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STATAWAARS : a promoter motif associated with spatial expression in the major effector-producing tissues of the plant-parasitic nematode Bursaphelenchus xylophilus

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Date
27/07/2018
Author
Espada, Margarida
Eves-van den Akker, Sebastian
Maier, Tom
Vijayapalani, Paramasivan
Baum, Thomas
Mota, Manuel
Jones, John T.
Keywords
Bursaphelenchus xylophilus
Effectors
Gene regulation
Promoter motif
Pharyngeal gland cells
Host-pathogen interaction
Plant-parasitic nematode
QH301 Biology
DAS
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Abstract
Background:  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. 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. Results:  Using 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. Conclusions:  We 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.
Citation
Espada , M , Eves-van den Akker , S , Maier , T , Vijayapalani , P , Baum , T , Mota , M & Jones , J T 2018 , ' STATAWAARS : a promoter motif associated with spatial expression in the major effector-producing tissues of the plant-parasitic nematode Bursaphelenchus xylophilus ' , BMC Genomics , vol. 19 , 553 . https://doi.org/10.1186/s12864-018-4908-2
Publication
BMC Genomics
Status
Peer reviewed
DOI
https://doi.org/10.1186/s12864-018-4908-2
ISSN
1471-2164
Type
Journal article
Rights
© The Author(s). 2018. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Description
This work was funded by National Funds through FCT – Foundation for Science and Technology under the Project UID/AGR/00115/2013. ME was funded by FCT under the PhD grant (SFRH/BD/84541/2012). The James Hutton Institute receives funding from the Rural and Environment Science and Analytical Services Division of the Scottish Government. This work was also supported by Hatch Act and State of Iowa funds. SE-vdA is supported by BBSRC grant BB/M014207/1 and BB/R011311/1.
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URI
http://hdl.handle.net/10023/15716

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