Skip to main content
OSTI.GOVU.S. Department of Energy Office of Scientific and Technical Information
U.S. Department of Energy
Office of Scientific and Technical Information
 

Insights into the evolution of the snail superfamily from metazoan wide molecular phylogenies and expression data in annelids

Journal Article · · BMC Evolutionary Biology (Online)
 [1];  [2];  [3];  [2];  [3];  [4]
  1. Université Paris Diderot (France). Centre National de la Recherche Scientifique (CNRS). Inst. Jacques Monod. Programme Development and Neurobiology; Centre National de la Recherche Scientifique (CNRS), Gif-sur-Yvette (France). Centre de Génétique Moléculaire. Evolution et Développement des Métazoaires; Université Paris Diderot (France). UFR des Sciences du Vivant; DOE/OSTI
  2. Centre National de la Recherche Scientifique (CNRS), Gif-sur-Yvette (France). Centre de Génétique Moléculaire. Evolution et Développement des Métazoaires
  3. Université Paris Diderot (France). Centre National de la Recherche Scientifique (CNRS). Inst. Jacques Monod. Programme Development and Neurobiology; Centre National de la Recherche Scientifique (CNRS), Gif-sur-Yvette (France). Centre de Génétique Moléculaire. Evolution et Développement des Métazoaires
  4. Université Paris Diderot (France). Centre National de la Recherche Scientifique (CNRS). Inst. Jacques Monod. Programme Development and Neurobiology; Centre National de la Recherche Scientifique (CNRS), Gif-sur-Yvette (France). Centre de Génétique Moléculaire. Evolution et Développement des Métazoaires; Université Paris Diderot (France). UFR des Sciences du Vivant
+ Show Author Affiliations
Background: An important issue concerning the evolution of duplicated genes is to understand why paralogous genes are retained in a genome even though the most likely fate for a redundant duplicated gene is nonfunctionalization and thereby its elimination. Here we study a complex superfamily generated by gene duplications, the snail related genes that play key roles during animal development. We investigate the evolutionary history of these genes by genomic, phylogenetic, and expression data studies. Results: We systematically retrieved the full complement of snail related genes in several sequenced genomes. Through phylogenetic analysis, we found that the snail superfamily is composed of three ancestral families, snail, scratchA and scratchB. Analyses of the organization of the encoded proteins point out specific molecular signatures, indicative of functional specificities for Snail, ScratchA and ScratchB proteins. We also report the presence of two snail genes in the annelid Platynereis dumerilii, which have distinct expression patterns in the developing mesoderm, nervous system, and foregut. The combined expression of these two genes is identical to that of two independently duplicated snail genes in another annelid, Capitella spI, but different aspects of the expression patterns are differentially shared among paralogs of Platynereis and Capitella. Conclusion: Our study indicates that the snail and scratchB families have expanded through multiple independent gene duplications in the different bilaterian lineages, and highlights potential functional diversifications of Snail and ScratchB proteins following duplications, as, in several instances, paralogous proteins in a given species show different domain organizations. Comparisons of the expression pattern domains of the two Platynereis and Capitella snail paralogs provide evidence for independent subfunctionalization events which have occurred in these two species. We propose that the snail related genes may be especially prone to subfunctionalization, and this would explain why the snail superfamily underwent so many independent duplications leading to maintenance of functional paralogs.
Research Organization:
USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
OSTI ID:
1626387
Journal Information:
BMC Evolutionary Biology (Online), Journal Name: BMC Evolutionary Biology (Online) Journal Issue: 1 Vol. 9; ISSN 1471-2148
Publisher:
BioMed CentralCopyright Statement
Country of Publication:
United States
Language:
English

References (74)

The polychaetePlatynereis dumerilii (Annelida): a laboratory animal with spiralian cleavage, lifelong segment proliferation and a mixed benthic/pelagic life cycle journal January 2004
A homologue ofsnail is expressed transiently in subsets of mesenchyme cells in the sea urchin embryo and is down-regulated in axis-deficient embryos journal January 2006
Expression patterns oftwist andsnail inTribolium (Coleoptera) suggest a homologous formation of mesoderm in long and short germ band insects journal January 1994
Expression ofsnail2,a Second Member of the Zebrafish Snail Family, in Cephalic Mesendoderm and Presumptive Neural Crest of Wild-Type andspadetailMutant Embryos journal November 1995
Conservation of Brachyury, Mef2, and Snail in the Myogenic Lineage of Jellyfish: A Connection to the Mesoderm of Bilateria journal April 2002
Prediction of complete gene structures in human genomic DNA journal April 1997
Characterisation of two snail genes in the gastropod mollusc Patella vulgata. Implications for understanding the ancestral function of the snail-related genes in Bilateria journal April 2002
Prospero and Snail expression during spider neurogenesis journal November 2003
Snail3 orthologues in vertebrates: divergent members of the Snail zinc-finger gene family journal January 2004
Characterization of twist and snail gene expression during mesoderm and nervous system development in the polychaete annelid Capitella sp. I journal May 2007
C2H2 zinc finger genes of the Gli, Zic, KLF, SP, Wilms’ tumour, Huckebein, Snail, Ovo, Spalt, Odd, Blimp-1, Fez and related gene families from Branchiostoma floridae journal September 2008
An amphioxus snail gene: Expression in paraxial mesoderm and neural plate suggests a conserved role in patterning the chordate embryo journal November 1998
Mutations that alter the morphology of the malpighian tubules in Drosophila journal September 1999
Dorsal and Snail homologs in leech development journal July 2001
Molecular and biological characterization of an isolate of the potyvirus passiflora virus Y naturally infecting soybean (Glycine max) in Brazil journal September 2022
The Drosophila gene escargot encodes a zinc finger motif found in snail-related genes journal February 1992
Transcriptional regulation by C-terminal binding proteins journal January 2007
Molecular Architecture of Annelid Nerve Cord Supports Common Origin of Nervous System Centralization in Bilateria journal April 2007
Timing and mechanism of ancient vertebrate genome duplications – the adventure of a hypothesis journal October 2005
Expression divergence between duplicate genes journal November 2005
Large-scale sequencing and the new animal phylogeny journal November 2006
Analysis of forkhead and snail expression reveals epithelial–mesenchymal transitions during embryonic and larval development of Nematostella vectensis journal November 2004
Complementary striped expression patterns of NK homeobox genes during segment formation in the annelid Platynereis journal May 2008
The increasing complexity of the Snail gene superfamily in metazoan evolution journal April 2001
The Drosophila developmental gene snail encodes a protein with nucleic acid binding fingers journal November 1987
Broad phylogenomic sampling improves resolution of the animal tree of life journal March 2008
Mammalian Scratch: A neural-specific Snail family transcriptional repressor journal March 2001
Evolutionary conservation pattern of zinc-finger domains of Drosophila segmentation genes. journal November 1992
A Simple, Fast, and Accurate Algorithm to Estimate Large Phylogenies by Maximum Likelihood journal October 2003
MRBAYES: Bayesian inference of phylogenetic trees journal August 2001
dCtBP mediates transcriptional repression by Knirps, Krüppel and Snail in the Drosophila embryo journal December 1998
The mesoderm determinant Snail collaborates with related zinc-finger proteins to control Drosophila neurogenesis journal November 1999
A family of Snail-related zinc finger proteins regulates two distinct and parallel mechanisms that mediate Drosophila neuroblast asymmetric divisions journal April 2001
Preservation of Duplicate Genes by Complementary, Degenerative Mutations journal April 1999
MUSCLE: multiple sequence alignment with high accuracy and high throughput journal March 2004
Genome-wide analyses identify transcription factors required for proper morphogenesis of Drosophila sensory neuron dendrites journal March 2006
scratch, a pan-neural gene encoding a zinc finger protein related to snail, promotes neuronal development. journal October 1995
GeneID in Drosophila journal April 2000
Control of Vertebrate Left-Right Asymmetry by a Snail -Related Zinc Finger Gene journal February 1997
Interaction of Short-Range Repressors with Drosophila CtBP in the Embryo journal April 1998
Control of Cell Behavior During Vertebrate Development by Slug , a Zinc Finger Gene journal May 1994
The LIM Protein AJUBA Recruits Protein Arginine Methyltransferase 5 To Mediate SNAIL-Dependent Transcriptional Repression journal May 2008
The Ajuba LIM Domain Protein Is a Corepressor for SNAG Domain–Mediated Repression and Participates in Nucleocytoplasmic Shuttling journal October 2007
atonal- and achaete-scute-related genes in the annelid Platynereis dumerilii: insights into the evolution of neural basic-Helix-Loop-Helix genes journal June 2008
Investigating the origins of triploblasty: `mesodermal' gene expression in a diploblastic animal, the sea anemone Nematostella vectensis (phylum, Cnidaria; class, Anthozoa) journal May 2004
The Snail genes as inducers of cell movement and survival: implications in development and cancer journal July 2005
The snail gene required for mesoderm formation in Drosophila is expressed dynamically in derivatives of all three germ layers journal April 1991
Altered mitotic domains reveal fate map changes in Drosophila embryos mutant for zygotic dorsoventral patterning genes journal April 1992
Induction of the prospective neural crest of Xenopus journal March 1995
Determination of wing cell fate by the escargot and snail genes in Drosophila journal April 1996
Dorsoventral patterning of the vertebrate neural tube is conserved in a protochordate journal June 1997
Conserved and divergent roles for members of the Snail family of transcription factors in the chick and mouse embryo journal August 1998
The Snail protein family regulates neuroblast expression ofinscuteableandstring, genes involved in asymmetry and cell division inDrosophila journal December 2001
Concatenated Analysis Sheds Light on Early Metazoan Evolution and Fuels a Modern “Urmetazoon” Hypothesis journal January 2009
Fluorescent two-color whole mount in situ hybridization in Platynereis dumerilii (Polychaeta, Annelida), an emerging marine molecular model for evolution and development journal October 2005
Cellular resolution expression profiling using confocal detection of NBT/BCIP precipitate by reflection microscopy journal June 2007
Genome evolution and speciation genetics of clawed frogs (Xenopus and Silurana) journal January 2008
Evolution by Gene Duplication book January 1970
Lamprey snail highlights conserved and novel patterning roles in vertebrate embryos journal October 2008
The Drosophila gene escargot encodes a zinc finger motif found in snail-related genes journal February 1992
The increasing complexity of the Snail gene superfamily in metazoan evolution journal April 2001
The Trichoplax genome and the nature of placozoans journal August 2008
The snail superfamily of zinc-finger transcription factors journal March 2002
MrBayes 3: Bayesian phylogenetic inference under mixed models journal August 2003
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs journal September 1997
The Pfam protein families database journal December 2007
A General Empirical Model of Protein Evolution Derived from Multiple Protein Families Using a Maximum-Likelihood Approach journal May 2001
BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data journal July 1997
The LIM Protein AJUBA Recruits Protein Arginine Methyltransferase 5 To Mediate SNAIL-Dependent Transcriptional Repression journal May 2008
The Gfi-1 Proto-Oncoprotein Contains a Novel Transcriptional Repressor Domain, SNAG, and Inhibits G1 Arrest Induced by Interleukin-2 Withdrawal journal November 1996
The Ajuba LIM Domain Protein Is a Corepressor for SNAG Domain–Mediated Repression and Participates in Nucleocytoplasmic Shuttling journal October 2007
Cloning and developmental expression of Sna, a murine homologue of the Drosophila snail gene journal September 1992
Differential regulation of gastrulation and neuroectodermal gene expression by Snail in the Drosophila embryo journal October 1997
Expression Patterns of a twist-Related Gene in Embryos of the Spider Achaearanea tepidariorum Reveal Divergent Aspects of Mesoderm Development in the Fly and Spider journal February 2005

Cited By (2)

Genome-Wide Heterogeneity of Nucleotide Substitution Model Fit journal January 2011
Functional analysis of Scratch2 domains: implications in the evolution of Snail transcriptional repressors posted_content January 2018

Similar Records

Evolutionary history of the iroquois/Irx genes in metazoans
Journal Article · Tue Apr 14 20:00:00 EDT 2009 · BMC Evolutionary Biology (Online) · OSTI ID:1626384
Insights into bilaterian evolution from three spiralian genomes
Journal Article · Fri Jan 06 23:00:00 EST 2012 · Nature (London) · OSTI ID:1165995
Genomic Organization and Expression Demonstrate Spatial and Temporal Hox Gene Colinearity in the Lophotrochozoan Capitella sp. I
Journal Article · Mon Dec 22 19:00:00 EST 2008 · PLoS ONE · OSTI ID:1627363

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Evolutionary Biology
Genetics & Heredity