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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

Identification of ascarosides from plant-parasitic nematodes.(a) Examples of ascarosides previously identified from C. elegans and other nematode species. (b) HPLC-MS analysis of M. hapla exo-metabolome samples, showing ion chromatograms scaled to 100% of the ascaroside peak corresponding to m/z=[M-H]− for seven detected ascarosides. (c) Chemical structures of identified ascarosides and relative quantitative distribution as determined by HPLC-MS. For high-resolution MS data, see Supplementary Table 1. Quantitative ascaroside profiles of M. incognita and M. javanica are shown in Supplementary Fig. 1.
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f1: Identification of ascarosides from plant-parasitic nematodes.(a) Examples of ascarosides previously identified from C. elegans and other nematode species. (b) HPLC-MS analysis of M. hapla exo-metabolome samples, showing ion chromatograms scaled to 100% of the ascaroside peak corresponding to m/z=[M-H]− for seven detected ascarosides. (c) Chemical structures of identified ascarosides and relative quantitative distribution as determined by HPLC-MS. For high-resolution MS data, see Supplementary Table 1. Quantitative ascaroside profiles of M. incognita and M. javanica are shown in Supplementary Fig. 1.

Mentions: To investigate the possibility that plants respond to ascarosides, we first characterized the ascaroside profiles produced by several genera of plant-parasitic nematodes. We used media supernatant samples to analyze the excreted metabolome (‘exo-metabolome') of infective juveniles of three species of root-knot nematodes, Meloidogyne incognita, M. javanica and M. hapla, as well as cyst (Heterodera glycines) and lesion (Pratylenchus brachyurus) nematodes, using a recently developed sensitive and selective mass spectrometric (MS) screening method27 (Fig. 1). MS analysis of exo-metabolome samples revealed excretion of similar sets of ascarosides in all analyzed species. In Meloidogyne spp., ascr#18, a compound featuring an 11-carbon side chain, was most abundant, followed by compounds with longer carbon side chains (Fig. 1a–c; Supplementary Fig. 1 and Supplementary Table 1). Concentrations of ascr#18 in the analyzed Meloidogyne spp. culture media samples were variable and ranged from 5 nM to 100 nM. Analysis of H. glycines and P. brachyurus metabolome samples also revealed ascr#18, albeit in smaller amounts than in Meloidogyne spp. (Supplementary Table 1). Exo-metabolome samples of adult M. hapla, H. glycines and P. brachyurus contained trace amounts of ascr#18, whereas the other ascarosides found in infective juveniles could not be detected in adults. These results show that plant-parasitic nematodes, like most other previously analyzed nematode species19, produce ascarosides. Notably, the analyzed species from three genera of plant-parasitic nematodes all produce ascr#18 as the most abundant ascaroside. Ascr#18 had previously been identified as a minor component of the ascaroside profile produced by the model organism C. elegans27 and is also produced by entomopathogenic nematodes1920.


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)

Identification of ascarosides from plant-parasitic nematodes.(a) Examples of ascarosides previously identified from C. elegans and other nematode species. (b) HPLC-MS analysis of M. hapla exo-metabolome samples, showing ion chromatograms scaled to 100% of the ascaroside peak corresponding to m/z=[M-H]− for seven detected ascarosides. (c) Chemical structures of identified ascarosides and relative quantitative distribution as determined by HPLC-MS. For high-resolution MS data, see Supplementary Table 1. Quantitative ascaroside profiles of M. incognita and M. javanica are shown in Supplementary Fig. 1.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f1: Identification of ascarosides from plant-parasitic nematodes.(a) Examples of ascarosides previously identified from C. elegans and other nematode species. (b) HPLC-MS analysis of M. hapla exo-metabolome samples, showing ion chromatograms scaled to 100% of the ascaroside peak corresponding to m/z=[M-H]− for seven detected ascarosides. (c) Chemical structures of identified ascarosides and relative quantitative distribution as determined by HPLC-MS. For high-resolution MS data, see Supplementary Table 1. Quantitative ascaroside profiles of M. incognita and M. javanica are shown in Supplementary Fig. 1.
Mentions: To investigate the possibility that plants respond to ascarosides, we first characterized the ascaroside profiles produced by several genera of plant-parasitic nematodes. We used media supernatant samples to analyze the excreted metabolome (‘exo-metabolome') of infective juveniles of three species of root-knot nematodes, Meloidogyne incognita, M. javanica and M. hapla, as well as cyst (Heterodera glycines) and lesion (Pratylenchus brachyurus) nematodes, using a recently developed sensitive and selective mass spectrometric (MS) screening method27 (Fig. 1). MS analysis of exo-metabolome samples revealed excretion of similar sets of ascarosides in all analyzed species. In Meloidogyne spp., ascr#18, a compound featuring an 11-carbon side chain, was most abundant, followed by compounds with longer carbon side chains (Fig. 1a–c; Supplementary Fig. 1 and Supplementary Table 1). Concentrations of ascr#18 in the analyzed Meloidogyne spp. culture media samples were variable and ranged from 5 nM to 100 nM. Analysis of H. glycines and P. brachyurus metabolome samples also revealed ascr#18, albeit in smaller amounts than in Meloidogyne spp. (Supplementary Table 1). Exo-metabolome samples of adult M. hapla, H. glycines and P. brachyurus contained trace amounts of ascr#18, whereas the other ascarosides found in infective juveniles could not be detected in adults. These results show that plant-parasitic nematodes, like most other previously analyzed nematode species19, produce ascarosides. Notably, the analyzed species from three genera of plant-parasitic nematodes all produce ascr#18 as the most abundant ascaroside. Ascr#18 had previously been identified as a minor component of the ascaroside profile produced by the model organism C. elegans27 and is also produced by entomopathogenic nematodes1920.

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