Abstract
BackgroundPlant-parasitic nematodes cause severe damage to a wide range of crop and forest species worldwide. The migratory endoparasitic nematode, Bursaphelenchus xylophilus, (pinewood nematode) is a quarantine pathogen that infects pine trees and has a hugely detrimental economic impact on the forestry industry. Under certain environmental conditions large areas of infected trees can be destroyed, leading to damage on an ecological scale. The interactions of B. xylophilus with plants are mediated by secreted effector proteins produced in the pharyngeal gland cells. Identification of effectors is important to understand mechanisms of parasitism and to develop new control measures for the pathogens.ResultsUsing an approach pioneered in cyst nematodes, we have analysed the promoter regions of a small panel of previously validated pharyngeal gland cell effectors from B. xylophilus to identify an associated putative regulatory promoter motif: STATAWAARS. The presence of STATAWAARS in the promoter region of an uncharacterized gene is a predictor that the corresponding gene encodes a putatively secreted protein, consistent with effector function. Furthermore, we are able to experimentally validate that a subset of STATAWAARS-containing genes are specifically expressed in the pharyngeal glands. Finally, we independently validate the association of STATAWAARS with tissue-specific expression by directly sequencing the mRNA of pharyngeal gland cells. We combine a series of criteria, including STATAWAARS predictions and abundance in the gland cell transcriptome, to generate a comprehensive effector repertoire for B. xylophilus. The genes highlighted by this approach include many previously described effectors and a series of novel “pioneer” effectors.ConclusionsWe provide a major scientific advance in the area of effector regulation. We identify a novel promoter motif (STATAWAARS) associated with expression in the pharyngeal gland cells. Our data, coupled with those from previous studies, suggest that lineage-specific promoter motifs are a theme of effector regulation in the phylum Nematoda.
Highlights
Plant-parasitic nematodes cause severe damage to a wide range of crop and forest species worldwide
Identification of a promoter motif associated with pharyngeal gland cell expression Recent analysis of the genome sequence of G. rostochiensis allowed identification of a non-coding promoter motif associated with genes expressed in the dorsal pharyngeal gland cell [14] which has subsequently been used as a tool to predict effectors in this genus
Employing a differential motif discovery algorithm, we identified a promoter motif that was highly enriched in the effector set (Fisher’s exact test; p-value: 1e-18)
Summary
Plant-parasitic nematodes cause severe damage to a wide range of crop and forest species worldwide. The migratory endoparasitic nematode, Bursaphelenchus xylophilus, (pinewood nematode) is a quarantine pathogen that infects pine trees and has a hugely detrimental economic impact on the forestry industry. Plant-parasitic nematodes (PPN) infect a broad range of plants of agricultural and economic importance. They display a wide range of interactions with their hosts and many are biotrophic pathogens. The pinewood nematode, Bursaphelenchus xylophilus, is a migratory endoparasitic nematode that causes extensive damage to forestry across many parts of the world. The beetle may migrate to another tree colonized by fungi or may feed on living trees In the latter case the nematode leaves the beetle and infects the host tree, feeding on parenchymal and epithelial cells. Most notably in hot climates, death of infected trees can occur within weeks of infection [1, 3]
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