ascaroside in plant-parasitic nematodes, induce hallmark defense responses including the expression of genes associated with MAMP-triggered immunity, activation of mitogen-activated protein kinases, as well as salicylic acid- and jasmonic acid-mediated defense signalling pathways.These results indicate that plants recognize ascarosides as a conserved molecular signature of nematodes.

View Article: PubMed Central - PubMed

Affiliation: 1] Boyce Thompson Institute for Plant Research, Ithaca, New York 14853, USA [2] Department of Plant Pathology and Microbiology, University of California Riverside, Riverside, California 92521, USA.

ABSTRACT
Plant-defense responses are triggered by perception of conserved microbe-associated molecular patterns (MAMPs), for example, flagellin or peptidoglycan. However, it remained unknown whether plants can detect conserved molecular patterns derived from plant-parasitic animals, including nematodes. Here we show that several genera of plant-parasitic nematodes produce small molecules called ascarosides, an evolutionarily conserved family of nematode pheromones. Picomolar to micromolar concentrations of ascr#18, the major ascaroside in plant-parasitic nematodes, induce hallmark defense responses including the expression of genes associated with MAMP-triggered immunity, activation of mitogen-activated protein kinases, as well as salicylic acid- and jasmonic acid-mediated defense signalling pathways. Ascr#18 perception increases resistance in Arabidopsis, tomato, potato and barley to viral, bacterial, oomycete, fungal and nematode infections. These results indicate that plants recognize ascarosides as a conserved molecular signature of nematodes. Using small-molecule signals such as ascarosides to activate plant immune responses has potential utility to improve economic and environmental sustainability of agriculture.

No MeSH data available.


Related in: MedlinePlus