Skip to main content
SpringerLink
Log in

Phylogeny of forkhead genes in three spiralians and their expression in Pacific oyster Crassostrea gigas

  • Biology
  • Published:
Chinese Journal of Oceanology and Limnology Aims and scope Submit manuscript

Abstract

The Fox genes encode a group of transcription factors that contain a forkhead domain, which forms a structure known as a winged helix. These transcription factors play a crucial role in several key biological processes, including development. High-degree identity in the canonical forkhead domain has been used to divide Fox proteins into 23 families (FoxA to FoxS). We surveyed the genome of three spiralians, the oyster Crassostrea gigas, the limpet Lottia gigantea, and the annelid Capitella teleta. We identified 25 C. gigas fox genes, 21 L. gigantea fox genes, and 25 C. teleta fox genes. The C. gigas fox and L. gigantea fox genes represented 19 of the 23 families, whereas FoxI, Q1, R, and S were missing. The majority of the Fox families were observed within the C. teleta fox genes, with the exception of FoxR and S. In addition, the foxAB-like gene, foxY-like gene, and foxH gene were also present in the three genomes. The conserved FoxC-FoxL1 cluster, observed in mammals, was also found in C. gigas. The diversity of temporal expression patterns observed across the developmental process implies the C. gigas fox genes exert a wide range of functions. Further functional studies are required to gain insight into the evolution of Fox genes in bilaterians.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Arenas-Mena C. 2006. Embryonic expression of HeFoxA1 and HeFoxA2 in an indirectly developing polychaete. Development Genes and Evolution, 216: 727–736.

    Article  Google Scholar 

  • Bayne B. 1971. Some Morphological Changes that Occur at the Metamorphosis of the Larvae of Mytilus edulis. Cambridge University Press, Cambridge, Britain. p.259–280.

    Google Scholar 

  • Bernard F R. 1974. Particle sorting and labial palp function in the Pacific oyster Crassostrea gigas. Biological Bulletin, 146: 1–10.

    Article  Google Scholar 

  • Berthelin C, Kellner K, Mathieu M. 2000. Histological characterization and glucose incorporation into glycogen of the Pacific oyster Crassostrea gigas storage cells. Marine Biotechnology, 2(2): 136–145.

    Google Scholar 

  • Boyle M J, Seaver E C. 2008. Developmental expression of foxA and gata genes during gut formation in the polychaete annelid Capitella sp. I. Evolution Development, 10: 89–105.

    Article  Google Scholar 

  • Boyle M J, Seaver E C. 2010. Expression of FoxA and GATA transcription factors correlates with regionalized gut development in two lophotrochozoan marine worms: Chaetopterus (Annelida) and Themiste lageniformis (Sipuncula). Evolution Development, 1: 2, http://dx.doi.org/10.1186/2041-9139-1-2.

    Google Scholar 

  • Carlsson P, Mahlapuu M. 2002. Forkhead transcription factors: key players in development and metabolism. Developmental Biology, 250: 1–23.

    Article  Google Scholar 

  • Clark K L, Halay E D, Lai E, Burley S K. 1993. Co-crystal structure of the HNF-3/fork head DNA-recognition motif resembles histone H5. Nature, 364: 412–420.

    Article  Google Scholar 

  • Cutting A D, Bannister S C, Doran T J, Sinclair A H, Tizard M V, Smith C A. 2012. The potential role of microRNAs in regulating gonadal sex differentiation in the chicken embryo. Chromosome Research, 20: 201–213.

    Article  Google Scholar 

  • Fleury E, Huvet A, Lelong C, Lorgeril J, Boulo V, Gueguen Y et al. 2009. Generation and analysis of a 29,745 unique expressed sequence tags from the Pacific oyster ( Crassostrea gigas) assembled into a publicly accessible database: the GigasDatabase. BMC Genomics, 10: 341.

    Article  Google Scholar 

  • Gosling E M. 2003. Bivalve Molluscs: Biology, Ecology and Culture. Wiley-Blackwell.

    Book  Google Scholar 

  • Granadino B, Pêrez-Sanchez C, Rey-Campos J. 2000. Fork head transcription factors. Current Genomics, 1: 353–382.

    Article  Google Scholar 

  • Hiroyuki K, Naoki H, Daichi G S, Hiroki O, Miho Y, Tatsumi S. 2013. A genome-wide survey of genes encoding transcription factors in Japanese pearl oyster Pinctada fucata: II. Tbx, Fox, Ets, HMG, NFκB, bZIP, and C2H2 Zinc Fingers. Zoological Science, 30: 858–867.

    Article  Google Scholar 

  • Hope I A, Mounsey A, Bauer P, Aslam S. 2003. The forkhead gene family of Caenorhabditis elegans. Gene, 304: 43–55.

    Article  Google Scholar 

  • Huan P, Wang H X, Dong B, Liu B Z. 2012. Identification of differentially expressed proteins involved in the early larval development of the Pacific oyster Crassostrea gigas. Journal of Proteomics, 75(13): 3 855–3 865.

    Article  Google Scholar 

  • Huelsenbeck J P, Ronquist F. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17: 754–755.

    Article  Google Scholar 

  • Kasumi Y, Yutaka S, Françoise M, Shimeld S M, Degnan B. 2003. A genomewide survey of developmentally relevant genes in Ciona intestinalis III. Genes for Fox, ETS, nuclear receptors and NFκB. Development Genes and Evolution, 213: 235–244.

    Article  Google Scholar 

  • Klaus H K, Walter K, Daniel E M. 2000. Unified nomenclature for the winged helix/forkhead transcription factors. Genes Development, 14: 142–146.

    Google Scholar 

  • Koba N, Ohfuji T, Ha Y, Mizushima S, Tsukada A, Saito N, Shimada K. 2008. Proflies of mRNA expression of FoxL2, P450arom, DMRT1, AMH, P450c17, SF1, Erα and AR, in relation to gonadal sex differentiation in duck embryo. Journal of Poultry Science, 45: 132–138.

    Article  Google Scholar 

  • Kos R, Reedy M V, Johnson R L, Erickson C A. 2001. The winged-helix transcription factor FoxD3 is important for establishing the neural crest lineage and repressing melanogenesis in avian embryos. Development, 128: 1 467–1 479.

    Google Scholar 

  • Lai E, Prezioso V R, Tao W F, Chen W S, Darnell J E. 1991. Hepatocyte nuclear factor 3 alpha belongs to a gene family in mammals that is homologous to the Drosophila homeotic gene fork head. Genes Development, 5: 416–427.

    Article  Google Scholar 

  • Larroux C, Luke G N, Koopman P, Rokhsar D S, Shimeld S M, Degnan B M. 2008. Genesis and expansion of metazoan transcription factor gene classes. Molecular Biology and Evolution, 25: 980–996.

    Article  Google Scholar 

  • Lartillot N, Gouar M L, Adoutte A. 2002. Expression patterns of fork head and goosecoid homologues in the mollusc Patella vulgata supports the ancestry of the anterior mesendoderm across Bilateria. Development Genes and Evolution, 212: 551–561.

    Article  Google Scholar 

  • Li C, Tucker P W. 1993. DNA-binding properties and secondary structural model of the hepatocyte nuclear factor 3/fork head domain. Proceedings of the National Academy of Sciences USA, 90: 11 583–11 587.

    Article  Google Scholar 

  • Lough R G, Gonor J J. 1971. Early embryonic stages of Adula californiensis (Pelecypoda: Mytilidae) and the effect of temperature and salinity on developmental rate. Marine Biology, 8: 118–125.

    Article  Google Scholar 

  • Masuko K, Masaru K. 2004. Human FOX gene family. International Journal of Oncology, 25: 1 495–1 500.

    Google Scholar 

  • Mazet F, Amemiya C T, Shimeld S M. 2006. An ancient Fox gene cluster in bilaterian animals. Current Biology, 16: R314–316.

    Article  Google Scholar 

  • Mazet F, Luke G N, Shimeld S M. 2005. The amphioxus FOXQ1 gene is expressed in the developing endostyle. Gene Expression Patterns, 5: 313–315.

    Article  Google Scholar 

  • Mazet F, Shimeld S M. 2002. The evolution of chordate neural segmentation. Development Biology, 251: 258–270.

    Article  Google Scholar 

  • Mazet F, Yu J K, Liberles D A, Holland L Z, Shimeld S M. 2003. Phylogenetic relationships of the Fox (Forkhead) gene family in the Bilateria. Gene, 316: 79–89.

    Article  Google Scholar 

  • Michio O, Yutaka S. 2003. Expression of FoxE and FoxQ genes in the endostyle of Ciona intestinalis. Development Genes and Evolution, 213: 416–419.

    Article  Google Scholar 

  • Monteiro A S, Ferrier D E. 2006. Hox genes are not always colinear. International Journal of Biological Sci ences, 2: 95–103.

    Article  Google Scholar 

  • Naimi A, Martinez A S, Specq M L, Diss B, Mathieu M, Sourdaine P. 2009. Molecular cloning and gene expression of Cg -FoxL2 during the development and the adult gametogenetic cycle in the oyster Crassostrea gigas. Comparative Biochemistry and Physiology, Part B, 154: 134–142.

    Article  Google Scholar 

  • Nakae J, Cao Y, Oki M, Orba Y, Sawa H, Kiyonari H, Iskandar K, Suga K, Lombes M, Hayashi Y. 2008. Forkhead transcription factor FoxO1 in adipose tissue regulates energy storage and expenditure. Diabetes, 57(3): 563–576.

    Article  Google Scholar 

  • Ogg S, Paradis S, Gottlieb S, Patterson G I, Lee L T H A, Ruvkun G. 1997. The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature, 389(6654): 994–999.

    Article  Google Scholar 

  • Pohl B S, Knochel W. 2005. Of fox and frogs: fox(forkhead/winged helix) transcription factors in Xenopus development. Gene, 344: 21–32.

    Article  Google Scholar 

  • Ransick A, Rast J P, Minokawa T, Calestani C, Davidson E H. 2002. New early zygotic regulators expressed in endomesoderm of sea urchin embryos discovered by differential array hybridization. Development Biology, 246: 132–147.

    Article  Google Scholar 

  • Ronquist F, Huelsenbeck J P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19: 1 572–1 574.

    Article  Google Scholar 

  • Santerre C, Sourdaine P, Martinez A S. 2012. Expression of a natural antisense transcript of Cg-Foxl2 during the gonadic differentiation of the oyster Crassostrea gigas: first demonstration in the gonads of a lophotrochozoa species. Sexual development, 6: 210–221.

    Article  Google Scholar 

  • Shen X Y, Cui J Z, Gong Q L. 2011. Fox gene loci in Takifugu rubripes and Tetraodon nigroviridis genomes and comparison with those of medaka and zebrafish genomes. Genome, 54: 965–972.

    Article  Google Scholar 

  • Shen X Y, Cui J Z, Nagahama Y. 2012. The forkhead gene family in medaka: expression patterns and gene evolution. Cytogenet ic and Genome Res earch, 136: 123–130.

    Article  Google Scholar 

  • Shimeld S M, Boyle M J, Brunet T, Luke G N, Seaver E C. 2010. Clustered Fox genes in lophotrochozoans and the evolution of the bilaterian Fox gene cluster. Developmental Biology, 340: 234–248.

    Article  Google Scholar 

  • Simakov O, Marletaz F, Cho S J, Edsinger-Gonzales E, Havlak P, Hellsten U. 2012. Insights into bilaterian evolution from three spiralian genomes. Nature, 493: 526–531.

    Article  Google Scholar 

  • Sridhar H, Klaus H K. 2009. The evolution of Fox genes and their role in development and disease. Nature, 10: 233–240.

    Google Scholar 

  • Sullivan F X, Kumar R, Kriz R, Stahl M, Xu G Y, Rouse J, Chang X J, Boodhoo A, Potvin B, Cumming D A. 1998. Molecular cloning of human GDP-mannose 4, 6-dehydratase and reconstitution of GDP-fucose biosynthesis in vitro. Journal of Biological Chemistry, 273: 8 193–8 202.

    Article  Google Scholar 

  • Takahashi H, Takahashi K, Liu F C. 2000. FOXP Genes, Neural Development, Speech and Language Disorders. In: Madame Curie Bioscience Database. Austin (TX): Landes Bioscience. http://www.ncbi.nlm.nih.gov/books/NBK7023/.

    Google Scholar 

  • Thompson J D, Gibson T J, Plewniak F, Jeanmougin F, Higgins D G. 1997. The CLUSTALX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25: 4 876–4 882.

    Article  Google Scholar 

  • Tu Q, Brown C T, Davidson E H, Oliveri P. 2006. Sea urchin Forkhead gene family: phylogeny and embryonic expression. Development Biology, 300: 49–62.

    Article  Google Scholar 

  • Wang D S, Kobayashi T, Zhou L Y, Paul-Prasanth B, Ijiri S, Sakai F et al. 2007. Foxl2 up-regulates aromatase gene transcription in a female-specific manner by binding to the promoter as well as interacting with ad4 binding protein/steroidogenic factor 1. Molecular Endocrinology, 21: 712–725.

    Article  Google Scholar 

  • Weigel D, Jäckle H. 1990. The fork head domain: a novel DNA binding motif of eukaryotic transcription factors. Cell, 63: 455–456.

    Article  Google Scholar 

  • Weigel D, Jurgens G, Kuttner F, Seifert E, Jackle H. 1989. The homeotic gene fork head encodes a nuclear protein and is expressed in the terminal regions of the Drosophila embryo. Cell, 57: 645–658.

    Article  Google Scholar 

  • Wotton K R, Mazet F, Shimeld S M. 2003. Expression of FoxC, FoxF, FoxL1, and FoxQ1 genes in the dogfish Scyliorhinus canicula defines ancient and derived roles for Fox genes in vertebrate development. Developmental Dynamics, 237: 1 590–1 603.

    Article  Google Scholar 

  • Yu J K, Mazet F, Chen Y T, Huang S W, Jung K C, Shimeld S M. 2008. The Fox genes of Branchiostoma floridae. Development Genes and Evolution, 218: 629–638.

    Article  Google Scholar 

  • Zannini M, Avantaggiato V, Biffali E, Aronone M I, Sato K, Pischetola M, Taylor B A, Phillips S J, Simeone A, Di Lauro R. 1997. TTF-2, a new forkhead protein, shows a temporal expression in the developing thyroid which is consistent with a role in controlling the onset of differentiation. EMBO Journal, 16(11): 3 185–3 197.

    Article  Google Scholar 

  • Zhang G F, Fang X D, Guo X M, Li L, Luo R B, Xu F et al. 2012. The oyster genome reveals stress adaptation and complexity of shell formation. Nature, 490: 49–54.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. National & Local Joint Engineering Laboratory of Ecological Mariculture, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China

    Mei Yang  (杨梅), Fei Xu  (许飞), Jun Liu  (刘俊), Huayong Que  (阙华勇), Li Li  (李莉) & Guofan Zhang  (张国范)

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Mei Yang  (杨梅) & Jun Liu  (刘俊)

Authors
  1. Mei Yang  (杨梅)
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fei Xu  (许飞)
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jun Liu  (刘俊)
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Huayong Que  (阙华勇)
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Li Li  (李莉)
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Guofan Zhang  (张国范)
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Li Li  (李莉) or Guofan Zhang  (张国范).

Additional information

Supported by the National Basic Research Program of China (973 Program) (No. 2010CB126401), the National Natural Science Foundation of China (No. 31402285), the National High Technology Research and Development Program of China (863 Program) (No. 2012AA10A405), the Earmarked Fund for Modern Agro-Industry Technology Research System (No. CARS-48), the Taishan Scholars Climbing Program of Shandong Province, and the Oversea Taishan Scholars Program of Shandong Province

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yang, M., Xu, F., Liu, J. et al. Phylogeny of forkhead genes in three spiralians and their expression in Pacific oyster Crassostrea gigas . Chin. J. Ocean. Limnol. 32, 1207–1223 (2014). https://doi.org/10.1007/s00343-015-4009-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00343-015-4009-x

Keyword

Search

Navigation