Mechanosensation of rice root border cells activates serotonin-mediated pre-invasion behaviors in Meloidogyne graminicola via DEG/ENaC channels.

BACKGROUND: Plant-parasitic nematodes (PPNs) locate host roots primarily through chemosensation, yet the sensory events that convert root contact into the stylet thrusts required for host penetration remain obscure. Root border cells (RBCs), terminally differentiated cells shed from the root cap, constitute the first point of physical contact between the root and invading nematodes, but whether and how RBCs trigger pre-invasion behaviors is unknown.

RESULTS: Here we showed that rice (Oryza sativa) RBCs induce preparasitic second-stage juveniles (pre-J2) of the rice root-knot nematode Meloidogyne graminicola to exhibit stylet thrusting, feeding behaviors, and marked up‑regulation of the serotonin biosynthesis gene Mg‑tph‑1 in a density‑dependent manner. Among RBC components, the insoluble polysaccharide cellulose is the predominant inducer. We identified two Degenerin/Epithelial Sodium Channel (DEG/ENaC) mechanosensory genes, Mg‑del‑1 and Mg‑unc‑105, both highly expressed in infective J2. RNA interference targeting either gene reduced nematode motility and abolished RBC‑ or cellulose‑induced stylet thrusting and feeding. Furthermore, silencing Mg‑del‑1 or Mg‑unc‑105 downregulated the serotonergic pathway genes Mg‑unc‑43 and Mg‑tph‑1, and markedly reduced 5‑HT immunoreactivity in J2 responding to mechanical stimulation.

CONCLUSIONS: We propose that specific DEG/ENaC channels mediate the mechanosensing of RBCs or root cellulose by root‑knot nematodes, activating a downstream serotonergic circuit that drives stylet thrusting. This work uncovers a previously uncharacterized mechanosensory pathway in plant‑nematode interactions and identifies nematode DEG/ENaC channels as promising targets for disrupting parasitism, offering a new mechanosensory‑based strategy for nematode control.