Abstract

Bacteria, fungi, and nematodes in the rhizosphere have profound impacts on all aspects of plant biology, and small-molecule signaling is presumed to play a central role in mediating these interactions. We found that ascaroside pheromones secreted by plant-parasitic nematodes are metabolized by plants and associated microorganisms in a manner that can starkly alter the chemical message encoded by these pheromones. For example, comparative metabolomics of monocots and dicots revealed that nematode-derived ascarosides that are attractive to other nematodes are converted into derivatives that confer repellency. An Arabidopsis mutant defective in two peroxisomal acyl-CoA oxidases does not metabolize ascr#18 and does not repel nematodes, indicating that plants, like nematodes, employ conserved peroxisomal β-oxidation to edit ascarosides and change their message. These findings suggest that plant-editing of nematode pheromones may represent a broadly conserved defense mechanism that acts in parallel to conventional pattern-triggered immunity. Moreover, we found that, in addition to triggering defense responses, ascarosides can directly modulate plant growth and development. Fungi and some bacteria can also metabolize nematode-derived ascarosides, demonstrating that plants and microorganisms are part of a biosynthetic network that can actively modulate and interfere with chemical signaling across phyla.

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