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. 2016 Feb;17(2):286-95.
doi: 10.1111/mpp.12280. Epub 2015 Jun 16.

Identification and characterization of parasitism genes from the pinewood nematode Bursaphelenchus xylophilus reveals a multilayered detoxification strategy

Margarida Espada  1   2 , Ana Cláudia Silva  1   2   3 , Sebastian Eves van den Akker  4 , Peter J A Cock  2 , Manuel Mota  1 , John T Jones  2   3   5
Affiliations

Identification and characterization of parasitism genes from the pinewood nematode Bursaphelenchus xylophilus reveals a multilayered detoxification strategy

Margarida Espada et al. Mol Plant Pathol. 2016 Feb.

Abstract

The migratory endoparasitic nematode Bursaphelenchus xylophilus, which is the causal agent of pine wilt disease, has phytophagous and mycetophagous phases during its life cycle. This highly unusual feature distinguishes it from other plant-parasitic nematodes and requires profound changes in biology between modes. During the phytophagous stage, the nematode migrates within pine trees, feeding on the contents of parenchymal cells. Like other plant pathogens, B. xylophilus secretes effectors from pharyngeal gland cells into the host during infection. We provide the first description of changes in the morphology of these gland cells between juvenile and adult life stages. Using a comparative transcriptomics approach and an effector identification pipeline, we identify numerous novel parasitism genes which may be important for the mediation of interactions of B. xylophilus with its host. In-depth characterization of all parasitism genes using in situ hybridization reveals two major categories of detoxification proteins, those specifically expressed in either the pharyngeal gland cells or the digestive system. These data suggest that B. xylophilus incorporates effectors in a multilayer detoxification strategy in order to protect itself from host defence responses during phytophagy.

Keywords: Bursaphelenchus xylophilus; effectors; gland cells; transcriptome; xenobiotic metabolism.

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Figures

Figure 1
Figure 1
Positions of pharyngeal gland cells in adult (A) and juvenile (B) Bursaphelenchus xylophilus. DG, dorsal glands; M, median bulb; S, stylet; SVG, subventral glands. Subventral glands (white) and dorsal gland (orange) are outlined in the insets. Scale bar, 20 μm.
Figure 2
Figure 2
Bioinformatics pipeline for the identification of candidate effectors from Bursaphelenchus xylophilus. DE, differentially expressed; dpi, days post‐infection; FF, fungal feeder.
Figure 3
Figure 3
Localization of the candidate proteases and detoxification enzymes encoding gene expression in the intestine by in situ hybridization, with the exception of putative epoxide hydrolase (BUX.s00298.34) (a) which was expressed in the glandular tissues surrounding the anterior sense organs. (b) Putative multicopper oxidase (BUX.s01281.17). (c) Putative flavin monooxygenase (BUX.s01337.7). (d) Putative peptidase C46 (BUX.s01109.245). (e) Putative UDP‐glucuronosyl transferase (UGT) (BUX.s00422.680). (f) Putative CYP33 C‐related (BUX.s01144.121). (g) Putative peptidase M13 (BUX.s01661.67). (h) Putative peptidase A1 (BUX.s00532.10). (i) Putative peptidase S28 (BUX.s01144.130).
Figure 4
Figure 4
Localization of candidate effector expression in the pharyngeal gland cells by in situ hybridization. (a) BUX.s00422.201. (b) BUX.s00083.48. (c) BUX.s00116.698. (d) BUX.s01109.178. (e) BUX.s01066.2. (f) BUX.s00116.606. (g) BUX.s01254.333. (h) BUX.s01144.122. (i) BUX.s00647.112. (j) BUX.s01147.177. k and l are control forward probe. G, dorsal gland cell; M, median bulb; SVG, subventral glands.
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