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Evidence for a dispersed Hox gene cluster in the platyhelminth parasite Schistosoma mansoni

Evidence for a dispersed Hox gene cluster in the platyhelminth parasite Schistosoma mansoni
Evidence for a dispersed Hox gene cluster in the platyhelminth parasite Schistosoma mansoni
In most bilaterian organisms so far studied, Hox genes are organized in genomic clusters and determine development along the anteroposterior axis. It has been suggested that this clustering, together with spatial and temporal colinearity of gene expression, represents the ancestral condition. However, in organisms with derived modes of embryogenesis and lineage-dependent mechanisms for the determination of cell fate, temporal colinearity of expression can be lost and Hox cluster organization disrupted, as is the case for the ecdysozoans Drosophila melanogaster and Caenorhabditis elegans and the urochordates Ciona intestinalis and Oikopleura dioica. We sought to determine whether a lophotrochozoan, the platyhelminth parasite Schistosoma mansoni, possesses a conserved or disrupted Hox cluster. Using a polymerase chain reaction (PCR)-based strategy, we have cloned and characterized three novel S. mansoni genes encoding orthologues of Drosophila labial (SmHox1), deformed (SmHox4), and abdominal A (SmHox8), as well as the full-length coding sequence of the previously described Smox1, which we identify as an orthologue of fushi tarazu. Quantitative reverse transcriptase-PCR showed that the four genes were expressed at all life-cycle stages but that levels of expression were differentially regulated. Phylogenetic analysis and the conservation of "parapeptide" sequences C-terminal to the homeodomains of SmHox8 and Smox1 support the grouping of platyhelminths within the lophotrochozoan clade. However, Bacterial Artificial Chromosome (BAC) library screening followed by genome walking failed to reconstitute a cluster. The BAC clones containing Hox genes were sequenced, and in no case were other Hox genes found on the same clone. Moreover, the SmHox4 and SmHox8 genes contained single very large introns (>40 kbp) further indicating that the schistosome Hox cluster is highly extended. Localization of the Hox genes to chromosomes using fluorescence in situ hybridization showed that SmHox4 and SmHox8 are on the long arm of chromosome 4, whereas SmHox1 and Smox1 are on chromosome 3. In silico screening of the available genome sequences corroborated results of Southern blotting and BAC library screening that indicate that there are no paralogues of SmHox1, SmHox4, or SmHox8. The schistosome Hox cluster is therefore not duplicated, but is both dispersed and disintegrated in the genome.
Amino Acid Sequence, Animals, Chromosome Mapping, Chromosome Walking, Chromosomes, Artificial, Bacterial, Gene Expression, Gene Expression Regulation, Developmental, Genes, Helminth, Genes, Homeobox, Homeodomain Proteins/chemistry, Larva, Life Cycle Stages, Molecular Sequence Data, Phylogeny, Reverse Transcriptase Polymerase Chain Reaction, Schistosoma mansoni/genetics, Sequence Analysis, Protein
0737-4038
2491-2503
Pierce, Raymond J
6fa8266a-5803-43c3-af4b-8d241c4ee84c
Wu, Wenjie
700ff098-ef67-41cb-8f36-f6d00d445110
Hirai, Hirohisa
696fe726-fd3c-4914-badc-c1eaa2876850
Ivens, Al
f6b6c828-bd07-412f-9c07-f076a2f6ebd1
Murphy, Lee D
f0961bb5-948d-4e7e-9d7f-2889d80cd91d
Noël, Christophe
26cd9c91-a3df-46d0-9f03-fe7940589739
Johnston, David A
b41163c9-b9d2-425c-af99-2a357204014e
Artiguenave, François
5bfb0a7f-b645-421e-af3a-d7d3f05dbaac
Adams, Martin
e87c9595-d6c8-420d-a9b3-a44508cfad5f
Cornette, Jocelyne
d9cd0c87-5d45-4cdc-925e-993602351c36
Viscogliosi, Eric
714cce9a-44d5-43be-b252-dfe97d00ca2d
Capron, Monique
6d02d62d-a06a-4dba-91cf-9ffd7136cd26
Balavoine, Guillaume
9e15ed97-16fd-4eb3-9fdc-f250954388ce
Pierce, Raymond J
6fa8266a-5803-43c3-af4b-8d241c4ee84c
Wu, Wenjie
700ff098-ef67-41cb-8f36-f6d00d445110
Hirai, Hirohisa
696fe726-fd3c-4914-badc-c1eaa2876850
Ivens, Al
f6b6c828-bd07-412f-9c07-f076a2f6ebd1
Murphy, Lee D
f0961bb5-948d-4e7e-9d7f-2889d80cd91d
Noël, Christophe
26cd9c91-a3df-46d0-9f03-fe7940589739
Johnston, David A
b41163c9-b9d2-425c-af99-2a357204014e
Artiguenave, François
5bfb0a7f-b645-421e-af3a-d7d3f05dbaac
Adams, Martin
e87c9595-d6c8-420d-a9b3-a44508cfad5f
Cornette, Jocelyne
d9cd0c87-5d45-4cdc-925e-993602351c36
Viscogliosi, Eric
714cce9a-44d5-43be-b252-dfe97d00ca2d
Capron, Monique
6d02d62d-a06a-4dba-91cf-9ffd7136cd26
Balavoine, Guillaume
9e15ed97-16fd-4eb3-9fdc-f250954388ce

Pierce, Raymond J, Wu, Wenjie, Hirai, Hirohisa, Ivens, Al, Murphy, Lee D, Noël, Christophe, Johnston, David A, Artiguenave, François, Adams, Martin, Cornette, Jocelyne, Viscogliosi, Eric, Capron, Monique and Balavoine, Guillaume (2005) Evidence for a dispersed Hox gene cluster in the platyhelminth parasite Schistosoma mansoni. Molecular Biology and Evolution, 22 (12), 2491-2503. (doi:10.1093/molbev/msi239).

Record type: Article

Abstract

In most bilaterian organisms so far studied, Hox genes are organized in genomic clusters and determine development along the anteroposterior axis. It has been suggested that this clustering, together with spatial and temporal colinearity of gene expression, represents the ancestral condition. However, in organisms with derived modes of embryogenesis and lineage-dependent mechanisms for the determination of cell fate, temporal colinearity of expression can be lost and Hox cluster organization disrupted, as is the case for the ecdysozoans Drosophila melanogaster and Caenorhabditis elegans and the urochordates Ciona intestinalis and Oikopleura dioica. We sought to determine whether a lophotrochozoan, the platyhelminth parasite Schistosoma mansoni, possesses a conserved or disrupted Hox cluster. Using a polymerase chain reaction (PCR)-based strategy, we have cloned and characterized three novel S. mansoni genes encoding orthologues of Drosophila labial (SmHox1), deformed (SmHox4), and abdominal A (SmHox8), as well as the full-length coding sequence of the previously described Smox1, which we identify as an orthologue of fushi tarazu. Quantitative reverse transcriptase-PCR showed that the four genes were expressed at all life-cycle stages but that levels of expression were differentially regulated. Phylogenetic analysis and the conservation of "parapeptide" sequences C-terminal to the homeodomains of SmHox8 and Smox1 support the grouping of platyhelminths within the lophotrochozoan clade. However, Bacterial Artificial Chromosome (BAC) library screening followed by genome walking failed to reconstitute a cluster. The BAC clones containing Hox genes were sequenced, and in no case were other Hox genes found on the same clone. Moreover, the SmHox4 and SmHox8 genes contained single very large introns (>40 kbp) further indicating that the schistosome Hox cluster is highly extended. Localization of the Hox genes to chromosomes using fluorescence in situ hybridization showed that SmHox4 and SmHox8 are on the long arm of chromosome 4, whereas SmHox1 and Smox1 are on chromosome 3. In silico screening of the available genome sequences corroborated results of Southern blotting and BAC library screening that indicate that there are no paralogues of SmHox1, SmHox4, or SmHox8. The schistosome Hox cluster is therefore not duplicated, but is both dispersed and disintegrated in the genome.

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More information

Published date: 1 December 2005
Additional Information: © The Author 2005. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oupjournals.org
Keywords: Amino Acid Sequence, Animals, Chromosome Mapping, Chromosome Walking, Chromosomes, Artificial, Bacterial, Gene Expression, Gene Expression Regulation, Developmental, Genes, Helminth, Genes, Homeobox, Homeodomain Proteins/chemistry, Larva, Life Cycle Stages, Molecular Sequence Data, Phylogeny, Reverse Transcriptase Polymerase Chain Reaction, Schistosoma mansoni/genetics, Sequence Analysis, Protein

Identifiers

Local EPrints ID: 468918
URI: http://eprints.soton.ac.uk/id/eprint/468918
ISSN: 0737-4038
PURE UUID: eec1bc19-a2a4-48a1-8b48-2318e2488f81
ORCID for David A Johnston: ORCID iD orcid.org/0000-0001-6703-6014

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Date deposited: 01 Sep 2022 16:44
Last modified: 17 Mar 2024 03:11

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Contributors

Author: Raymond J Pierce
Author: Wenjie Wu
Author: Hirohisa Hirai
Author: Al Ivens
Author: Lee D Murphy
Author: Christophe Noël
Author: David A Johnston ORCID iD
Author: François Artiguenave
Author: Martin Adams
Author: Jocelyne Cornette
Author: Eric Viscogliosi
Author: Monique Capron
Author: Guillaume Balavoine

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