The Transcriptome of Nacobbus aberrans Reveals Insights into the Evolution of Sedentary Endoparasitism in Plant-Parasitic Nematodes

Within the phylum Nematoda, plant-parasitism is hypothesized to have arisen independently on at least four occasions. The most economically damaging plant-parasitic nematode species, and consequently the most widely studied, are those that feed as they migrate destructively through host roots causin...

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Main Authors: Eves-van den Akker, Sebastian, Lilley, Catherine J., Danchin, Etienne G. J., Rancurel, Corinne, Cock, Peter J. A., Urwin, Peter E., Jones, John T.
Format: Online
Language:English
Published: Oxford University Press 2014
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4202313/
id pubmed-4202313
recordtype oai_dc
spelling pubmed-42023132014-10-21 The Transcriptome of Nacobbus aberrans Reveals Insights into the Evolution of Sedentary Endoparasitism in Plant-Parasitic Nematodes Eves-van den Akker, Sebastian Lilley, Catherine J. Danchin, Etienne G. J. Rancurel, Corinne Cock, Peter J. A. Urwin, Peter E. Jones, John T. Research Article Within the phylum Nematoda, plant-parasitism is hypothesized to have arisen independently on at least four occasions. The most economically damaging plant-parasitic nematode species, and consequently the most widely studied, are those that feed as they migrate destructively through host roots causing necrotic lesions (migratory endoparasites) and those that modify host root tissue to create a nutrient sink from which they feed (sedentary endoparasites). The false root-knot nematode Nacobbus aberrans is the only known species to have both migratory endoparasitic and sedentary endoparasitic stages within its life cycle. Moreover, its sedentary stage appears to have characteristics of both the root-knot and the cyst nematodes. We present the first large-scale genetic resource of any false-root knot nematode species. We use RNAseq to describe relative abundance changes in all expressed genes across the life cycle to provide interesting insights into the biology of this nematode as it transitions between modes of parasitism. A multigene phylogenetic analysis of N. aberrans with respect to plant-parasitic nematodes of all groups confirms its proximity to both cyst and root-knot nematodes. We present a transcriptome-wide analysis of both lateral gene transfer events and the effector complement. Comparing parasitism genes of typical root-knot and cyst nematodes to those of N. aberrans has revealed interesting similarities. Importantly, genes that were believed to be either cyst nematode, or root-knot nematode, “specific” have both been identified in N. aberrans. Our results provide insights into the characteristics of a common ancestor and the evolution of sedentary endoparasitism of plants by nematodes. Oxford University Press 2014-08-13 /pmc/articles/PMC4202313/ /pubmed/25123114 http://dx.doi.org/10.1093/gbe/evu171 Text en © The Author(s) 2014. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
repository_type Open Access Journal
institution_category Foreign Institution
institution US National Center for Biotechnology Information
building NCBI PubMed
collection Online Access
language English
format Online
author Eves-van den Akker, Sebastian
Lilley, Catherine J.
Danchin, Etienne G. J.
Rancurel, Corinne
Cock, Peter J. A.
Urwin, Peter E.
Jones, John T.
spellingShingle Eves-van den Akker, Sebastian
Lilley, Catherine J.
Danchin, Etienne G. J.
Rancurel, Corinne
Cock, Peter J. A.
Urwin, Peter E.
Jones, John T.
The Transcriptome of Nacobbus aberrans Reveals Insights into the Evolution of Sedentary Endoparasitism in Plant-Parasitic Nematodes
author_facet Eves-van den Akker, Sebastian
Lilley, Catherine J.
Danchin, Etienne G. J.
Rancurel, Corinne
Cock, Peter J. A.
Urwin, Peter E.
Jones, John T.
author_sort Eves-van den Akker, Sebastian
title The Transcriptome of Nacobbus aberrans Reveals Insights into the Evolution of Sedentary Endoparasitism in Plant-Parasitic Nematodes
title_short The Transcriptome of Nacobbus aberrans Reveals Insights into the Evolution of Sedentary Endoparasitism in Plant-Parasitic Nematodes
title_full The Transcriptome of Nacobbus aberrans Reveals Insights into the Evolution of Sedentary Endoparasitism in Plant-Parasitic Nematodes
title_fullStr The Transcriptome of Nacobbus aberrans Reveals Insights into the Evolution of Sedentary Endoparasitism in Plant-Parasitic Nematodes
title_full_unstemmed The Transcriptome of Nacobbus aberrans Reveals Insights into the Evolution of Sedentary Endoparasitism in Plant-Parasitic Nematodes
title_sort transcriptome of nacobbus aberrans reveals insights into the evolution of sedentary endoparasitism in plant-parasitic nematodes
description Within the phylum Nematoda, plant-parasitism is hypothesized to have arisen independently on at least four occasions. The most economically damaging plant-parasitic nematode species, and consequently the most widely studied, are those that feed as they migrate destructively through host roots causing necrotic lesions (migratory endoparasites) and those that modify host root tissue to create a nutrient sink from which they feed (sedentary endoparasites). The false root-knot nematode Nacobbus aberrans is the only known species to have both migratory endoparasitic and sedentary endoparasitic stages within its life cycle. Moreover, its sedentary stage appears to have characteristics of both the root-knot and the cyst nematodes. We present the first large-scale genetic resource of any false-root knot nematode species. We use RNAseq to describe relative abundance changes in all expressed genes across the life cycle to provide interesting insights into the biology of this nematode as it transitions between modes of parasitism. A multigene phylogenetic analysis of N. aberrans with respect to plant-parasitic nematodes of all groups confirms its proximity to both cyst and root-knot nematodes. We present a transcriptome-wide analysis of both lateral gene transfer events and the effector complement. Comparing parasitism genes of typical root-knot and cyst nematodes to those of N. aberrans has revealed interesting similarities. Importantly, genes that were believed to be either cyst nematode, or root-knot nematode, “specific” have both been identified in N. aberrans. Our results provide insights into the characteristics of a common ancestor and the evolution of sedentary endoparasitism of plants by nematodes.
publisher Oxford University Press
publishDate 2014
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4202313/
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