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Peer-reviewedCC BYBMC plant biology

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

  • Xiping Long1
  • Wenxuan Xiao1
  • Xuqi Shi1
  • Shan Ye1,2
  • Deliang Peng3
  • Zhong Ding4,5
  • Zhuhong Yang6,7
7 affiliations
  1. 1College of Plant Protection, Hunan Agricultural University, Changsha, 410128, P.R. China.
  2. 2Hunan Provincial Engineering and Technology Research Center for Biopesticide and Formulation Processing, Changsha, 410128, P.R. China.
  3. 3State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, 100193, P.R. China.
  4. 4College of Plant Protection, Hunan Agricultural University, Changsha, 410128, P.R. China. [email protected].
  5. 5Hunan Provincial Engineering and Technology Research Center for Biopesticide and Formulation Processing, Changsha, 410128, P.R. China. [email protected].
  6. 6College of Plant Protection, Hunan Agricultural University, Changsha, 410128, P.R. China. [email protected].
  7. 7Hunan Provincial Engineering and Technology Research Center for Biopesticide and Formulation Processing, Changsha, 410128, P.R. China. [email protected].
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Abstract

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.

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Cite

BibTeXRIS
BibTeX
@article{long2026mechanosensation,
  title = {{Mechanosensation of rice root border cells activates serotonin-mediated pre-invasion behaviors in Meloidogyne graminicola via DEG/ENaC channels.}},
  author = {Xiping Long and Wenxuan Xiao and Xuqi Shi and Shan Ye and Deliang Peng and Zhong Ding and Zhuhong Yang},
  journal = {BMC plant biology},
  year = {2026},
  month = jul,
  doi = {10.1186/s12870-026-09616-1},
  url = {https://europepmc.org/article/MED/42902160},
  note = {CC BY},
}
RIS
TY  - JOUR
TI  - Mechanosensation of rice root border cells activates serotonin-mediated pre-invasion behaviors in Meloidogyne graminicola via DEG/ENaC channels.
AU  - Xiping Long
AU  - Wenxuan Xiao
AU  - Xuqi Shi
AU  - Shan Ye
AU  - Deliang Peng
AU  - Zhong Ding
AU  - Zhuhong Yang
PY  - 2026
DA  - 2026/07/01
JO  - BMC plant biology
DO  - 10.1186/s12870-026-09616-1
UR  - https://europepmc.org/article/MED/42902160
AB  - 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.
SN  - 1471-2229
ER  -