Identification and characterisation of serotonin signalling in the potato cyst nematodeGlobodera pallidareveals new targets for crop protection

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.

Elicitation of Differential Responses in the Root-Knot Nematode Meloidogyne incognita to Tomato Root Exudate Cytokinin, Flavonoids, and Alkaloids

“…23 For example, serotonin a known activator of stylet thrusting elicited a concentrationand time-dependent stylet thrusting, which reached a plateau at a high concentration. 23,24 Similarly, in the chemotaxis assays, attractiveness of J2s to the root exudate was concentrationdependent and significantly higher (77.2%; χ 2 = 26.1; df = 1; and p < 0.001) than the negative control. For instance, at 10 μg/g of sand, the attractiveness of the root exudate compared favorably to the positive control, MeSA, at 20 ng/g of sand (73.4%; χ 2 = 21.94; df = 1; and p < 0.001) (Figure 3B).…”

The nematode serotonin-gated chloride channel MOD-1: A novel target for anthelmintic therapy

“…A search of transcriptome data for the filarial nematode parasite Loa loa, Brugia malayi, and Wucheria bancrofti revealed predicted coding sequences for orthologs of mod-1 gene (17). MOD-1 is also present in plant parasitic nematodes, in which serotonergic signaling is important for plant invasion (18).…”

Serotonergic modulation of feeding behavior in Caenorhabditis elegans and other related nematodes

“…Serotonin also functions in the feeding behavior of plant pathogenic nematodes with a stylet to penetrate host plant roots. Reserpine, an antagonist of the vesicular monoamine transporter, inhibits movement of the stylet on the pharynx in potato cyst nematodes, Globodera pallida (Crisford et al, 2018). Taken together, serotonin is involved in the regulation of feeding behavior in a wide range of nematodes, even though these nematodes have different mouth structures and feeding habits from those of C. elegans.…”

“…Further studies on this system may contribute to studies on neuromodulation in higher animals, offering insights into the neural modulatory circuit mediating environmental input from sensory neurons and outputs to muscle movements. (Rivard et al, 2010) and (Van Megen et al, 2009), and serotonergic neurons are based on (Chiang et al, 2006;Crisford et al, 2018;Johnson et al, 1996;Rao et al, 2011;Rivard et al, 2010;Weeks et al, 2016;Wilecki et al, 2015) Fig. 5.…”

“…To adapt to diverse habitats and food sources, such as bacteria, other nematodes, and fungi, free-living and parasitic nematodes have evolved diverse feeding structures. Even though the mouth forms and feeding styles are different, serotonin is involved in regulation of feeding behaviors in a wide range of nematode species, suggesting the significance of serotonin in the evolution of feeding behaviors in the phylum, Nematoda (Crisford et al, 2018;Komuniecki et al, 2004;Okumura et al, 2017;Weeks et al, 2016;Wilecki et al, 2015).…”