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Identification and characterisation of serotonin signalling in the potato cyst nematode Globodera pallida reveals new targets for crop protection

Identification and characterisation of serotonin signalling in the potato cyst nematode Globodera pallida reveals new targets for crop protection
Identification and characterisation of serotonin signalling in the potato cyst nematode Globodera pallida reveals new targets for crop protection
Plant parasitic nematodes are microscopic pathogens that invade plant roots and cause extensive damage to crops. We have used a chemical biology approach to define mechanisms underpinning their parasitic behaviour: We discovered that reserpine, a plant alkaloid that inhibits the vesicular monoamine transporter (VMAT), potently impairs the ability of the potato cyst nematode Globodera pallida to enter the host plant root. We show this is due to an inhibition of serotonergic signalling that is essential for activation of the stylet which is used to access the host root. Prompted by this we identified core molecular components of G. pallida serotonin signalling encompassing the target of reserpine, VMAT; the synthetic enzyme for serotonin, tryptophan hydroxylase; the G protein coupled receptor SER-7 and the serotonin-gated chloride channel MOD-1. We cloned each of these molecular components and confirmed their functional identity by complementation of the corresponding C. elegans mutant thus mapping out serotonergic signalling in G. pallida. Complementary approaches testing the effect of chemical inhibitors of each of these signalling elements on discrete sub-behaviours required for parasitism and root invasion reinforce the critical role of serotonin. Thus, targeting the serotonin signalling pathway presents a promising new route to control plant parasitic nematodes.
1553-7366
1-27
Crisford, Anna
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Calahorro, Fernando
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Ludlow, Elizabeth
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Marvin, Jessica M. C.
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Hibbard, Jennifer K.
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Lilley, Catherine J.
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Kearn, James
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Keefe, Francesca
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Johnson, Peter
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Harmer, Rachael
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Urwin, Peter E.
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O’connor, Vincent
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Holden-dye, Lindy
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Dillman, Adler R.
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Crisford, Anna
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Calahorro, Fernando
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Ludlow, Elizabeth
630f2ba6-3922-4535-8808-508bf51c96b4
Marvin, Jessica M. C.
583ebc78-578f-4400-a909-25464a983ea2
Hibbard, Jennifer K.
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Lilley, Catherine J.
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Kearn, James
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Keefe, Francesca
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Johnson, Peter
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Harmer, Rachael
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Urwin, Peter E.
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O’connor, Vincent
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Holden-dye, Lindy
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Dillman, Adler R.
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Crisford, Anna, Calahorro, Fernando, Ludlow, Elizabeth, Marvin, Jessica M. C., Hibbard, Jennifer K., Lilley, Catherine J., Kearn, James, Keefe, Francesca, Johnson, Peter, Harmer, Rachael, Urwin, Peter E., O’connor, Vincent and Holden-dye, Lindy , Dillman, Adler R. (ed.) (2020) Identification and characterisation of serotonin signalling in the potato cyst nematode Globodera pallida reveals new targets for crop protection. PLoS Pathogens, 16 (10), 1-27, [e1008884]. (doi:10.1371/journal.ppat.1008884).

Record type: Article

Abstract

Plant parasitic nematodes are microscopic pathogens that invade plant roots and cause extensive damage to crops. We have used a chemical biology approach to define mechanisms underpinning their parasitic behaviour: We discovered that reserpine, a plant alkaloid that inhibits the vesicular monoamine transporter (VMAT), potently impairs the ability of the potato cyst nematode Globodera pallida to enter the host plant root. We show this is due to an inhibition of serotonergic signalling that is essential for activation of the stylet which is used to access the host root. Prompted by this we identified core molecular components of G. pallida serotonin signalling encompassing the target of reserpine, VMAT; the synthetic enzyme for serotonin, tryptophan hydroxylase; the G protein coupled receptor SER-7 and the serotonin-gated chloride channel MOD-1. We cloned each of these molecular components and confirmed their functional identity by complementation of the corresponding C. elegans mutant thus mapping out serotonergic signalling in G. pallida. Complementary approaches testing the effect of chemical inhibitors of each of these signalling elements on discrete sub-behaviours required for parasitism and root invasion reinforce the critical role of serotonin. Thus, targeting the serotonin signalling pathway presents a promising new route to control plant parasitic nematodes.

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Accepted/In Press date: 14 August 2020
e-pub ahead of print date: 2 October 2020

Identifiers

Local EPrints ID: 444493
URI: http://eprints.soton.ac.uk/id/eprint/444493
ISSN: 1553-7366
PURE UUID: 1d8ded1b-b9a4-4b6c-b1aa-2600370b6d10
ORCID for Lindy Holden-dye: ORCID iD orcid.org/0000-0002-9704-1217

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Date deposited: 21 Oct 2020 16:31
Last modified: 18 Feb 2021 16:34

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Contributors

Author: Anna Crisford
Author: Fernando Calahorro
Author: Elizabeth Ludlow
Author: Jessica M. C. Marvin
Author: Jennifer K. Hibbard
Author: Catherine J. Lilley
Author: James Kearn
Author: Francesca Keefe
Author: Peter Johnson
Author: Rachael Harmer
Author: Peter E. Urwin
Author: Vincent O’connor
Editor: Adler R. Dillman

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