Rather than by direct acquisition via lateral gene transfer, GHF5 cellulases were passed on from early Pratylenchidae to root-knot and cyst nematodes

<p>Abstract</p> <p>Background</p> <p>Plant parasitic nematodes are unusual Metazoans as they are equipped with genes that allow for symbiont-independent degradation of plant cell walls. Among the cell wall-degrading enzymes, glycoside hydrolase family 5 (GHF5) cellulase...

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Main Authors: Rybarczyk-Mydłowska Katarzyna, Maboreke Hazel Ruvimbo, van Megen Hanny, van den Elsen Sven, Mooyman Paul, Smant Geert, Bakker Jaap, Helder Johannes
Format: Article
Language:English
Published: BMC 2012-11-01
Series:BMC Evolutionary Biology
Subjects:
Online Access:http://www.biomedcentral.com/1471-2148/12/221
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spelling doaj-5dabeefc0ea24b6f9701d21a83381dd92021-09-02T01:11:32ZengBMCBMC Evolutionary Biology1471-21482012-11-0112122110.1186/1471-2148-12-221Rather than by direct acquisition via lateral gene transfer, GHF5 cellulases were passed on from early Pratylenchidae to root-knot and cyst nematodesRybarczyk-Mydłowska KatarzynaMaboreke Hazel Ruvimbovan Megen Hannyvan den Elsen SvenMooyman PaulSmant GeertBakker JaapHelder Johannes<p>Abstract</p> <p>Background</p> <p>Plant parasitic nematodes are unusual Metazoans as they are equipped with genes that allow for symbiont-independent degradation of plant cell walls. Among the cell wall-degrading enzymes, glycoside hydrolase family 5 (GHF5) cellulases are relatively well characterized, especially for high impact parasites such as root-knot and cyst nematodes<it>.</it> Interestingly, ancestors of extant nematodes most likely acquired these GHF5 cellulases from a prokaryote donor by one or multiple lateral gene transfer events. To obtain insight into the origin of GHF5 cellulases among evolutionary advanced members of the order Tylenchida, cellulase biodiversity data from less distal family members were collected and analyzed.</p> <p>Results</p> <p>Single nematodes were used to obtain (partial) genomic sequences of cellulases from representatives of the genera <it>Meloidogyne, Pratylenchus, Hirschmanniella</it> and <it>Globodera.</it> Combined Bayesian analysis of ≈ 100 cellulase sequences revealed three types of catalytic domains (A, B, and C). Represented by 84 sequences, type B is numerically dominant, and the overall topology of the catalytic domain type shows remarkable resemblance with trees based on neutral (= pathogenicity-unrelated) small subunit ribosomal DNA sequences. Bayesian analysis further suggested a sister relationship between the lesion nematode <it>Pratylenchus thornei</it> and all type B cellulases from root-knot nematodes. Yet, the relationship between the three catalytic domain types remained unclear. Superposition of intron data onto the cellulase tree suggests that types B and C are related, and together distinct from type A that is characterized by two unique introns.</p> <p>Conclusions</p> <p>All Tylenchida members investigated here harbored one or multiple GHF5 cellulases. Three types of catalytic domains are distinguished, and the presence of at least two types is relatively common among plant parasitic Tylenchida. Analysis of coding sequences of cellulases suggests that root-knot and cyst nematodes did not acquire this gene directly by lateral genes transfer. More likely, these genes were passed on by ancestors of a family nowadays known as the Pratylenchidae.</p> http://www.biomedcentral.com/1471-2148/12/221Lateral gene transferCellulaseNematodesPlant parasitism
collection DOAJ
language English
format Article
sources DOAJ
author Rybarczyk-Mydłowska Katarzyna
Maboreke Hazel Ruvimbo
van Megen Hanny
van den Elsen Sven
Mooyman Paul
Smant Geert
Bakker Jaap
Helder Johannes
spellingShingle Rybarczyk-Mydłowska Katarzyna
Maboreke Hazel Ruvimbo
van Megen Hanny
van den Elsen Sven
Mooyman Paul
Smant Geert
Bakker Jaap
Helder Johannes
Rather than by direct acquisition via lateral gene transfer, GHF5 cellulases were passed on from early Pratylenchidae to root-knot and cyst nematodes
BMC Evolutionary Biology
Lateral gene transfer
Cellulase
Nematodes
Plant parasitism
author_facet Rybarczyk-Mydłowska Katarzyna
Maboreke Hazel Ruvimbo
van Megen Hanny
van den Elsen Sven
Mooyman Paul
Smant Geert
Bakker Jaap
Helder Johannes
author_sort Rybarczyk-Mydłowska Katarzyna
title Rather than by direct acquisition via lateral gene transfer, GHF5 cellulases were passed on from early Pratylenchidae to root-knot and cyst nematodes
title_short Rather than by direct acquisition via lateral gene transfer, GHF5 cellulases were passed on from early Pratylenchidae to root-knot and cyst nematodes
title_full Rather than by direct acquisition via lateral gene transfer, GHF5 cellulases were passed on from early Pratylenchidae to root-knot and cyst nematodes
title_fullStr Rather than by direct acquisition via lateral gene transfer, GHF5 cellulases were passed on from early Pratylenchidae to root-knot and cyst nematodes
title_full_unstemmed Rather than by direct acquisition via lateral gene transfer, GHF5 cellulases were passed on from early Pratylenchidae to root-knot and cyst nematodes
title_sort rather than by direct acquisition via lateral gene transfer, ghf5 cellulases were passed on from early pratylenchidae to root-knot and cyst nematodes
publisher BMC
series BMC Evolutionary Biology
issn 1471-2148
publishDate 2012-11-01
description <p>Abstract</p> <p>Background</p> <p>Plant parasitic nematodes are unusual Metazoans as they are equipped with genes that allow for symbiont-independent degradation of plant cell walls. Among the cell wall-degrading enzymes, glycoside hydrolase family 5 (GHF5) cellulases are relatively well characterized, especially for high impact parasites such as root-knot and cyst nematodes<it>.</it> Interestingly, ancestors of extant nematodes most likely acquired these GHF5 cellulases from a prokaryote donor by one or multiple lateral gene transfer events. To obtain insight into the origin of GHF5 cellulases among evolutionary advanced members of the order Tylenchida, cellulase biodiversity data from less distal family members were collected and analyzed.</p> <p>Results</p> <p>Single nematodes were used to obtain (partial) genomic sequences of cellulases from representatives of the genera <it>Meloidogyne, Pratylenchus, Hirschmanniella</it> and <it>Globodera.</it> Combined Bayesian analysis of ≈ 100 cellulase sequences revealed three types of catalytic domains (A, B, and C). Represented by 84 sequences, type B is numerically dominant, and the overall topology of the catalytic domain type shows remarkable resemblance with trees based on neutral (= pathogenicity-unrelated) small subunit ribosomal DNA sequences. Bayesian analysis further suggested a sister relationship between the lesion nematode <it>Pratylenchus thornei</it> and all type B cellulases from root-knot nematodes. Yet, the relationship between the three catalytic domain types remained unclear. Superposition of intron data onto the cellulase tree suggests that types B and C are related, and together distinct from type A that is characterized by two unique introns.</p> <p>Conclusions</p> <p>All Tylenchida members investigated here harbored one or multiple GHF5 cellulases. Three types of catalytic domains are distinguished, and the presence of at least two types is relatively common among plant parasitic Tylenchida. Analysis of coding sequences of cellulases suggests that root-knot and cyst nematodes did not acquire this gene directly by lateral genes transfer. More likely, these genes were passed on by ancestors of a family nowadays known as the Pratylenchidae.</p>
topic Lateral gene transfer
Cellulase
Nematodes
Plant parasitism
url http://www.biomedcentral.com/1471-2148/12/221
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