The amphioxus genome illuminates vertebrate origins and cephalochordate biology

Linda Z. Holland; Ricard Albalat; Kaoru Azumi; Elia Benito-Gutierrez; Matthew J. Blow; Marianne Bronner-Fraser; Frederic Brunet; Thomas Butts; Simona Candiani; Larry J. Dishaw; David E. K. Ferrier; Jordi Garcia-Fernandez; Jeremy J. Gibson-Brown; Carmela Gissi; Adam Godzik; Finn Hallbook; Dan Hirose; Kazuyoshi Hosomichi; Tetsuro Ikuta; Hidetoshi Inoko; Masanori Kasahara; Jun Kasamatsu; Takeshi Kawashima; Ayuko Kimura; Masaaki Kobayashi; Zbynek Kozmik; Kaoru Kubokawa; Vincent Laudet; Gary W. Litman; Alice C. McHardy; Daniel Meulemans; Masaru Nonaka; Robert P. Olinski; Zeev Pancer; Len A. Pennacchio; Mario Pestarino; Jonathan P. Rast; Isidore Rigoutsos; Marc Robinson-Rechavi; Graeme Roch; Hidetoshi Saiga; Yasunori Sasakura; Masanobu Satake; Yutaka Satou; Michael Schubert; Nancy Sherwood; Takashi Shiina; Naohito Takatori; Javier Tello; Pavel Vopalensky; Shuichi Wada; Anlong Xu; Yuzhen Ye; Keita Yoshida; Fumiko Yoshizaki; Jr-Kai Yu; Qing Zhang; Christian M. Zmasek; Pieter J. de Jong; Kazutoyo Osoegawa; Nicholas H. Putnam; Daniel S. Rokhsar; Noriyuki Satoh; Peter W. H. Holland

doi:10.1101/gr.073676.107

The amphioxus genome illuminates vertebrate origins and cephalochordate biology

Linda Z. Holland, Ricard Albalat, Kaoru Azumi, Elia Benito-Gutierrez, Matthew J. Blow, Marianne Bronner-Fraser, Frederic Brunet, Thomas Butts, Simona Candiani, Larry J. Dishaw, David E. K. Ferrier, Jordi Garcia-Fernandez, Jeremy J. Gibson-Brown, Carmela Gissi, Adam Godzik, Finn Hallbook, Dan Hirose, Kazuyoshi Hosomichi, Tetsuro Ikuta, Hidetoshi InokoMasanori Kasahara, Jun Kasamatsu, Takeshi Kawashima, Ayuko Kimura, Masaaki Kobayashi, Zbynek Kozmik, Kaoru Kubokawa, Vincent Laudet, Gary W. Litman, Alice C. McHardy, Daniel Meulemans, Masaru Nonaka, Robert P. Olinski, Zeev Pancer, Len A. Pennacchio, Mario Pestarino, Jonathan P. Rast, Isidore Rigoutsos, Marc Robinson-Rechavi, Graeme Roch, Hidetoshi Saiga, Yasunori Sasakura, Masanobu Satake, Yutaka Satou, Michael Schubert, Nancy Sherwood, Takashi Shiina, Naohito Takatori, Javier Tello, Pavel Vopalensky, Shuichi Wada, Anlong Xu, Yuzhen Ye, Keita Yoshida, Fumiko Yoshizaki, Jr-Kai Yu, Qing Zhang, Christian M. Zmasek, Pieter J. de Jong, Kazutoyo Osoegawa, Nicholas H. Putnam, Daniel S. Rokhsar, Noriyuki Satoh, Peter W. H. Holland

Research output: Contribution to journal › Article › peer-review

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Abstract

Cephalochordates, urochordates, and vertebrates evolved from a common ancestor over 520 million years ago. To improve our understanding of chordate evolution and the origin of vertebrates, we intensively searched for particular genes, gene families, and conserved noncoding elements in the sequenced genome of the cephalochordate Branchiostoma floridae, commonly called amphioxus or lancelets. Special attention was given to homeobox genes, opsin genes, genes involved in neural crest development, nuclear receptor genes, genes encoding components of the endocrine and immune systems, and conserved cis-regulatory enhancers. The amphioxus genome contains a basic set of chordate genes involved in development and cell signaling, including a fifteenth Hox gene. This set includes many genes that were co-opted in vertebrates for new roles in neural crest development and adaptive immunity. However, where amphioxus has a single gene, vertebrates often have two, three, or four paralogs derived from two whole-genome duplication events. In addition, several transcriptional enhancers are conserved between amphioxus and vertebrates-a very wide phylogenetic distance. In contrast, urochordate genomes have lost many genes, including a diversity of homeobox families and genes involved in steroid hormone function. The amphioxus genome also exhibits derived features, including duplications of opsins and genes proposed to function in innate immunity and endocrine systems. Our results indicate that the amphioxus genome is elemental to an understanding of the biology and evolution of nonchordate deuterostomes, invertebrate chordates, and vertebrates.

Original language	English
Pages (from-to)	1100-1111
Number of pages	12
Journal	Genome Research
Volume	18
Early online date	18 Jun 2008
DOIs	https://doi.org/10.1101/gr.073676.107
Publication status	Published - Jul 2008

Keywords

NEURAL CREST
CIONA-INTESTINALIS
NERVOUS-SYSTEM
DROSOPHILA-MELANOGASTER
BRANCHIOSTOMA-BELCHERI
MOLECULAR EVOLUTION
IMMUNE-SYSTEM
SEA-URCHIN
GENE
INSIGHTS

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Holland, L. Z., Albalat, R., Azumi, K., Benito-Gutierrez, E., Blow, M. J., Bronner-Fraser, M., Brunet, F., Butts, T., Candiani, S., Dishaw, L. J., Ferrier, D. E. K., Garcia-Fernandez, J., Gibson-Brown, J. J., Gissi, C., Godzik, A., Hallbook, F., Hirose, D., Hosomichi, K., Ikuta, T., ... Holland, P. W. H. (2008). The amphioxus genome illuminates vertebrate origins and cephalochordate biology. Genome Research, 18, 1100-1111. https://doi.org/10.1101/gr.073676.107

@article{ef83493a6948455fa77f2685709adee8,

title = "The amphioxus genome illuminates vertebrate origins and cephalochordate biology",

abstract = "Cephalochordates, urochordates, and vertebrates evolved from a common ancestor over 520 million years ago. To improve our understanding of chordate evolution and the origin of vertebrates, we intensively searched for particular genes, gene families, and conserved noncoding elements in the sequenced genome of the cephalochordate Branchiostoma floridae, commonly called amphioxus or lancelets. Special attention was given to homeobox genes, opsin genes, genes involved in neural crest development, nuclear receptor genes, genes encoding components of the endocrine and immune systems, and conserved cis-regulatory enhancers. The amphioxus genome contains a basic set of chordate genes involved in development and cell signaling, including a fifteenth Hox gene. This set includes many genes that were co-opted in vertebrates for new roles in neural crest development and adaptive immunity. However, where amphioxus has a single gene, vertebrates often have two, three, or four paralogs derived from two whole-genome duplication events. In addition, several transcriptional enhancers are conserved between amphioxus and vertebrates-a very wide phylogenetic distance. In contrast, urochordate genomes have lost many genes, including a diversity of homeobox families and genes involved in steroid hormone function. The amphioxus genome also exhibits derived features, including duplications of opsins and genes proposed to function in innate immunity and endocrine systems. Our results indicate that the amphioxus genome is elemental to an understanding of the biology and evolution of nonchordate deuterostomes, invertebrate chordates, and vertebrates.",

keywords = "NEURAL CREST, CIONA-INTESTINALIS, NERVOUS-SYSTEM, DROSOPHILA-MELANOGASTER, BRANCHIOSTOMA-BELCHERI, MOLECULAR EVOLUTION, IMMUNE-SYSTEM, SEA-URCHIN, GENE, INSIGHTS",

author = "Holland, {Linda Z.} and Ricard Albalat and Kaoru Azumi and Elia Benito-Gutierrez and Blow, {Matthew J.} and Marianne Bronner-Fraser and Frederic Brunet and Thomas Butts and Simona Candiani and Dishaw, {Larry J.} and Ferrier, {David E. K.} and Jordi Garcia-Fernandez and Gibson-Brown, {Jeremy J.} and Carmela Gissi and Adam Godzik and Finn Hallbook and Dan Hirose and Kazuyoshi Hosomichi and Tetsuro Ikuta and Hidetoshi Inoko and Masanori Kasahara and Jun Kasamatsu and Takeshi Kawashima and Ayuko Kimura and Masaaki Kobayashi and Zbynek Kozmik and Kaoru Kubokawa and Vincent Laudet and Litman, {Gary W.} and McHardy, {Alice C.} and Daniel Meulemans and Masaru Nonaka and Olinski, {Robert P.} and Zeev Pancer and Pennacchio, {Len A.} and Mario Pestarino and Rast, {Jonathan P.} and Isidore Rigoutsos and Marc Robinson-Rechavi and Graeme Roch and Hidetoshi Saiga and Yasunori Sasakura and Masanobu Satake and Yutaka Satou and Michael Schubert and Nancy Sherwood and Takashi Shiina and Naohito Takatori and Javier Tello and Pavel Vopalensky and Shuichi Wada and Anlong Xu and Yuzhen Ye and Keita Yoshida and Fumiko Yoshizaki and Jr-Kai Yu and Qing Zhang and Zmasek, {Christian M.} and {de Jong}, {Pieter J.} and Kazutoyo Osoegawa and Putnam, {Nicholas H.} and Rokhsar, {Daniel S.} and Noriyuki Satoh and Holland, {Peter W. H.}",

year = "2008",

month = jul,

doi = "10.1101/gr.073676.107",

language = "English",

volume = "18",

pages = "1100--1111",

journal = "Genome Research",

issn = "1088-9051",

publisher = "Cold Spring Harbor Laboratory Press",

}

Holland, LZ, Albalat, R, Azumi, K, Benito-Gutierrez, E, Blow, MJ, Bronner-Fraser, M, Brunet, F, Butts, T, Candiani, S, Dishaw, LJ, Ferrier, DEK, Garcia-Fernandez, J, Gibson-Brown, JJ, Gissi, C, Godzik, A, Hallbook, F, Hirose, D, Hosomichi, K, Ikuta, T, Inoko, H, Kasahara, M, Kasamatsu, J, Kawashima, T, Kimura, A, Kobayashi, M, Kozmik, Z, Kubokawa, K, Laudet, V, Litman, GW, McHardy, AC, Meulemans, D, Nonaka, M, Olinski, RP, Pancer, Z, Pennacchio, LA, Pestarino, M, Rast, JP, Rigoutsos, I, Robinson-Rechavi, M, Roch, G, Saiga, H, Sasakura, Y, Satake, M, Satou, Y, Schubert, M, Sherwood, N, Shiina, T, Takatori, N, Tello, J, Vopalensky, P, Wada, S, Xu, A, Ye, Y, Yoshida, K, Yoshizaki, F, Yu, J-K, Zhang, Q, Zmasek, CM, de Jong, PJ, Osoegawa, K, Putnam, NH, Rokhsar, DS, Satoh, N & Holland, PWH 2008, 'The amphioxus genome illuminates vertebrate origins and cephalochordate biology', Genome Research, vol. 18, pp. 1100-1111. https://doi.org/10.1101/gr.073676.107

TY - JOUR

T1 - The amphioxus genome illuminates vertebrate origins and cephalochordate biology

AU - Holland, Linda Z.

AU - Albalat, Ricard

AU - Azumi, Kaoru

AU - Benito-Gutierrez, Elia

AU - Blow, Matthew J.

AU - Bronner-Fraser, Marianne

AU - Brunet, Frederic

AU - Butts, Thomas

AU - Candiani, Simona

AU - Dishaw, Larry J.

AU - Ferrier, David E. K.

AU - Garcia-Fernandez, Jordi

AU - Gibson-Brown, Jeremy J.

AU - Gissi, Carmela

AU - Godzik, Adam

AU - Hallbook, Finn

AU - Hirose, Dan

AU - Hosomichi, Kazuyoshi

AU - Ikuta, Tetsuro

AU - Inoko, Hidetoshi

AU - Kasahara, Masanori

AU - Kasamatsu, Jun

AU - Kawashima, Takeshi

AU - Kimura, Ayuko

AU - Kobayashi, Masaaki

AU - Kozmik, Zbynek

AU - Kubokawa, Kaoru

AU - Laudet, Vincent

AU - Litman, Gary W.

AU - McHardy, Alice C.

AU - Meulemans, Daniel

AU - Nonaka, Masaru

AU - Olinski, Robert P.

AU - Pancer, Zeev

AU - Pennacchio, Len A.

AU - Pestarino, Mario

AU - Rast, Jonathan P.

AU - Rigoutsos, Isidore

AU - Robinson-Rechavi, Marc

AU - Roch, Graeme

AU - Saiga, Hidetoshi

AU - Sasakura, Yasunori

AU - Satake, Masanobu

AU - Satou, Yutaka

AU - Schubert, Michael

AU - Sherwood, Nancy

AU - Shiina, Takashi

AU - Takatori, Naohito

AU - Tello, Javier

AU - Vopalensky, Pavel

AU - Wada, Shuichi

AU - Xu, Anlong

AU - Ye, Yuzhen

AU - Yoshida, Keita

AU - Yoshizaki, Fumiko

AU - Yu, Jr-Kai

AU - Zhang, Qing

AU - Zmasek, Christian M.

AU - de Jong, Pieter J.

AU - Osoegawa, Kazutoyo

AU - Putnam, Nicholas H.

AU - Rokhsar, Daniel S.

AU - Satoh, Noriyuki

AU - Holland, Peter W. H.

PY - 2008/7

Y1 - 2008/7

N2 - Cephalochordates, urochordates, and vertebrates evolved from a common ancestor over 520 million years ago. To improve our understanding of chordate evolution and the origin of vertebrates, we intensively searched for particular genes, gene families, and conserved noncoding elements in the sequenced genome of the cephalochordate Branchiostoma floridae, commonly called amphioxus or lancelets. Special attention was given to homeobox genes, opsin genes, genes involved in neural crest development, nuclear receptor genes, genes encoding components of the endocrine and immune systems, and conserved cis-regulatory enhancers. The amphioxus genome contains a basic set of chordate genes involved in development and cell signaling, including a fifteenth Hox gene. This set includes many genes that were co-opted in vertebrates for new roles in neural crest development and adaptive immunity. However, where amphioxus has a single gene, vertebrates often have two, three, or four paralogs derived from two whole-genome duplication events. In addition, several transcriptional enhancers are conserved between amphioxus and vertebrates-a very wide phylogenetic distance. In contrast, urochordate genomes have lost many genes, including a diversity of homeobox families and genes involved in steroid hormone function. The amphioxus genome also exhibits derived features, including duplications of opsins and genes proposed to function in innate immunity and endocrine systems. Our results indicate that the amphioxus genome is elemental to an understanding of the biology and evolution of nonchordate deuterostomes, invertebrate chordates, and vertebrates.

AB - Cephalochordates, urochordates, and vertebrates evolved from a common ancestor over 520 million years ago. To improve our understanding of chordate evolution and the origin of vertebrates, we intensively searched for particular genes, gene families, and conserved noncoding elements in the sequenced genome of the cephalochordate Branchiostoma floridae, commonly called amphioxus or lancelets. Special attention was given to homeobox genes, opsin genes, genes involved in neural crest development, nuclear receptor genes, genes encoding components of the endocrine and immune systems, and conserved cis-regulatory enhancers. The amphioxus genome contains a basic set of chordate genes involved in development and cell signaling, including a fifteenth Hox gene. This set includes many genes that were co-opted in vertebrates for new roles in neural crest development and adaptive immunity. However, where amphioxus has a single gene, vertebrates often have two, three, or four paralogs derived from two whole-genome duplication events. In addition, several transcriptional enhancers are conserved between amphioxus and vertebrates-a very wide phylogenetic distance. In contrast, urochordate genomes have lost many genes, including a diversity of homeobox families and genes involved in steroid hormone function. The amphioxus genome also exhibits derived features, including duplications of opsins and genes proposed to function in innate immunity and endocrine systems. Our results indicate that the amphioxus genome is elemental to an understanding of the biology and evolution of nonchordate deuterostomes, invertebrate chordates, and vertebrates.

KW - NEURAL CREST

KW - CIONA-INTESTINALIS

KW - NERVOUS-SYSTEM

KW - DROSOPHILA-MELANOGASTER

KW - BRANCHIOSTOMA-BELCHERI

KW - MOLECULAR EVOLUTION

KW - IMMUNE-SYSTEM

KW - SEA-URCHIN

KW - GENE

KW - INSIGHTS

UR - http://www.scopus.com/inward/record.url?scp=46449117597&partnerID=8YFLogxK

U2 - 10.1101/gr.073676.107

DO - 10.1101/gr.073676.107

M3 - Article

SN - 1088-9051

VL - 18

SP - 1100

EP - 1111

JO - Genome Research

JF - Genome Research

ER -

The amphioxus genome illuminates vertebrate origins and cephalochordate biology

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Keywords

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