Plant metabolism of nematode pheromones mediates plant-nematode interactions

Authors: MANOHAR, MURLI - Boyce Thompson Institute; TENJO-CASTANO, FRANCISCO - Boyce Thompson Institute; CHEN, SHIYAN - Cornell University; ZHANG, YING - Boyce Thompson Institute; KUMARI, ANSHU - Boyce Thompson Institute; WILLIAMSON, VALERIE - University Of California, Davis; Wang, Xiaohong; KLESSIG, DANIEL - Boyce Thompson Institute; SHROEDER, FRANK - Boyce Thompson Institute

Submitted to: Nature Communications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/13/2019
Publication Date: 1/10/2020
Citation: Manohar, M., Tenjo-Castano, F., Chen, S., Zhang, Y.K., Kuman, A., Williamson, V.M., Wang, X., Klessig, D.F., Shroeder, F.C. 2020. Plant metabolism of nematode pheromones mediates plant-nematode interactions. Nature Communications. 11(208). https://doi.org/10.1038/s41467-019-14104-2.
DOI: https://doi.org/10.1038/s41467-019-14104-2

Interpretive Summary: Plant-parasitic nematodes are devastating pests, which significantly affect global crop production. These nematodes produce a conserved family of pheromones, of which ascr#18 was previously identified as the major molecule that can activate plant defenses against a range of plant pathogens. However, the underlying mechanism of ascr#18-trigerred plant defense is largely unknown. In this study, analytical analyses revealed that ascr#18 was converted into derivative molecules in plants, and subsequently secreted into the root rhizosphere. Ascr#18-mediated defense was not effective against nematode infection on the Arabidopsis mutant acx1acx5, which is defective in ascr#18 metabolism. Furthermore, results of in vitro avoidance assay suggest that ascr#18 and its derived forms processed by plants may function as a repellent against nematode migration towards plant roots. This study indicates that plants have evolved a unique ability to utilize nematode-derived signals to resist nematode infection. This knowledge may have implications for developing novel strategies to control plant-parasitic nematodes.

Technical Abstract: Plant-parasitic nematodes profoundly impact global crop production. Chemical signaling is presumed to play a central role in modulating plant-nematode interactions. However, the nature of the signals and underlying mechanisms are poorly understood. Here we show that the ascaroside ascr#18, a small signaling molecule secreted by plant-parasitic nematodes, is metabolized by plants to generate chemical signals that act as repellents against parasitic nematodes and hence reduce infection. High-resolution mass spectral analyses revealed that ascr#18 is converted into shorter side-chained ascarosides, including several new compounds. Studies with Arabidopsis mutant acx1acx5 demonstrated that plants use peroxisomal ß-oxidation (pßo) to metabolize ascr#18. Pßo is a highly conserved pathway involved in a variety of metabolic functions. These data highlight an evolutionarily conserved chemotropic mechanism that regulates pre-invasion phase of plant-nematode interactions, identifies a novel function of pßo in metabolizing foreign signaling molecules, and may have implications for development of novel strategies to control nematode infestation.