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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...

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Autores principales: 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, Holden-Dye, Lindy
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7556481/
https://www.ncbi.nlm.nih.gov/pubmed/33007049
http://dx.doi.org/10.1371/journal.ppat.1008884
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author 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
Holden-Dye, Lindy
author_facet 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
Holden-Dye, Lindy
author_sort Crisford, Anna
collection PubMed
description 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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spelling pubmed-75564812020-10-21 Identification and characterisation of serotonin signalling in the potato cyst nematode Globodera pallida reveals new targets for crop protection 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 Holden-Dye, Lindy PLoS Pathog Research Article 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. Public Library of Science 2020-10-02 /pmc/articles/PMC7556481/ /pubmed/33007049 http://dx.doi.org/10.1371/journal.ppat.1008884 Text en © 2020 Crisford et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
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
Holden-Dye, Lindy
Identification and characterisation of serotonin signalling in the potato cyst nematode Globodera pallida reveals new targets for crop protection
title Identification and characterisation of serotonin signalling in the potato cyst nematode Globodera pallida reveals new targets for crop protection
title_full Identification and characterisation of serotonin signalling in the potato cyst nematode Globodera pallida reveals new targets for crop protection
title_fullStr Identification and characterisation of serotonin signalling in the potato cyst nematode Globodera pallida reveals new targets for crop protection
title_full_unstemmed Identification and characterisation of serotonin signalling in the potato cyst nematode Globodera pallida reveals new targets for crop protection
title_short Identification and characterisation of serotonin signalling in the potato cyst nematode Globodera pallida reveals new targets for crop protection
title_sort identification and characterisation of serotonin signalling in the potato cyst nematode globodera pallida reveals new targets for crop protection
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7556481/
https://www.ncbi.nlm.nih.gov/pubmed/33007049
http://dx.doi.org/10.1371/journal.ppat.1008884
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