Genome-wide analysis of the sox family in the calcareous sponge Sycon ciliatum: multiple genes with unique expression patterns
Sox genes are HMG-domain containing transcription factors with important roles in developmental processes in animals; many of them appear to have conserved functions among eumetazoans. Demosponges have fewer Sox genes than eumetazoans, but their roles remain unclear. The aim of this study is to gain insight into the early evolutionary history of the Sox gene family by identification and expression analysis of Sox genes in the calcareous sponge Sycon ciliatum.
Calcaronean Sox related sequences were retrieved by searching recently generated genomic and transcriptome sequence resources and analyzed using variety of phylogenetic methods and identification of conserved motifs. Expression was studied by whole mount in situ hybridization.
We have identified seven Sox genes and four Sox-related genes in the complete genome of Sycon ciliatum. Phylogenetic and conserved motif analyses showed that five of Sycon Sox genes represent groups B, C, E, and F present in cnidarians and bilaterians. Two additional genes are classified as Sox genes but cannot be assigned to specific subfamilies, and four genes are more similar to Sox genes than to other HMG-containing genes. Thus, the repertoire of Sox genes is larger in this representative of calcareous sponges than in the demosponge Amphimedon queenslandica. It remains unclear whether this is due to the expansion of the gene family in Sycon or a secondary reduction in the Amphimedon genome. In situ hybridization of Sycon Sox genes revealed a variety of expression patterns during embryogenesis and in specific cell types of adult sponges.
In this study, we describe a large family of Sox genes in Sycon ciliatum with dynamic expression patterns, indicating that Sox genes are regulators in development and cell type determination in sponges, as observed in higher animals. The revealed differences between demosponge and calcisponge Sox genes repertoire highlight the need to utilize models representing different sponge lineages to describe sponge development, a prerequisite for deciphering evolution of metazoan developmental mechanisms.
- Guth SI, Wegner M: Having it both ways: sox protein function between conservation and innovation. Cell Mol Life Sci 2008, 65:3000–3018. CrossRef
- Lefebvre V, Dumitriu B, Penzo-Méndez A, Han Y, Pallavi B: Control of cell fate and differentitation by Sry-related high-mobility-group box (Sox) transcription factors. Int J Biochem Cell B 2007, 39:2195–2214. CrossRef
- Gubbay J, Collignon J, Koopman P, Capel B, Economou A, Munsterberg A, Vivian N, Goodfellow P, Lovell-Badge R: A gene mapping to the sex-determining region of the mouse Y chromosome is a member of a novel family of embryonically expressed genes. Nature 1990, 346:245–250. CrossRef
- Schepers GE, Teasdale RD, Koopman P: Twenty pairs of sox: extent, homology, and nomenclature of the mouse and human sox transcription factor gene families. Dev Cell 2002, 3:167–170. CrossRef
- Bowles J, Schepers G, Koopman P: Phylogeny of the SOX family of developmental transcription factors based on sequence and structural indicators. Dev Biol 2000, 227:239–255. CrossRef
- King N, Westbrook MJ, Young S, Kuo A, Abedin M, Chapman J, Fairclough S, Hellsten U, Isogai Y, Letunic I, Marr M, Pincus D, Putnam N, Rokas A, Wright KJ, Zuzow R, Dirks W, Good M, Goodstein D, Lemons D, Li W, Lyons JB, Morris A, Nichols S, Richter DJ, Salamov A, Sequencing JG, Bork P, Lim WA, Manning G, et al.: The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 2008, 451:783–788. CrossRef
- Sebé-Pedrós A, de Mendoza A, Lang BF, Degnan BM, Ruiz-Trillo I: Unexpected repertoire of metazoan transcription factors in the unicellular holozoan capsaspora owczarzaki . Mol Biol Evol 2011, 28:1241–1254. CrossRef
- Larroux C, Fahey B, Liubicich D, Hinman VF, Gauthier M, Gongora M, Green K, Wörheide G, Leys SP, Degnan BM: Developmental expression of transcription factor genes in a demosponge: insights into the origin of metazoan multicellularity. Evol Dev 2006, 8:150–173. CrossRef
- Larroux C, Luke GN, Koopman P, Rokhsar DS, Shimeld SM, Degnan BM: Genesis and expansion of metazoan transcription factor gene classes. Mol Biol Evol 2008, 25:980–996. CrossRef
- Srivastava M, Begovic E, Chapman J, Putnam NH, Hellsten U, Kawashima T, Kuo A, Mitros T, Salamov A, Carpenter ML, Signorovitch AY, Moreno MA, Kamm K, Grimwood J, Schmutz J, Shapiro H, Grigoriev IV, Buss LW, Schierwater B, Dellaporta SL, Rokhsar DS: The Trichoplax genome and the nature of placozoans. Nature 2008, 454:955–960. CrossRef
- Magie CR, Pang K, Martindale MQ: Genomic inventory and expression of Sox and Fox genes in the cnidarian Nematostella vectensis . Dev Genes Evol 2005, 215:618–630. CrossRef
- Shinzato C, Iguchi A, Hayward DC, Technau U, Ball EE, Miller DJ: Sox genes in the coral Acropora millepora : divergent expression patterns reflect differences in developmental mechanisms within the Anthozoa. BMC Evol Biol 2008, 8:311. CrossRef
- Jager M, Queinnec E, Le Guyarde H, Manuel M: Multiple Sox genes are expressed in stem cells or in differentiating neuro-sensory cells in the hydrozoan Clytia hemisphaerica . EvoDevo 2011, 2:12. CrossRef
- Jager M, Queinnec E, Chiori R, Le Guyader H, Manuel M: Insights into the early evolution of SOX genes from expression analyses in a ctenophore. J Exp Zool B Mol Dev Evol 2008, 310:650–667. CrossRef
- Jager M, Queinnec E, Houliston E, Manuel M: Expansion of the SOX gene family predated the emergence of the Bilateria. Mol Phylogenet Evol 2006, 39:468–477. CrossRef
- Adamska M, Degnan B, Green K, Zwafink C: What sponges can tell us about the evolution of developmental processes. Zoology 2011, 114:1–10. CrossRef
- Franzen W: Oogenesis and larval development of Scypha ciliata (Porifera, Calcarea). Zoomorphology 1988, 107:349–357. CrossRef
- Leys SP, Eerkes-Medrano D: Gastrulation in Calcareous Sponges: in Search of Haeckel’s Gastraea. Integr Comp Biol 2005, 45:342–351. CrossRef
- Ereskovsky AV: The Comparative Embryology of Sponges. Springer, Netherlands; 2010. CrossRef
- Bergsten J: A review of long-branch attraction. Cladistics 2005, 21:163–193. CrossRef
- Phochanukul N, Russell S: No backbone but lots of SOX: the invertebrate SOX family. Int J Biochem Cell Biol 2009, 42:453–464. CrossRef
- Amano S, Hori I: Metamorphosis of calcareous sponges I. Ultrastructure of free-swimming larvae. Invertebr Reprod Dev 1992, 21:81–90. CrossRef
- Gallissian MF, Vacelet J: Ultrastructure of the oocyte and embryo of the calcified sponge ( Petrobiona massiliana Porifera, Calcarea). Zoomorphology 1992, 112:133–141. CrossRef
- Tuzet O: Éponges calcaires. In Traité de Zoologie. Anatomie, Systématique, Biologie. Spongiaires. Edited by: Grassé P-P. Masson et Cie, Paris; 1973:27–132.
- Meulemans D, Bronner-Fraser M: The amphioxus soxB family: implications for the evolution of vertebrate placodes. Int J Biol Sci 2007, 3:356–364. CrossRef
- Nanda T, DeFalco SHY, Phochanukul LN, Camara N, VanDoren M, Russell S: Sox100B, a drosophila group e sox-domain gene, is required for somatic testis differentiation. Sexual Development 2009, 3:26–37. CrossRef
- Edgar RC: MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinform 2004, 5:113. CrossRef
- Abascal F, Zardoya R, Posada D: ProtTest: Selection of best-fit models of protein evolution. Bioinformatics 2005, 21:2104–2105. CrossRef
- Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O: New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of phyML 3.0. Syst Biol 2010, 59:307–321. CrossRef
- Ronquist F, Huelsenbeck JP, van der Mark P: MrBayes 3.1. 2005.
- Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS: MEME Suite: tools for motif discovery and searching. Nucleic Acids Research 2010, suppl 2:W202-W208.
- Sigrist CJA, Cerutti L, de Castro E, Langendijk-Genevaux PS, Bulliard V, Bairoch A, Hulo N: PROSITE, a protein domain database for functional characterization and annotation. Nucleic Acids Research 2010, 38:161–166. CrossRef
- Larroux C, Fahey B, Adamska M, Richards GS, Gauthier M, Green K, Lovas E, Degnanet BM: Whole-Mount In Situ Hybridization in Amphimedon . Cold Spring Harbor Protocols 2008.
- Genome-wide analysis of the sox family in the calcareous sponge Sycon ciliatum: multiple genes with unique expression patterns
- Open Access
- Available under Open Access This content is freely available online to anyone, anywhere at any time.
- Online Date
- July 2012
- Online ISSN
- BioMed Central
- Additional Links
- Author Affiliations
- 1. Sars International Centre for Marine Molecular Biology, Thormøhlensgt. 55, Bergen, 5008, Norway
- 2. Department of Biology and Centre for Geobiology, University of Bergen, Thormøhlensgt. 55, Bergen, 5008, Norway