The beet cyst nematode Heterodera schachtii modulates the expression of WRKY transcription factors in syncytia to favour its development in Arabidopsis roots.

Muhammad Amjad Ali,Holger Bohlmann,David P Kreil,Krzysztof Wieczorek

doi:10.1371/journal.pone.0102360

Abstract

Cyst nematodes invade the roots of their host plants as second stage juveniles and induce a syncytium which is the only source of nutrients throughout their life. A recent transcriptome analysis of syncytia induced by the beet cyst nematode Heterodera schachtii in Arabidopsis roots has shown that thousands of genes are up-regulated or down-regulated in syncytia as compared to root segments from uninfected plants. Among the down-regulated genes are many which code for WRKY transcription factors. Arabidopsis contains 66 WRKY genes with 59 represented by the ATH1 GeneChip. Of these, 28 were significantly down-regulated and 6 up-regulated in syncytia as compared to control root segments. We have studied here the down-regulated genes WRKY6, WRKY11, WRKY17 and WRKY33 in detail. We confirmed the down-regulation in syncytia with promoter::GUS lines. Using various overexpression lines and mutants it was shown that the down-regulation of these WRKY genes is important for nematode development, probably through interfering with plant defense reactions. In case of WRKY33, this might involve the production of the phytoalexin camalexin.

Highlights

Plant parasitic nematodes are obligate biotrophic parasites of a large number of plant species
Since WRKY33, WRKY6, WRKY11, and WRKY17 were among the most strongly down-regulated genes in syncytia [4] we have studied these genes in more detail
A comparison of 5 and 15 dpi syncytia uncovered only 2 genes that were significantly differently expressed; WRKY40 and WRKY54 (Figure S3). Both genes were up-regulated in older syncytia and WRKY54 was significantly up-regulated in syncytia compared to control root segments

Summary

Introduction

Plant parasitic nematodes are obligate biotrophic parasites of a large number of plant species. The sugar beet cyst nematode Heterodera schachtii can complete its life cycle on Arabidopsis plants in vitro within 6 weeks and this model system is widely used for studying plant nematode interactions at the molecular level [3]. By using this model system, we recently performed a transcriptome analysis of 5 and 15 dpi (days post inoculation) syncytia using Affymetrix GeneChip analysis with microaspirated syncytial material [4]. This study has revealed that 34.2% out of a total of 21,138 Arabidopsis genes were differentially expressed as compared to uninfected control root segments. This and other transcriptome studies conducted on different plant species have demonstrated high metabolic activity in the nematode feeding cells [4,5,6,7,8,9]

Methods

Results

Conclusion