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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

Effects of ascr#18 on resistance to a fungal pathogen in barley and to two species of nematodes in Arabidopsis.(a) Effect of leaf pretreatment with ascr#18 on resistance of barley to Blumeria graminis f. sp. hordei (Bgh). Leaves were sprayed with ascr#18 solutions 48 h before inoculation. Bgh pustules were counted at 7 d.p.i. Data are average±s.d. (n =10). (b) Induction of PR-1 expression by leaf pretreatment with ascr#18. Plants were inoculated with Bgh 48 h post pretreatment and leaves were collected at 16 h.p.i. for qRT-PCR analysis. Data are average±s.d. (n=3). (c) Effect of ascr#18 on Arabidopsis susceptibility to sugar-beet cyst nematode (H. schachtii). Ten days-old Arabidopsis seedlings were pretreated with buffer or 0.01 and 0.3 μM of ascr#18 for 48 h before inoculation with about 200 freshly hatched and surface-sterilized juveniles per seedlings. The numbers of females were counted 4 weeks after inoculation. (d) Effect of ascr#18 on Arabidopsis susceptibility to root-knot nematode (M. incognita). Ten day-old Arabidopsis seedlings were pretreated with the indicated ascr#18 concentrations for 48 h before inoculation with ∼300 freshly hatched and surface-sterilized juveniles per seedlings. The numbers of galls were counted under microscope 6 weeks after inoculation. Data are average±s.d. (n=5). (*P≤0.05; **P≤0.005; ***P≤0.0005, two-tailed t-test).
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f4: Effects of ascr#18 on resistance to a fungal pathogen in barley and to two species of nematodes in Arabidopsis.(a) Effect of leaf pretreatment with ascr#18 on resistance of barley to Blumeria graminis f. sp. hordei (Bgh). Leaves were sprayed with ascr#18 solutions 48 h before inoculation. Bgh pustules were counted at 7 d.p.i. Data are average±s.d. (n =10). (b) Induction of PR-1 expression by leaf pretreatment with ascr#18. Plants were inoculated with Bgh 48 h post pretreatment and leaves were collected at 16 h.p.i. for qRT-PCR analysis. Data are average±s.d. (n=3). (c) Effect of ascr#18 on Arabidopsis susceptibility to sugar-beet cyst nematode (H. schachtii). Ten days-old Arabidopsis seedlings were pretreated with buffer or 0.01 and 0.3 μM of ascr#18 for 48 h before inoculation with about 200 freshly hatched and surface-sterilized juveniles per seedlings. The numbers of females were counted 4 weeks after inoculation. (d) Effect of ascr#18 on Arabidopsis susceptibility to root-knot nematode (M. incognita). Ten day-old Arabidopsis seedlings were pretreated with the indicated ascr#18 concentrations for 48 h before inoculation with ∼300 freshly hatched and surface-sterilized juveniles per seedlings. The numbers of galls were counted under microscope 6 weeks after inoculation. Data are average±s.d. (n=5). (*P≤0.05; **P≤0.005; ***P≤0.0005, two-tailed t-test).

Mentions: To test whether ascr#18 activates defense responses in monocots, leaves of barley (Hordeum vulgare) were sprayed with ascr#18 48 h prior to inoculation with the virulent fungal pathogen Blumeria graminis f. sp. hordei (Bgh). Pretreatment with a wide range of ascr#18 concentrations (0.01–1 μM) increased resistance to Bgh, based on the reduced numbers of pustules formed on the leaves (Fig. 4a). This pretreatment also induced PR-1 transcript accumulation; even higher levels of PR-1 expression were observed in ascr#18-pretreated leaves that were subsequently inoculated with Bgh, suggesting a priming effect of ascr#18 in barley (Fig. 4b). Taken together, our results show that ascr#18 is perceived by monocots and dicots and induces defense responses that enhance resistance against four major classes of pathogens.


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)

Effects of ascr#18 on resistance to a fungal pathogen in barley and to two species of nematodes in Arabidopsis.(a) Effect of leaf pretreatment with ascr#18 on resistance of barley to Blumeria graminis f. sp. hordei (Bgh). Leaves were sprayed with ascr#18 solutions 48 h before inoculation. Bgh pustules were counted at 7 d.p.i. Data are average±s.d. (n =10). (b) Induction of PR-1 expression by leaf pretreatment with ascr#18. Plants were inoculated with Bgh 48 h post pretreatment and leaves were collected at 16 h.p.i. for qRT-PCR analysis. Data are average±s.d. (n=3). (c) Effect of ascr#18 on Arabidopsis susceptibility to sugar-beet cyst nematode (H. schachtii). Ten days-old Arabidopsis seedlings were pretreated with buffer or 0.01 and 0.3 μM of ascr#18 for 48 h before inoculation with about 200 freshly hatched and surface-sterilized juveniles per seedlings. The numbers of females were counted 4 weeks after inoculation. (d) Effect of ascr#18 on Arabidopsis susceptibility to root-knot nematode (M. incognita). Ten day-old Arabidopsis seedlings were pretreated with the indicated ascr#18 concentrations for 48 h before inoculation with ∼300 freshly hatched and surface-sterilized juveniles per seedlings. The numbers of galls were counted under microscope 6 weeks after inoculation. Data are average±s.d. (n=5). (*P≤0.05; **P≤0.005; ***P≤0.0005, two-tailed t-test).
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f4: Effects of ascr#18 on resistance to a fungal pathogen in barley and to two species of nematodes in Arabidopsis.(a) Effect of leaf pretreatment with ascr#18 on resistance of barley to Blumeria graminis f. sp. hordei (Bgh). Leaves were sprayed with ascr#18 solutions 48 h before inoculation. Bgh pustules were counted at 7 d.p.i. Data are average±s.d. (n =10). (b) Induction of PR-1 expression by leaf pretreatment with ascr#18. Plants were inoculated with Bgh 48 h post pretreatment and leaves were collected at 16 h.p.i. for qRT-PCR analysis. Data are average±s.d. (n=3). (c) Effect of ascr#18 on Arabidopsis susceptibility to sugar-beet cyst nematode (H. schachtii). Ten days-old Arabidopsis seedlings were pretreated with buffer or 0.01 and 0.3 μM of ascr#18 for 48 h before inoculation with about 200 freshly hatched and surface-sterilized juveniles per seedlings. The numbers of females were counted 4 weeks after inoculation. (d) Effect of ascr#18 on Arabidopsis susceptibility to root-knot nematode (M. incognita). Ten day-old Arabidopsis seedlings were pretreated with the indicated ascr#18 concentrations for 48 h before inoculation with ∼300 freshly hatched and surface-sterilized juveniles per seedlings. The numbers of galls were counted under microscope 6 weeks after inoculation. Data are average±s.d. (n=5). (*P≤0.05; **P≤0.005; ***P≤0.0005, two-tailed t-test).
Mentions: To test whether ascr#18 activates defense responses in monocots, leaves of barley (Hordeum vulgare) were sprayed with ascr#18 48 h prior to inoculation with the virulent fungal pathogen Blumeria graminis f. sp. hordei (Bgh). Pretreatment with a wide range of ascr#18 concentrations (0.01–1 μM) increased resistance to Bgh, based on the reduced numbers of pustules formed on the leaves (Fig. 4a). This pretreatment also induced PR-1 transcript accumulation; even higher levels of PR-1 expression were observed in ascr#18-pretreated leaves that were subsequently inoculated with Bgh, suggesting a priming effect of ascr#18 in barley (Fig. 4b). Taken together, our results show that ascr#18 is perceived by monocots and dicots and induces defense responses that enhance resistance against four major classes of pathogens.

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