Ascarosides coordinate the dispersal of a plant-parasitic nematode with the metamorphosis of its vector beetle.

Lilin Zhao,Satya Chinta,Yanan Wei,Yunpeng Liu,Zhen Zou,Peijun Qin,Jianghua Sun,Haiying Yu,Xiangbo Kong,Xinxing Zhang,Wei Zhang,Songnian Hu,Rebecca A Butcher,Jiao Zhou

doi:10.1038/ncomms12341

Abstract

Insect vectors are required for the transmission of many species of parasitic nematodes, but the mechanisms by which the vectors and nematodes coordinate their life cycles are poorly understood. Here, we report that ascarosides, an evolutionarily conserved family of nematode pheromones, are produced not only by a plant-parasitic nematode, but also by its vector beetle. The pinewood nematode and its vector beetle cause pine wilt disease, which threatens forest ecosystems world-wide. Ascarosides secreted by the dispersal third-stage nematode LIII larvae promote beetle pupation by inducing ecdysone production in the beetle and up-regulating ecdysone-dependent gene expression. Once the beetle develops into the adult stage, it secretes ascarosides that attract the dispersal fourth-stage nematode LIV larvae, potentially facilitating their movement into the beetle trachea for transport to the next pine tree. These results demonstrate that ascarosides play a key role in the survival and spread of pine wilt disease.

Highlights

Insect vectors are required for the transmission of many species of parasitic nematodes, but the mechanisms by which the vectors and nematodes coordinate their life cycles are poorly understood
In field observations over three seasons, we found that beetle larvae associated with pinewood nematode (PWN) tended to pupate and become adults earlier than those without the nematodes (Supplementary Table 1)
The presence of L2 into dispersal juveniles (LIII) larvae decreased the time required for the beetles to develop from larvae to adults by about 10 days (Supplementary Fig. 1b), similar to what was observed in the field (Supplementary Table 1)

Summary

Introduction

Insect vectors are required for the transmission of many species of parasitic nematodes, but the mechanisms by which the vectors and nematodes coordinate their life cycles are poorly understood. Once the beetle develops into the adult stage, it secretes ascarosides that attract the dispersal fourth-stage nematode LIV larvae, potentially facilitating their movement into the beetle trachea for transport to the pine tree. These results demonstrate that ascarosides play a key role in the survival and spread of pine wilt disease. Once the beetle larvae become late pupae or early adults, the LIII larvae are induced to develop into fourth-stage dispersal juveniles (LIV) These LIV enter the tracheal system of the beetle for transport to a new pine tree host[2,5]. Knowledge of these interspecific signals could potentially shed light on the driving forces behind the spread of PWN and inspire better approaches to preventing transmission

Methods

Results

Conclusion