Disparate gain and loss of parasitic abilities among nematode lineages

Martijn Holterman, Akbar Karegar, Paul Mooijman, Hanny van Megen, Sven van den Elsen, M.T.W. Vervoort, Casper W. Quist, Gerrit Karssen, Wilfrida Decraemer, Charles H. Opperman, David M. Bird, Jan Kammenga, Aska Goverse, Geert Smant, Hans Helder*

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

11 Citations (Scopus)

Abstract

Plant parasitism has arisen time and again in multiple phyla, including bacteria, fungi, insects and nematodes. In most of these organismal groups, the overwhelming diversity hampers a robust reconstruction of the origins and diversification patterns of this trophic lifestyle. Being a moderately diversified phylum with ≈ 4,100 plant parasites (15% of total biodiversity) subdivided over four independent lineages, nematodes constitute a major organismal group for which the genesis of plant parasitism could be mapped. Since substantial crop losses worldwide have been attributed to less than 1% of these plant parasites, research efforts are severely biased towards this minority. With the first molecular characterisation of numerous basal and supposedly harmless plant parasites as well as their non-parasitic relatives, we were able to generate a comprehensive molecular framework that allows for the reconstruction of trophic diversification for a complete phylum. In each lineage plant parasites reside in a single taxonomic grouping (family or order), and by taking the coverage of the next lower taxonomic level as a measure for representation, 50, 67, 100 and 85% of the known diversity was included. We revealed distinct gain and loss patterns with regard to plant parasitism per se as well as host exploitation strategies between these lineages. Our map of parasitic nematode biodiversity also revealed an unanticipated time reversal in which the two most ancient lineages showed the lowest level of ecological diversification and vice versa.

Original languageEnglish
Article numbere0185445
Number of pages18
JournalPLoS ONE
Volume12
Issue number9
DOIs
Publication statusPublished - 2017

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Aptitude
Nematoda
Biodiversity
Parasites
parasites
parasitism
Fungi
Crops
Bacteria
biodiversity
crop losses
plant parasitic nematodes
lifestyle
Insects
Life Style
insects
fungi
bacteria
Research

Cite this

@article{4c9941d99cb445888b39f2289c0682a7,
title = "Disparate gain and loss of parasitic abilities among nematode lineages",
abstract = "Plant parasitism has arisen time and again in multiple phyla, including bacteria, fungi, insects and nematodes. In most of these organismal groups, the overwhelming diversity hampers a robust reconstruction of the origins and diversification patterns of this trophic lifestyle. Being a moderately diversified phylum with ≈ 4,100 plant parasites (15{\%} of total biodiversity) subdivided over four independent lineages, nematodes constitute a major organismal group for which the genesis of plant parasitism could be mapped. Since substantial crop losses worldwide have been attributed to less than 1{\%} of these plant parasites, research efforts are severely biased towards this minority. With the first molecular characterisation of numerous basal and supposedly harmless plant parasites as well as their non-parasitic relatives, we were able to generate a comprehensive molecular framework that allows for the reconstruction of trophic diversification for a complete phylum. In each lineage plant parasites reside in a single taxonomic grouping (family or order), and by taking the coverage of the next lower taxonomic level as a measure for representation, 50, 67, 100 and 85{\%} of the known diversity was included. We revealed distinct gain and loss patterns with regard to plant parasitism per se as well as host exploitation strategies between these lineages. Our map of parasitic nematode biodiversity also revealed an unanticipated time reversal in which the two most ancient lineages showed the lowest level of ecological diversification and vice versa.",
author = "Martijn Holterman and Akbar Karegar and Paul Mooijman and {van Megen}, Hanny and {van den Elsen}, Sven and M.T.W. Vervoort and Quist, {Casper W.} and Gerrit Karssen and Wilfrida Decraemer and Opperman, {Charles H.} and Bird, {David M.} and Jan Kammenga and Aska Goverse and Geert Smant and Hans Helder",
year = "2017",
doi = "10.1371/journal.pone.0185445",
language = "English",
volume = "12",
journal = "PLoS ONE",
issn = "1932-6203",
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Disparate gain and loss of parasitic abilities among nematode lineages. / Holterman, Martijn; Karegar, Akbar; Mooijman, Paul; van Megen, Hanny; van den Elsen, Sven; Vervoort, M.T.W.; Quist, Casper W.; Karssen, Gerrit; Decraemer, Wilfrida; Opperman, Charles H.; Bird, David M.; Kammenga, Jan; Goverse, Aska; Smant, Geert; Helder, Hans.

In: PLoS ONE, Vol. 12, No. 9, e0185445, 2017.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Disparate gain and loss of parasitic abilities among nematode lineages

AU - Holterman, Martijn

AU - Karegar, Akbar

AU - Mooijman, Paul

AU - van Megen, Hanny

AU - van den Elsen, Sven

AU - Vervoort, M.T.W.

AU - Quist, Casper W.

AU - Karssen, Gerrit

AU - Decraemer, Wilfrida

AU - Opperman, Charles H.

AU - Bird, David M.

AU - Kammenga, Jan

AU - Goverse, Aska

AU - Smant, Geert

AU - Helder, Hans

PY - 2017

Y1 - 2017

N2 - Plant parasitism has arisen time and again in multiple phyla, including bacteria, fungi, insects and nematodes. In most of these organismal groups, the overwhelming diversity hampers a robust reconstruction of the origins and diversification patterns of this trophic lifestyle. Being a moderately diversified phylum with ≈ 4,100 plant parasites (15% of total biodiversity) subdivided over four independent lineages, nematodes constitute a major organismal group for which the genesis of plant parasitism could be mapped. Since substantial crop losses worldwide have been attributed to less than 1% of these plant parasites, research efforts are severely biased towards this minority. With the first molecular characterisation of numerous basal and supposedly harmless plant parasites as well as their non-parasitic relatives, we were able to generate a comprehensive molecular framework that allows for the reconstruction of trophic diversification for a complete phylum. In each lineage plant parasites reside in a single taxonomic grouping (family or order), and by taking the coverage of the next lower taxonomic level as a measure for representation, 50, 67, 100 and 85% of the known diversity was included. We revealed distinct gain and loss patterns with regard to plant parasitism per se as well as host exploitation strategies between these lineages. Our map of parasitic nematode biodiversity also revealed an unanticipated time reversal in which the two most ancient lineages showed the lowest level of ecological diversification and vice versa.

AB - Plant parasitism has arisen time and again in multiple phyla, including bacteria, fungi, insects and nematodes. In most of these organismal groups, the overwhelming diversity hampers a robust reconstruction of the origins and diversification patterns of this trophic lifestyle. Being a moderately diversified phylum with ≈ 4,100 plant parasites (15% of total biodiversity) subdivided over four independent lineages, nematodes constitute a major organismal group for which the genesis of plant parasitism could be mapped. Since substantial crop losses worldwide have been attributed to less than 1% of these plant parasites, research efforts are severely biased towards this minority. With the first molecular characterisation of numerous basal and supposedly harmless plant parasites as well as their non-parasitic relatives, we were able to generate a comprehensive molecular framework that allows for the reconstruction of trophic diversification for a complete phylum. In each lineage plant parasites reside in a single taxonomic grouping (family or order), and by taking the coverage of the next lower taxonomic level as a measure for representation, 50, 67, 100 and 85% of the known diversity was included. We revealed distinct gain and loss patterns with regard to plant parasitism per se as well as host exploitation strategies between these lineages. Our map of parasitic nematode biodiversity also revealed an unanticipated time reversal in which the two most ancient lineages showed the lowest level of ecological diversification and vice versa.

U2 - 10.1371/journal.pone.0185445

DO - 10.1371/journal.pone.0185445

M3 - Article

VL - 12

JO - PLoS ONE

JF - PLoS ONE

SN - 1932-6203

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M1 - e0185445

ER -