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

Anna Crisford, Fernando Calahorro, Elizabeth Ludlow, Jessica M.C. Marvin, Jennifer K. Hibbard, Catherine J. Lilley, James Kearn, Francesca Keefe, Rachael Harmer, Peter E. Urwin, Vincent O’Connor, Lindy Holden-Dye
doi: https://doi.org/10.1101/358358
Anna Crisford
1Biological Sciences, Highfield Campus, University of Southampton, Southampton SO17 1BJ, UK
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Fernando Calahorro
1Biological Sciences, Highfield Campus, University of Southampton, Southampton SO17 1BJ, UK
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Elizabeth Ludlow
1Biological Sciences, Highfield Campus, University of Southampton, Southampton SO17 1BJ, UK
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Jessica M.C. Marvin
2Centre for Plant Sciences, School of Biology, Faculty of Biological Sciences, University of Leeds, Leeds. LS2 9JT, UK
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Jennifer K. Hibbard
2Centre for Plant Sciences, School of Biology, Faculty of Biological Sciences, University of Leeds, Leeds. LS2 9JT, UK
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Catherine J. Lilley
2Centre for Plant Sciences, School of Biology, Faculty of Biological Sciences, University of Leeds, Leeds. LS2 9JT, UK
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James Kearn
1Biological Sciences, Highfield Campus, University of Southampton, Southampton SO17 1BJ, UK
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Francesca Keefe
1Biological Sciences, Highfield Campus, University of Southampton, Southampton SO17 1BJ, UK
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Rachael Harmer
1Biological Sciences, Highfield Campus, University of Southampton, Southampton SO17 1BJ, UK
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Peter E. Urwin
2Centre for Plant Sciences, School of Biology, Faculty of Biological Sciences, University of Leeds, Leeds. LS2 9JT, UK
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Vincent O’Connor
1Biological Sciences, Highfield Campus, University of Southampton, Southampton SO17 1BJ, UK
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Lindy Holden-Dye
1Biological Sciences, Highfield Campus, University of Southampton, Southampton SO17 1BJ, UK
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  • For correspondence: lmhd@soton.ac.uk
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Abstract

Plant parasitic nematodes are microscopic pests that invade plant roots and cause extensive damage to crops worldwide. To investigate mechanisms underpinning their parasitic behaviour we used a chemical biology approach: We discovered that reserpine, a plant alkaloid known for its antagonism of the mammalian vesicular monoamine transporter VMAT and ability to impart a global depletion of synaptic biogenic amines in the nervous system, potently impairs the ability of the potato cyst nematode Globodera pallida to enter the host plant root. We show that this effect of reserpine is mediated by an inhibition of serotonergic signalling that is essential for activation of the stylet, a lance-like organ that protrudes from the mouth of the worm and which is used to pierce the host root to gain access. 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 found that inhibitors of tryptophan hydroxylase, SER-7 and MOD-1 phenocopy the plant protecting action of reserpine. Thus targeting the serotonin signalling pathway presents a promising new route to control plant parasitic nematodes.

Summary Indian snakeroot, an herbal medicine prepared from the roots of the shrub Rauwolfia serpentina, has been used for centuries for its calming action. The major active constituent is reserpine which works by depleting a specific class of mood regulating chemical in the brain, the biogenic amines. We have discovered a remarkable effect of reserpine on a pest of global concern, the plant parasitic nematodes. These microscopic worms invade the roots of crops presenting a severe threat to food production. We show that reserpine disables serotonin signalling in the worm’s ‘brain’ that regulates the rhythmic thrusting of the stylet: a lance-like structure that protrudes from its mouth to pierce the plant root and which is essential to its parasitic lifecycle. Thus, reserpine joins nicotine as another intriguing example of Nature evolving its own protection against pests. We have identified key components of the serotonin signalling pathway in the potato cyst nematode Globodera pallida and show that chemicals that target these sites inhibit the ability of the nematode to invade its host plant. We conclude that biogenic amine transmitters are intimately involved in the worm’s parasitic behaviour and provide a new discrete route to crop protection.

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Posted June 29, 2018.
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Identification and characterisation of serotonin signalling in the potato cyst nematode Globodera pallida reveals new targets for crop protection
Anna Crisford, Fernando Calahorro, Elizabeth Ludlow, Jessica M.C. Marvin, Jennifer K. Hibbard, Catherine J. Lilley, James Kearn, Francesca Keefe, Rachael Harmer, Peter E. Urwin, Vincent O’Connor, Lindy Holden-Dye
bioRxiv 358358; doi: https://doi.org/10.1101/358358
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Identification and characterisation of serotonin signalling in the potato cyst nematode Globodera pallida reveals new targets for crop protection
Anna Crisford, Fernando Calahorro, Elizabeth Ludlow, Jessica M.C. Marvin, Jennifer K. Hibbard, Catherine J. Lilley, James Kearn, Francesca Keefe, Rachael Harmer, Peter E. Urwin, Vincent O’Connor, Lindy Holden-Dye
bioRxiv 358358; doi: https://doi.org/10.1101/358358

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