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Title: Genome organization of the vg1 and nodal3 gene clusters in the allotetraploid frog Xenopus laevis

Abstract

Extracellular factors belonging to the TGF-β family play pivotal roles in the formation and patterning of germ layers during early Xenopus embryogenesis. Here, we show that the vg1 and nodal3 genes of Xenopus laevis are present in gene clusters on chromosomes XLA1L and XLA3L, respectively, and that both gene clusters have been completely lost from the syntenic S chromosome regions. The presence of gene clusters and chromosome-specific gene loss were confirmed by cDNA FISH analyses. Sequence and expression analyses revealed that paralogous genes in the vg1 and nodal3 clusters on the L chromosomes were also altered compared to their Xenopus tropicalis orthologs. X. laevis vg1 and nodal3 paralogs have potentially become pseudogenes or sub-functionalized genes and are expressed at different levels. As X. tropicalis has a single vg1 gene on chromosome XTR1, the ancestral vg1 gene in X. laevis appears to have been expanded on XLA1L. Of note, two reported vg1 genes, vg1(S20) and vg1(P20), reside in the cluster on XLA1L. The nodal3 gene cluster is also present on X. tropicalis chromosome XTR3, but phylogenetic analysis indicates that nodal3 genes in X. laevis and X. tropicalis were independently expanded and/or evolved in concert within each cluster by gene conversion. Lastly,more » these findings provide insights into the function and molecular evolution of TGF-β family genes in response to allotetraploidization.« less

Authors:
 [1];  [2];  [1];  [3];  [3];  [4];  [1];  [1];  [4];  [2];  [5];  [6]
+ Show Author Affiliations
  1. Hiroshima University, Higashi-Hiroshima(Japan). Amphibian Research Center
  2. Nagoya University, Furo-cho, Chikusa-ku, Nagoya (Japan)
  3. HudsonAlpha Institute of Biotechnology, Huntsville, AL (United States)
  4. Kitasato University, Minamiku, Sagamihara (Japan)
  5. Univ. of California, Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Okinawa Institute of Science and Technology Graduate University, Onna, Okinawa (Japan)
  6. Uiversity of Tokyo, Tokyo (Japan)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1633220
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Developmental Biology
Additional Journal Information:
Journal Volume: 426; Journal Issue: 2; Journal ID: ISSN 0012-1606
Publisher:
Elsevier
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; vg1; gdf1; nodal3; Xenopus; TGF-β; Genomic structure

Citation Formats

Suzuki, Atsushi, Uno, Yoshinobu, Takahashi, Shuji, Grimwood, Jane, Schmutz, Jeremy, Mawaribuchi, Shuuji, Yoshida, Hitoshi, Takebayashi-Suzuki, Kimiko, Ito, Michihiko, Matsuda, Yoichi, Rokhsar, Daniel, and Taira, Masanori. Genome organization of the vg1 and nodal3 gene clusters in the allotetraploid frog Xenopus laevis. United States: N. p., 2016. Web. doi:10.1016/j.ydbio.2016.04.014.
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Suzuki, Atsushi, Uno, Yoshinobu, Takahashi, Shuji, Grimwood, Jane, Schmutz, Jeremy, Mawaribuchi, Shuuji, Yoshida, Hitoshi, Takebayashi-Suzuki, Kimiko, Ito, Michihiko, Matsuda, Yoichi, Rokhsar, Daniel, & Taira, Masanori. Genome organization of the vg1 and nodal3 gene clusters in the allotetraploid frog Xenopus laevis. United States. https://doi.org/10.1016/j.ydbio.2016.04.014
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Suzuki, Atsushi, Uno, Yoshinobu, Takahashi, Shuji, Grimwood, Jane, Schmutz, Jeremy, Mawaribuchi, Shuuji, Yoshida, Hitoshi, Takebayashi-Suzuki, Kimiko, Ito, Michihiko, Matsuda, Yoichi, Rokhsar, Daniel, and Taira, Masanori. Wed . "Genome organization of the vg1 and nodal3 gene clusters in the allotetraploid frog Xenopus laevis". United States. https://doi.org/10.1016/j.ydbio.2016.04.014. https://www.osti.gov/servlets/purl/1633220.
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@article{osti_1633220,
title = {Genome organization of the vg1 and nodal3 gene clusters in the allotetraploid frog Xenopus laevis},
author = {Suzuki, Atsushi and Uno, Yoshinobu and Takahashi, Shuji and Grimwood, Jane and Schmutz, Jeremy and Mawaribuchi, Shuuji and Yoshida, Hitoshi and Takebayashi-Suzuki, Kimiko and Ito, Michihiko and Matsuda, Yoichi and Rokhsar, Daniel and Taira, Masanori},
abstractNote = {Extracellular factors belonging to the TGF-β family play pivotal roles in the formation and patterning of germ layers during early Xenopus embryogenesis. Here, we show that the vg1 and nodal3 genes of Xenopus laevis are present in gene clusters on chromosomes XLA1L and XLA3L, respectively, and that both gene clusters have been completely lost from the syntenic S chromosome regions. The presence of gene clusters and chromosome-specific gene loss were confirmed by cDNA FISH analyses. Sequence and expression analyses revealed that paralogous genes in the vg1 and nodal3 clusters on the L chromosomes were also altered compared to their Xenopus tropicalis orthologs. X. laevis vg1 and nodal3 paralogs have potentially become pseudogenes or sub-functionalized genes and are expressed at different levels. As X. tropicalis has a single vg1 gene on chromosome XTR1, the ancestral vg1 gene in X. laevis appears to have been expanded on XLA1L. Of note, two reported vg1 genes, vg1(S20) and vg1(P20), reside in the cluster on XLA1L. The nodal3 gene cluster is also present on X. tropicalis chromosome XTR3, but phylogenetic analysis indicates that nodal3 genes in X. laevis and X. tropicalis were independently expanded and/or evolved in concert within each cluster by gene conversion. Lastly, these findings provide insights into the function and molecular evolution of TGF-β family genes in response to allotetraploidization.},
doi = {10.1016/j.ydbio.2016.04.014},
journal = {Developmental Biology},
number = 2,
volume = 426,
place = {United States},
year = {Wed Oct 05 00:00:00 EDT 2016},
month = {Wed Oct 05 00:00:00 EDT 2016}
}
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Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1016/j.ydbio.2016.04.014
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Figures / Tables:

Figure 1 Figure 1: Structure and expression of the vg1 gene cluster. (A) Schematic diagrams of the vg1 gene cluster in X. tropicalis (XTR) and X. laevis (XLA). Arrowheads indicate the direction and positions of genes. Distances in the schematic are proportional to the nucleotide lengths of the genes, except for vg1p.Smore » which contains a partial exon 1. Magenta and blue arrowheads indicate complete vg1 genes and the vg1 pseudogene, respectively. Orange and blue bars indicate the region covered by BAC full-sequences and scaffold70461 which were originally constructed in the v7.1 assembly. (B) cDNA FISH analysis of the vg1 gene. Hybridization signals (upper) are shown along with Hoechst staining images (lower) of chromosomes 1L and 1S. The position of the vg1 gene alongside the chromosome banding pattern of XLA1L. (C) RNA-seq expression profile of vg1 genes during oogenesis and early development. oo12, oo34 and oo56 indicate oocyte stage 1/2, 3/4 and 5/6, respectively.« less
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Works referenced in this record:

XPACE4 is a localized pro-protein convertase required for mesoderm induction and the cleavage of specific TGFβ proteins in Xenopus development
journal, February 2005

  • Birsoy, Bilge; Berg, Linnea; Williams, P. Huw
  • Development, Vol. 132, Issue 3
  • DOI: 10.1242/dev.01599

Vg1 is an essential signaling molecule in Xenopus development
journal, January 2006

  • Birsoy, Bilge; Kofron, Matt; Schaible, Kyle
  • Development, Vol. 133, Issue 1
  • DOI: 10.1242/dev.02144

Developmental expression of the protein product of Vg1, a localized maternal mRNA in the frog Xenopus laevis.
journal, April 1989

Secretion and mesoderm-inducing activity of the TGF-beta-related domain of Xenopus Vg1.
journal, December 1993

Localization of Xenopus Vg1 mRNA by Vera Protein and the Endoplasmic Reticulum
journal, May 1997

A Novel TGF-β-like Gene,fugacin,Specifically Expressed in the Spemann Organizer ofXenopus
journal, December 1995

  • Ecochard, V.; Cayrol, C.; Foulquier, F.
  • Developmental Biology, Vol. 172, Issue 2
  • DOI: 10.1006/dbio.1995.8052

Consed: A Graphical Tool for Sequence Finishing
journal, March 1998

  • Gordon, David; Abajian, Chris; Green, Phil
  • Genome Research, Vol. 8, Issue 3
  • DOI: 10.1101/gr.8.3.195

Xenopus tropicalis nodal-related gene 3 regulates BMP signaling: an essential role for the pro-region
journal, January 2004

Gene duplication: Past, present and future
journal, October 1999

Application of fluorescencein situ hybridization in genome analysis of the mouse
journal, January 1995

A New Nomenclature of Xenopus laevis Chromosomes Based on the Phylogenetic Relationship to Silurana/Xenopus tropicalis
journal, April 2015

  • Matsuda, Yoichi; Uno, Yoshinobu; Kondo, Mariko
  • Cytogenetic and Genome Research, Vol. 145, Issue 3-4
  • DOI: 10.1159/000381292

Xnr3 affects brain patterning via cell migration in the neural-epidermal tissue boundary during early Xenopus embryogenesis
journal, January 2013

  • Morita, Mariko; Yamashita, Satoshi; Matsukawa, Shinya
  • The International Journal of Developmental Biology, Vol. 57, Issue 9-10
  • DOI: 10.1387/ijdb.130161tm

Vegetal messenger RNA localization directed by a 340-nt RNA sequence element in Xenopus oocytes
journal, February 1992

Concerted and Birth-and-Death Evolution of Multigene Families
journal, December 2005

Identification and cloning of localized maternal RNAs from xenopus eggs
journal, October 1985

Early developmental expression and experimental axis determination by the chicken Vg1 gene
journal, November 1996

A nodal-related gene defines a physical and functional domain within the Spemann organizer
journal, July 1995

Genomic organization and modulation of gene expression of the TGF-β and FGF pathways in the allotetraploid frog Xenopus laevis
journal, June 2017

MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0
journal, October 2013

  • Tamura, Koichiro; Stecher, Glen; Peterson, Daniel
  • Molecular Biology and Evolution, Vol. 30, Issue 12
  • DOI: 10.1093/molbev/mst197

Processed Vg1 protein is an axial mesoderm inducer in xenopus
journal, August 1993

Homoeologous chromosomes of Xenopus laevis are highly conserved after whole-genome duplication
journal, July 2013

Mesendoderm Induction and Reversal of Left–Right Pattern by Mouse Gdf1, a Vg1-Related Gene
journal, November 2000

  • Wall, Nancy A.; Craig, Eileen J.; Labosky, Patricia A.
  • Developmental Biology, Vol. 227, Issue 2
  • DOI: 10.1006/dbio.2000.9926

TGF-β Superfamily Signaling in Embryonic Development and Homeostasis
journal, March 2009

A novel role for a nodal-related protein; Xnr3 regulates convergent extension movements via the FGF receptor
journal, May 2003

  • Yokota, Chika; Kofron, Matt; Zuck, Mike
  • Development, Vol. 130, Issue 10
  • DOI: 10.1242/dev.00434
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    Phylogenetic evidence for independent origins of GDF1 and GDF3 genes in anurans and mammals
    journal, September 2018

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