STATAWAARS: a promoter motif associated with spatial expression in the major effector-producing tissues of the plant-parasitic nematode Bursaphelenchus xylophilus
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...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2018-07-01
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| Series: | BMC Genomics |
| Subjects: | |
| Online Access: | http://link.springer.com/article/10.1186/s12864-018-4908-2 |
| _version_ | 1811192892930129920 |
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| author | Margarida Espada Sebastian Eves-van den Akker Tom Maier Paramasivan Vijayapalani Thomas Baum Manuel Mota John T. Jones |
| author_facet | Margarida Espada Sebastian Eves-van den Akker Tom Maier Paramasivan Vijayapalani Thomas Baum Manuel Mota John T. Jones |
| author_sort | Margarida Espada |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-04-11T23:59:09Z |
| format | Article |
| id | doaj.art-6d11c5eaeb2d4813a274fba69b3aee07 |
| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-04-11T23:59:09Z |
| publishDate | 2018-07-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Genomics |
| spelling | doaj.art-6d11c5eaeb2d4813a274fba69b3aee072022-12-22T03:56:16ZengBMCBMC Genomics1471-21642018-07-0119111310.1186/s12864-018-4908-2STATAWAARS: a promoter motif associated with spatial expression in the major effector-producing tissues of the plant-parasitic nematode Bursaphelenchus xylophilusMargarida Espada0Sebastian Eves-van den Akker1Tom Maier2Paramasivan Vijayapalani3Thomas Baum4Manuel Mota5John T. Jones6NemaLab, ICAAM – Instituto de Ciências Agrárias e Ambientais Mediterrânicas, Universidade de Évora, Instituto de Investigação e Formação Avançada, Universidade de Évora, Pólo da Mitra, Ap. 94Department of Plant Sciences, University of CambridgeDepartment of Plant Pathology and Microbiology, Iowa State UniversityDepartment of Plant Pathology and Microbiology, Iowa State UniversityDepartment of Plant Pathology and Microbiology, Iowa State UniversityNemaLab, ICAAM - Departamento de Biologia, Instituto de Ciências Agrárias e Ambientais Mediterrânicas, Universidade de Évora, Escola de Ciências e Tecnologia, Universidade de Évora, Pólo da Mitra, Ap. 94Cell and Molecular Sciences Group, The James Hutton InstituteAbstract 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.http://link.springer.com/article/10.1186/s12864-018-4908-2Bursaphelenchus xylophilusEffectorsGene regulationPromoter motifPharyngeal gland cellsHost-pathogen interaction |
| spellingShingle | Margarida Espada Sebastian Eves-van den Akker Tom Maier Paramasivan Vijayapalani Thomas Baum Manuel Mota John T. Jones STATAWAARS: a promoter motif associated with spatial expression in the major effector-producing tissues of the plant-parasitic nematode Bursaphelenchus xylophilus BMC Genomics Bursaphelenchus xylophilus Effectors Gene regulation Promoter motif Pharyngeal gland cells Host-pathogen interaction |
| title | STATAWAARS: a promoter motif associated with spatial expression in the major effector-producing tissues of the plant-parasitic nematode Bursaphelenchus xylophilus |
| title_full | STATAWAARS: a promoter motif associated with spatial expression in the major effector-producing tissues of the plant-parasitic nematode Bursaphelenchus xylophilus |
| title_fullStr | STATAWAARS: a promoter motif associated with spatial expression in the major effector-producing tissues of the plant-parasitic nematode Bursaphelenchus xylophilus |
| title_full_unstemmed | STATAWAARS: a promoter motif associated with spatial expression in the major effector-producing tissues of the plant-parasitic nematode Bursaphelenchus xylophilus |
| title_short | STATAWAARS: a promoter motif associated with spatial expression in the major effector-producing tissues of the plant-parasitic nematode Bursaphelenchus xylophilus |
| title_sort | statawaars a promoter motif associated with spatial expression in the major effector producing tissues of the plant parasitic nematode bursaphelenchus xylophilus |
| topic | Bursaphelenchus xylophilus Effectors Gene regulation Promoter motif Pharyngeal gland cells Host-pathogen interaction |
| url | http://link.springer.com/article/10.1186/s12864-018-4908-2 |
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