Cite this paper:
LIU Jun, XU Fei, JI Peng, LI Li, ZHANG Guofan. Evolutionary dynamics of the Wnt gene family: implications for lophotrochozoans[J]. HaiyangYuHuZhao, 2018, 36(5): 1720-1730

Evolutionary dynamics of the Wnt gene family: implications for lophotrochozoans

LIU Jun1,2,4, XU Fei1,3,4, JI Peng1,2,4, LI Li1,4,5, ZHANG Guofan1,3,4
1 Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China;
2 University of Chinese Academy of Sciences, Beijing 100049, China;
3 Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266000, China;
4 National & Local Joint Engineering Laboratory of Ecological Mariculture, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China;
5 Laboratory for Marine Fisheries and Aquaculture, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266000, China
Abstract:
Genes encoding Wnt ligands, which have important roles in cell communication and organ development, are restricted to multicellular animals. We systematically studied Wnt genes from eumetazoan genomes, with emphasis on the poorly studied superphylum Lophotrochozoa (four annelids, seven mollusks, eight platyhelminths, one bdelloid rotifer, and one brachiopod species). Between 3 and 39 Wnt loci were identified in each genome, and the protostome-specific loss of Wnt3 genes was confirmed. We identified gastropod-specific loss of Wnt8, refining the previously proposed mollusk-specific loss. Some duplicated Wnt genes belonging to a same subfamily or closely related subfamilies showed tandem distribution in the lophotrochozoan genomes, indicating tandem duplication events during Wnt family evolution. Members of the conserved Wnt10-Wnt6-Wnt1-Wnt9 cluster showed highly correlated expression patterns over time in two assayed lophotrochozoans, the oyster Crassostrea gigas and the brachiopod Lingula anatina, reflecting the possible similar function of the clustered Wnt genes.
Key words:    phylogeny|gene cluster|time-course expression|tissue distribution   
Received: 2017-04-27   Revised:
Tools
PDF (979 KB) Free
Print this page
Add to favorites
Email this article to others
Authors
Articles by LIU Jun
Articles by XU Fei
Articles by JI Peng
Articles by LI Li
Articles by ZHANG Guofan
References:
Adams M D, Celniker S E, Holt R A et al. 2000. The genome sequence of Drosophila melanogaster. Science, 287(5461):2 185-2 195.
Adamska M, Larroux C, Adamski M et al. 2010. Structure and expression of conserved Wnt pathway components in the demosponge Amphimedon queenslandica. Evolution & Development, 12(5):494-518, https://doi.org/10.1111/j.1525-142X.2010.00435.x.
Albertin C B, Simakov O, Mitros T et al. 2015. The octopus genome and the evolution of cephalopod neural and morphological novelties. Nature, 524(7564):220-224, https://doi.org/10.1038/nature14668.
Berriman M, Haas B J, LoVerde P T et al. 2009. The genome of the blood fluke Schistosoma mansoni. Nature, 460(7253):352-358.
Capella-Gutiérrez S, Silla-Martínez J M, Gabaldón T. 2009.trimAl:a tool for automated alignment trimming in largescale phylogenetic analyses. Bioinformatics, 25(15):1 972-1 973.
Cho S J, Vallès Y, Giani Jr V C et al. 2010. Evolutionary dynamics of the wnt gene family:a lophotrochozoan perspective. Molecular Biology and Evolution, 27(7):1 645-1 658.
Colbourne J K, Pfrender M E, Gilbert D et al. 2011. The ecoresponsive genome of Daphnia pulex. Science, 331(6017):555-561.
Croce J C, McClay D R. 2008. Evolution of the Wnt pathways. In:Vincan E eds. Wnt Signaling. Methods in Molecular Biology. Humana Press, Totowa, NJ, USA. p.3-18.
Croce J C, Wu S Y, Byrum C et al. 2006. A genome-wide survey of the evolutionarily conserved Wnt pathways in the sea urchin Strongylocentrotus purpuratus.Developmental Biology, 300(1):121-131.
Domazet-Lošo T, Tautz D. 2010. A phylogenetically based transcriptome age index mirrors ontogenetic divergence patterns. Nature, 468(7325):815-818, https://doi.org/10.1038/nature09632.
Du Y S, Zhang L L, Xu F et al. 2013. Validation of housekeeping genes as internal controls for studying gene expression during Pacific oyster (Crassostrea gigas) development by quantitative real-time PCR. Fish & Shellfish Immunology, 34(3):939-945, https://doi.org/10.1016/j.fsi.2012.12.007.
Fagotto F. 2014. Wnt signaling during early Xenopus development. In:Kloc M, Kubiak J Z eds. Xenopus Development. John Wiley & Sons, Inc., Oxford, UK.
Flot J F, Hespeels B, Li X et al. 2013. Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga.Nature, 500(7463):453-457.
Force A, Lynch M, Pickett F B et al. 1999. Preservation of duplicate genes by complementary, degenerative mutations. Genetics, 151(4):1 531-1 545.
Garriock R J, Warkman A S, Meadows S M et al. 2007. Census of vertebrate Wnt genes:isolation and developmental expression of Xenopus Wnt2, Wnt3, Wnt9a, Wnt9b, Wnt10a, and Wnt16. Developmental Dynamics, 236(5):1 249-1 258.
Gordon M D, Dionne M S, Schneider D S et al. 2005. WntD is a feedback inhibitor of Dorsal/NF-κB in Drosophila development and immunity. Nature, 437(7059):746-749, https://doi.org/10.1038/nature04073.
Gurley K A, Elliott S A, Simakov O et al. 2010. Expression of secreted Wnt pathway components reveals unexpected complexity of the planarian amputation response.Developmental Biology, 347(1):24-39.
Gyoja F. 2014. A genome-wide survey of bHLH transcription factors in the Placozoan Trichoplax adhaerens reveals the ancient repertoire of this gene family in metazoan. Gene, 542(1):29-37, https://doi.org/10.1016/j.gene.2014.03.024.
Holstein T W. 2012. The evolution of the Wnt pathway. Cold Spring Harbor Perspectives in Biology, 4(7):a007922, https://doi.org/10.1101/cshperspect.a007922.
Howe D G, Bradford Y M, Conlin T et al. 2013. ZFIN, the Zebrafish Model Organism Database:increased support for mutants and transgenics. Nucleic Acids Research, 41(D1):D854-D860, https://doi.org/10.1093/nar/gks938.
Huelsenbeck J P, Ronquist F. 2001. MRBAYES:Bayesian inference of phylogenetic trees. Bioinformatics, 17(8):754-755.
Ihaka R, Gentleman R. 1996. R:a language for data analysis and graphics. Journal of Computational and Graphical Statistics, 5(3):299-314.
Janssen R, Le Gouar M, Pechmann M et al. 2010. Conservation, loss, and redeployment of Wnt ligands in protostomes:implications for understanding the evolution of segment formation. BMC Evolutionary Biology, 10:374.
Katoh K, Standley D M. 2013. MAFFT multiple sequence alignment software version 7:improvements in performance and usability. Molecular Biology and Evolution, 30(4):772-780.
Kenny N J, Namigai E K O, Marlétaz F et al. 2015. Draft genome assemblies and predicted microRNA complements of the intertidal lophotrochozoans Patella vulgata (Mollusca, Patellogastropoda) and Spirobranchus(Pomatoceros) lamarcki (Annelida, Serpulida). Marine Genomics, 24:139-146.
Korswagen H C. 2002. Canonical and non-canonical Wnt signaling pathways in Caenorhabditis elegans:variations on a common signaling theme. BioEssays, 24(9):801-810.
Koziol U, Jarero F, Olson P D et al. 2016. Comparative analysis of Wnt expression identifies a highly conserved developmental transition in flatworms. BMC Biology, 14:10.
Kusserow A, Pang K, Sturm C et al. 2005. Une