A host beetle pheromone regulates development and behavior in the nematode Pristionchus pacificus.

Jessica K Cinkornpumin,Ralf J Sommer,Xiaoyue Wang,Ray L Hong,Christoph Dieterich,James L Go,Dona R Wisidagama,Veronika Rapoport

doi:10.7554/elife.03229

Abstract

Nematodes and insects are the two most speciose animal phyla and nematode-insect associations encompass widespread biological interactions. To dissect the chemical signals and the genes mediating this association, we investigated the effect of an oriental beetle sex pheromone on the development and behavior of the nematode Pristionchus pacificus. We found that while the beetle pheromone is attractive to P. pacificus adults, the pheromone arrests embryo development, paralyzes J2 larva, and inhibits exit of dauer larvae. To uncover the mechanism that regulates insect pheromone sensitivity, a newly identified mutant, Ppa-obi-1, is used to reveal the molecular links between altered attraction towards the beetle pheromone, as well as hypersensitivity to its paralyzing effects. Ppa-obi-1 encodes lipid-binding domains and reaches its highest expression in various cell types, including the amphid neuron sheath and excretory cells. Our data suggest that the beetle host pheromone may be a species-specific volatile synomone that co-evolved with necromeny.

Highlights

An understanding of ecological interactions and evolutionary history can be beneficial to the understanding of the cellular and developmental processes of an organism
P. pacificus populations found on the oriental beetle E. orientalis in Japan and northeastern United States are attracted to the sex pheromone of the beetle, z-7-tetradecen-2-one (ZTDO) (Zhang et al, 1994; Herrmann et al, 2007)
Odor avoidance in obi mutants towards 1-octanol, a repellant common between P. pacificus and C. elegans, resembles wild type. These results indicate that both obi mutants are defective in sensing a beetle pheromone rather than more generally defective in chemosensation

Summary

Introduction

An understanding of ecological interactions and evolutionary history can be beneficial to the understanding of the cellular and developmental processes of an organism. In Pristionchus pacificus, an emerging model organism for the study of development and behavior (Hong and Sommer, 2006b), a systematic effort to identify the natural ecology of Pristionchus nematodes revealed that P. pacificus host preferences include the oriental beetle (Exomala orientalis) found in Japan and northeastern United States (Herrmann et al, 2007). Unlike several fructivorous Caenorhabditis species, Pristionchus species are considered to be necromenic nematodes that have species-specific beetle host preferences and feed on the microorganisms that emerge from the beetle carcass (Herrmann et al, 2006a, 2006b; Brown et al, 2011). Biologists have been aware of such species-specific insect–nematode associations for some time, the genetic basis for such interactions remains largely unknown

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