Volume 37 Issue 3
May  2016
Turn off MathJax
Article Contents
Jing WANG, Guang LI, Guang-Hui QIAN, Jun-Hao HUA, Yi-Quan WANG. Expression analysis of eight amphioxus genes involved in the Wnt/β-catenin signaling pathway. Zoological Research, 2016, 37(3): 136-143. doi: 10.13918/j.issn.2095-8137.2016.3.136
Citation: Jing WANG, Guang LI, Guang-Hui QIAN, Jun-Hao HUA, Yi-Quan WANG. Expression analysis of eight amphioxus genes involved in the Wnt/β-catenin signaling pathway. Zoological Research, 2016, 37(3): 136-143. doi: 10.13918/j.issn.2095-8137.2016.3.136

Expression analysis of eight amphioxus genes involved in the Wnt/β-catenin signaling pathway

doi: 10.13918/j.issn.2095-8137.2016.3.136
Funds:  This work was financially supported by the National Natural Science Foundation of China (31372188, 31471986) and the Science and Technology Innovation Commission of Shenzhen Municipality (CXZZ20120614164555920)
More Information
  • Corresponding author: Yi-Quan WANG
  • Received Date: 2015-11-25
  • Rev Recd Date: 2016-04-25
  • Publish Date: 2016-05-18
  • The Wnt/β-catenin signaling pathway plays a crucial role in the embryonic development of metazoans. Although the pathway has been studied extensively in many model animals, its function in amphioxus, the most primitive chordate, remains largely uncharacterized. To obtain basic data for functional analysis, we identified and isolated seven genes (Lrp5/6, Dvl, APC, CkIα, CkIδ, Gsk3β, and Gro) of the Wnt/β-catenin signaling pathway from the amphioxus (Branchiostoma floridae) genome. Phylogenetic analysis revealed that amphioxus had fewer members of each gene family than that found in vertebrates. Whole-mount in situ hybridization showed that the genes were maternally expressed and broadly distributed throughout the whole embryo at the cleavage and blastula stages. Among them, Dvl was expressed asymmetrically towards the animal pole, while the others were evenly distributed in all blastomeres. At the mid-gastrula stage, the genes were specifically expressed in the primitive endomesoderm, but displayed different patterns. When the embryo developed into the neurula stage, the gene expressions were mainly detected in either paraxial somites or the tail bud. With the development of the embryo, the expression levels further decreased gradually and remained only in some pharyngeal regions or the tail bud at the larva stage. Our results suggest that the Wnt/β-catenin pathway might be involved in amphioxus somite formation and posterior growth, but not in endomesoderm specification.
  • loading
  • [1]
    Beaster-Jones L, Kaltenbach SL, Koop D, Yuan SC, Chastain R, Holland LZ. 2008. Expression of somite segmentation genes in amphioxus:a clock without a wavefront? Development Genes and Evolution, 218(11-12):599-611.
    [2]
    Bolognesi R, Farzana L, Fischer TD, Brown SJ. 2008. Multiple Wnt genes are required for segmentation in the short-germ embryo of Tribolium castaneum. Current Biology, 18(20):1624-1629.
    [3]
    Darras S, Gerhart J, Terasaki M, Kirschner M, Lowe CJ. 2011. β-Catenin specifies the endomesoderm and defines the posterior organizer of the hemichordate Saccoglossus kowalevskii. Development, 138(5):959-970.
    [4]
    Delsuc F, Brinkmann H, Chourrout D, Philippe H. 2006. Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature, 439(7079):965-968.
    [5]
    Dunty WC, Jr., Biris KK, Chalamalasetty RB, Taketo MM, Lewandoski M, Yamaguchi TP. 2008. Wnt3a/β-Catenin signaling controls posterior body development by coordinating mesoderm formation and segmentation. Development, 135(1):85-94.
    [6]
    Henry JQ, Perry KJ, Wever J, Seaver E, Martindale MQ. 2008. β-Catenin is required for the establishment of vegetal embryonic fates in the nemertean, Cerebratulus lacteus. Developmental Biology, 317(1):368-379.
    [7]
    Hikasa H, Sokol SY. 2013. Wnt signaling in vertebrate axis specification. Cold Spring Harbor Perspectives in Biology, 5(1):a007955.
    [8]
    Holland LZ. 2002. Heads or tails? Amphioxus and the evolution of anteriorposterior patterning in deuterostomes. Developmental Biology, 241(2):209-228.
    [9]
    Holland LZ, Holland ND. 2007. A revised fate map for amphioxus and the evolution of axial patterning in chordates. Integrative and Comparative Biology, 47(3):360-372.
    [10]
    Holland LZ, Panfilio KA, Chastain R, Schubert M, Holland ND. 2005. Nuclear β-Catenin promotes non-neural ectoderm and posterior cell fates in amphioxus embryos. Developmental Dynamics, 233(4):1430-1443.
    [11]
    Holstein TW. 2012. The evolution of the Wnt pathway. Cold Spring Harbor Perspectives in Biology, 4(7):a007922.
    [12]
    Hoppler S, Moon RT. 1998. BMP-2/-4 and Wnt-8 cooperatively pattern the Xenopus mesoderm. Mechanisms of Development, 71(1-2):119-129.
    [13]
    Imai K, Takada N, Satoh N, Satou Y. 2000. β-Catenin mediates the specification of endoderm cells in ascidian embryos. Development, 127(14):3009-3020.
    [14]
    Li G, Shu ZH, Wang YQ. 2013. Year-round reproduction and induced spawning of Chinese amphioxus, Branchiostoma belcheri, in laboratory. PLoS One, 8(9):e75461.
    [15]
    Li G, Yang X, Shu ZH, Chen XY, Wang YQ. 2012. Consecutive spawnings of Chinese amphioxus, Branchiostoma belcheri, in captivity. PLoS One, 7(12):e50838.
    [16]
    Lin HC, Holland LZ, Holland ND. 2006. Expression of the AmphiTcf gene in amphioxus:insights into the evolution of the TCF/LEF gene family during vertebrate evolution. Developmental Dynamics, 235(12):3396-3403.
    [17]
    Logan CY, Nusse R. 2004. The Wnt signaling pathway in development and disease. Annual Review of Cell and Developmental Biology, 20:781-810.
    [18]
    Logan CY, Miller JR, Ferkowicz MJ, Mcclay DR. 1999. Nuclear β-Catenin is required to specify vegetal cell fates in the sea urchin embryo. Development, 126(2):345-357.
    [19]
    Martin BL, Kimelman D. 2009. Wnt signaling and the evolution of embryonic posterior development. Current Biology, 19(5):R215-R219.
    [20]
    Martindale MQ. 2005. The evolution of metazoan axial properties. Nature Reviews Genetics, 6(12):917-927.
    [21]
    McCauley BS, Akyar E, Saad HR, Hinman VF. 2015. Dose-dependent nuclear β-Catenin response segregates endomesoderm along the sea star primary axis. Development, 142(1):207-217.
    [22]
    Miller JR, Rowning BA, Larabell CA, Yang-Snyder JA, Bates RL, Moon RT. 1999. Establishment of the dorsal-ventral axis in Xenopus embryos coincides with the dorsal enrichment of dishevelled that is dependent on cortical rotation. The Journal of Cell Biology, 146(2):427-437.
    [23]
    Miyawaki K, Mito T, Sarashina I, Zhang HJ, Shinmyo Y, Ohuchi H, Noji S. 2004. Involvement of Wingless/Armadillo signaling in the posterior sequential segmentation in the cricket, Gryllus bimaculatus (Orthoptera), as revealed by RNAi analysis. Mechanisms of Development, 121(2):119-130.
    [24]
    Mizumoto K, Sawa H. 2007. Two βs or not two βs:regulation of asymmetric division by β-Catenin. Trends in Cell Biology, 17(10):465-473.
    [25]
    Momose T, Houliston E. 2007. Two oppositely localised frizzled RNAs as axis determinants in a cnidarian embryo. PLoS Biology, 5(4):e70.
    [26]
    Momose T, Derelle R, Houliston E. 2008. A maternally localised Wnt ligand required for axial patterning in the cnidarian Clytia hemisphaerica. Development, 135(12):2105-2113.
    [27]
    Niehrs C. 2004. Regionally specific induction by the Spemann-Mangold organizer. Nature Reviews Genetics, 5(6):425-434.
    [28]
    Onai T, Takai A, Setiamarga DH, Holland LZ. 2012. Essential role of Dkk3 for head formation by inhibiting Wnt/β-Catenin and Nodal/Vg1 signaling pathways in the basal chordate amphioxus. Evolution & Development, 14(4):338-350.
    [29]
    Onai T, Yu JK, Blitz IL, Cho KW, Holland LZ. 2010. Opposing Nodal/Vg1 and BMP signals mediate axial patterning in embryos of the basal chordate amphioxus. Developmental Biology, 344(1):377-389.
    [30]
    Onai T, Lin HC, Schubert M, Koop D, Osborne PW, Alvarez S, Alvarez R, Holland ND, Holland LZ. 2009. Retinoic acid and Wnt/β-Catenin have complementary roles in anterior/posterior patterning embryos of the basal chordate amphioxus. Developmental Biology, 332(2):223-233.
    [31]
    Petersen CP, Reddien PW. 2009. Wnt signaling and the polarity of the primary body axis. Cell, 139(6):1056-1068.
    [32]
    Qian GH, Li G, Chen XY, Wang YQ. 2013. Characterization and embryonic expression of four amphioxus Frizzled genes with important functions during early embryogenesis. Gene Expression Patterns, 13(8):445-453.
    [33]
    Ramel MC, Lekven AC. 2004. Repression of the vertebrate organizer by Wnt8 is mediated by Vent and Vox. Development, 131(16):3991-4000.
    [34]
    Rao TP, Kuhl M. 2008. An updated overview on Wnt signaling pathways:a prelude for more. Circulation Research, 106(12):1798-1806.
    [35]
    Schubert M, Holland LZ, Stokes MD, Holland ND. 2001. Three amphioxus Wnt genes (AmphiWnt3, AmphiWnt5, and AmphiWnt6) associated with the tail bud:the evolution of somitogenesis in chordates. Developmental Biology, 240(1):262-273.
    [36]
    Schubert M, Holland LZ, Panopoulou GD, Lehrach H, Holland ND. 2000. Characterization of amphioxus AmphiWnt8:insights into the evolution of patterning of the embryonic dorsoventral axis. Evolution & Development, 2(2):85-92.
    [37]
    Tadjuidje E, Cha SW, Louza M, Wylie C, Heasman J. 2011. The functions of maternal Dishevelled 2 and 3 in the early Xenopus embryo. Developmental Dynamics, 240(7):1727-1736.
    [38]
    Takada S, Stark KL, Shea MJ, Vassileva G, Mcmahon JA, Mcmahon AP. 1994. Wnt-3a regulates somite and tailbud formation in the mouse embryo. Genes & Development, 8(2):174-189.
    [39]
    Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5:molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28(10):2731-2739.
    [40]
    Tao QH, Yokota C, Puck H, Kofron M, Birsoy B, Yan D, Asashima M, Wylie CC, Lin XH, Heasman J. 2005. Maternal wnt11 activates the canonical wnt signaling pathway required for axis formation in Xenopus embryos. Cell, 120(6):857-871.
    [41]
    Tian Q, Nakayama T, Dixon MP, Christian JL. 1999. Post-transcriptional regulation of Xwnt-8 expression is required for normal myogenesis during vertebrate embryonic development. Development, 126(15):3371-3380.
    [42]
    Weitzel HE, Illies MR, Byrum CA, Xu RH, Wikramanayake AH, Ettensohn CA. 2004. Differential stability of β-Catenin along the animal-vegetal axis of the sea urchin embryo mediated by dishevelled. Development, 131(12):2947-2956.
    [43]
    Wikramanayake AH, Huang L, Klein WH. 1998. β-Catenin is essential for patterning the maternally specified animal-vegetal axis in the sea urchin embryo. Proceedings of the National Academy of Sciences of the United States of America, 95(16):9343-9348.
    [44]
    Wikramanayake AH, Hong M, Lee PN, Pang K, Byrum CA, Bince JM, Xu RH, Martindale MQ. 2003. An ancient role for nuclear β-Catenin in the evolution of axial polarity and germ layer segregation. Nature, 426(6965):446-450.
    [45]
    Yu JK, Holland LZ. 2009. Amphioxus whole-mount in situ hybridization. Cold Spring Harbor Protocols, 2009(9):pdb.prot5286.
    [46]
    Yu JK, Satou Y, Holland ND, Shin IT, Kohara Y, Satoh N, Bronner-Fraser M, Holland LZ. 2007. Axial patterning in cephalochordates and the evolution of the organizer. Nature, 445(7128):613-617.
  • Relative Articles

    [1] Yue Lan, Jiao Wang, Qiao Yang, Rui-Xiang Tang, Min Zhou, Guang-Lun Lei, Jing Li, Liang Zhang, Bi-Song Yue, Zhen-Xin Fan. Blood transcriptome analysis reveals gene expression features of breast-feeding rhesus macaque (Macaca mulatta) infants. Zoological Research, 2020, 41(4): 431-436.  doi: 10.24272/j.issn.2095-8137.2020.044
    [2] Chao-Chao Yan, Xin-Shang Zhang, Liang Zhou, Qiao Yang, Min Zhou, Lin-Wan Zhang, Jin-Chuan Xing, Zhi-Feng Yan, Megan Price, Jing Li, Bi-Song Yue, Zhen-Xin Fan. Effects of aging on gene expression in blood of captive Tibetan macaques (Macaca thibetana) and comparisons with expression in humans. Zoological Research, 2020, 41(5): 557-563.  doi: 10.24272/j.issn.2095-8137.2020.092
    [3] Ya-Fei DUAN, Ping LIU, Ji-Tao LI, Jian LI, Bao-Quan GAO, Ping CHEN. Cloning and expression analysis of Cathepsin L cDNA of Exopalaemon carinicauda. Zoological Research, 2013, 34(1): 39-46.  doi: 10.3724/SP.J.1141.2013.01039
    [4] XU Wei, Li Wei-Ye, WANG Yi-Quan. Identification and expressional analysis of green fluorescent protein genes in amphioxus. Zoological Research, 2012, 33(3): 304-313.  doi: 10.3724/SP.J.1141.2012.03304
    [5] LI Xin-Yi, LIN Yu-Shuang, ZHANG Hong-Wei. Phylogenetic analysis and expression patterns of tropomyosin in amphioxus. Zoological Research, 2012, 33(4): 389-394.  doi: 10.3724/SP.J.1141.2012.04389
    [6] JIN Li-Sha, HAO Xiang-Fen, PENG Bai-Lu, ZHANG Yan-Chun, WAN Yu-Ling, JI Fang, XIA Ji-. Differential expression of six obesity-related genes with different disease phases of T2DM in cynomolgus monkey. Zoological Research, 2011, 32(1): 50-55.  doi: 10.3724/SP.J.1141.2011.01050
    [7] ZHANG Xiu-Juan, LI Xue-Jia, XIA Ji-Liang, YAN Sun-Xing, JI Fang, ZHANG Yan-Chun. Expression status of diabetes-associated genes in middle and aged cynomolgus monkeys. Zoological Research, 2011, 32(3): 300-306.  doi: 10.3724/SP.J.1141.2011.03300
    [8] SHEN Wang, YE Mao, SHI Ge, WANG Ri-Xin. cDNA Cloning, Characterization and mRNA Expression of a Profilin from the Swimming Crab Portunus trituberculatus. Zoological Research, 2010, 31(3): 261-267.  doi: 10.3724/SP.J.1141.2010.0326
    [9] ZHOU Rui-Xue MENG Tao, Meng Hai-Bo, HENG Dun-Xue BIN Shi-Yu CHENG Jia, FU Gui-Hong, CHU Wu-Ying, *, ZHANG Jian-She , *. Selection of Reference Genes in Transcription Analysis of Gene Expression of the Mandarin Fish, Siniperca chuasti. Zoological Research, 2010, 31(2): 141-146.  doi: 10.3724/SP.J.1141.2010.02141
    [10] Li Wei-Ye, Zhong Jing, Wang Yi-Quan. Analysis of Amphioxus Geographic Populations in the West Pacific Ocean Based on COX Ι Gene. Zoological Research, 2010, 31(4): 375-380.  doi: 10.3724/SP.J.1141.2010.04375
    [11] ZHANG Yu-jun, MAO Bing-yu. Developmental Expression of an Amphioxus (Branchiostoma belcheri) Gene Encoding a GATA Transcription Factor. Zoological Research, 2009, 30(2): 137-143.  doi: 10.3724/SP.J.1141.2009.02137
    [12] WEI Yun-hu, ZHANG Yu-jun, CHEN Yuan, MAO Bing-yu. Expansion of the Actin Gene Family in Amphioxus. Zoological Research, 2009, 30(5): 473-479.  doi: 10.3724/SP.J.1141.2009.05473
    [13] LIU Chang-qing, LIU Shuai, BAO A-dong, LU Tao-feng, WU Hong-mei, ZHANG Hong-hai. Molecular Clone, Expression, Structure and Function Study of Beijing Fatty Chicken ADSL Gene. Zoological Research, 2008, 29(4): 353-362.
    [14] LIAO Wan-qin, LIANG Xu-fang *, WANG Lin, MA Xu, FANG Ling, LI Gui-sheng. cDNA Sequence Cloning and Tissue Expression of Uncoupling Protein 2 of Silver Carp (Hypophthalmichthys molitrix). Zoological Research, 2006, 27(4): 375-381.
    [15] WANG Yi-quan , *, ZHANG Qiu-jin, LU Xiao-mei, ZHONG Jing, SUN Yi. Laboratory Culturing and Acquirement of the Second Filial Generation of Amphioxus. Zoological Research, 2006, 27(6): 631-634.
    [16] CAO Yun-chang, WEN Hong-bo, LI Wen-sheng, LIN Hao-ran. The Profile of Growth Hormone Gene Expression in Extrapituitary Tissues of Lepomis cyanellus. Zoological Research, 2005, 26(2): 174-178.
    [17] WANG Yi-quan, FANG Shao-hua. Taxonomic and Molecular Phylogenetic Studies of Amphioxus: A Review and Prospective Evaluation. Zoological Research, 2005, 26(6): 666-672.
    [18] WENG You-Zhu, HUANG Wei-Quan, FANG Yong-Qiang, YAO Bing, SUN Lan. Study on GnRH Receptor (GnRHR) mRNA In situ Hybridization in The Nervous System,Hatschek's Pit and Gonad of Amphioxus,Branchiostoma belcheri. Zoological Research, 2000, 21(6): 437-441.
    [19] WANG Jin-xing, ZHAO Xiao-fan, GONG Bo. Studies on The Expression of Isozyme Genes in Pupae and Embryogenesis of Antheraea pernyi. Zoological Research, 1996, 17(3): 239-246.
    [20] SHEN Qi-zhang. In Low Temperature Keep the Embryo of Protosalanx Hyalocranius. Zoological Research, 1990, 11(3): 258-258.
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Article Metrics

    Article views (1234) PDF downloads(1659) Cited by()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return