The presence of an anteroposterior body axis is a fundamental feature of bilateria. Within this group, echinoderms have secondarily evolved pentameral symmetric body plans. Although all echinoderms present bilaterally symmetric larval stages, they dramatically rearrange their body axis and develop a pentaradial body plan during metamorphosis. Therefore, the location of their anteroposterior body axis in adult forms remains a contentious issue. Unlike other echinoderms, sea cucumbers present an obvious anteroposterior axis not rearranged during metamorphosis, thus representing an interesting group to study their anteroposterior axis patterning. Hox genes are known to play a broadly conserved role in anteroposterior axis patterning in deuterostomes. Here, we report the expression patterns of Hox genes from early development to pentactula stage in sea cucumber. In early larval stages, five Hox genes (AjHox1, AjHox7, AjHox8, AjHox11/13a, and AjHox11/13b) were expressed sequentially along the archenteron, suggesting that the role of anteroposterior patterning of the Hox genes is conserved in bilateral larvae of echinoderms. In doliolaria and pentactula stages, eight Hox genes (AjHox1, AjHox5, AjHox7, AjHox8, AjHox9/10, AjHox11/13a, AjHox11/13b, and AjHox11/13c) were expressed sequentially along the digestive tract, following a similar expression pattern to that found in the visceral mesoderm of other bilateria. Unlike other echinoderms, pentameral expression patterns of AjHox genes were not observed in sea cucumber. Altogether, we concluded that AjHox genes are involved in the patterning of the digestive tract in both larvae and metamorphosis of sea cucumbers. In addition, the anteroposterior axis in sea cucumbers might be patterned like that of other bilateria.
This is a preview of subscription content, log in to check access.
Buy single article
Instant access to the full article PDF.
Price includes VAT for USA
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
This is the net price. Taxes to be calculated in checkout.
Angerer LM, Dolecki GJ, Gagnon ML, Lum R, Wang G, Yang Q, Humphreys T, Angerer RC (1989) Progressively restricted expression of a homeo box gene within the aboral ectoderm of developing sea urchin embryos. Genes Dev 3:370–383
Arenas-Mena C, Martinez P, Cameron RA, Davidson EH (1998) Expression of the Hox gene complex in the indirect development of a sea urchin. Proc Natl Acad Sci U S A 95:13062–13067
Arenas-Mena C, Cameron RA, Davidson EH (2000) Spatial expression of Hox cluster genes in the ontogeny of a sea urchin. Development 127:4631–4643
Arenas-Mena C, Cameron RA, Davidson EH (2006) Hindgut specification and cell-adhesion functions of Sphox11/13b in the endoderm of the sea urchin embryo. Develop Growth Differ 48:463–472
Aronowicz J, Lowe CJ (2006) Hox gene expression in the hemichordate Saccoglossus kowalevskii and the evolution of deuterostome nervous systems. Integr Comp Biol 46(6):890–901
Baughman KW, McDougall C, Cummins SF, Hall M, Degnan BM, Satoh N, Shoguchi E (2014) Genomic organization of Hox and ParaHox clusters in the echinoderm, Acanthaster planci. Genesis 52:952–958
Beck F, Tata F, Chawengsaksophak K (2000) Homeobox genes and gut development. BioEssays 22:431–441
Bienz M (1994) Homeotic genes and positional signalling in the Drosophila viscera. Trends Genet 10(1):22–26
Bromham LD, Degnan BM (1999) Hemichordates and deuterostome evolution: robust molecular phylogenetic support for a hemichordate + echinoderm clade. Evol Dev 1:166–171
Cameron CB, Garey JR, Swalla BJ (2000) Evolution of the chordate body plan: new insights from phylogenetic analyses of deuterostome phyla. Proc Natl Acad Sci U S A 97:4469–4474
Cameron RA, Rowen L, Nesbitt R, Bloom S, Rast JP, Berney K, Arenas-Mena C, Martinez P, Lucas S, Richardson PM, Davidson EH, Peterson KJ, Hood L (2006) Unusual gene order and organization of the sea urchin Hox cluster. J Exp Zool B Mol Dev Evol 306B:45–58
Cisternas P, Byrne M (2009) Expression of Hox4 during development of the pentamerous juvenile sea star, Parvulastra exigua. Dev Genes Evol 219:613–618
Garcia-Fernandez J (2005) The genesis and evolution of homeobox gene clusters. Nat Rev Genet 6:881–892
Hano Y, Hayashi A, Yamaguchi S, Yamaguchi M (2001) Hox genes of the direct-type developing Sea urchin Peronella japonica. Zool Sci 18:353–359
Hara Y, Yamaguchi M, Akasaka K, Nakano H, Nonaka M, Amemiya S (2006) Expression patterns of Hox genes in larvae of the sea lily Metacrinus rotundus. Dev Genes Evol 216:797–809
Holland PWH, Garcia-Fernandez (1996) Hox genes and chordate evolution. Dev Biol 173:382–395
Ikuta T, Saiga H (2005) Organization of Hox genes in ascidians: present, past, and future. Dev Dyn 233:382–389
Irvine SQ, Martindale MQ (2000) Expression patterns of anterior Hox genes in the polychaete Chaetopterus: correlation with morphological boundaries. Dev Biol 217:333–351
Ishii M, Mitsunaga-Nakatsubo K, Kitajima T, Kusunoki S, Shimada H, Akasaka K (1999) Hbox1 and Hbox7 are involved in pattern formation in sea urchin embryos. Develop Growth Differ 41:241–252
Kato S, Tsurumaru S, Taga M, Yamana T, Shibata Y, Ohono K, Fujiwara A, Yamano K, Yoshikuni M (2009) Neuronal peptides induce oocyte maturation and gamete spawning of sea cucumber, Apostichopus japonicus. Dev Biol 326:169–176
Kawazoe Y, Sekimoto T, Araki M, Takagi K, Araki K, Yamamura K (2002) Region-specific gastrointestinal Hox code during murine embryonal gut development. Develop Growth Differ 44:77–84
Krumlauf R (1994) Hox genes in vertebrate development. Cell 78:191–201
Lewis EB (1978) A gene complex controlling segmentation in Drosophila. Nature 276:565–570
Martinez P, Rast JP, Arenas-Mena C, Davidson EH (1999) Organization of an echinoderm Hox gene cluster. Proc Natl Acad Sci U S A 96:1469–1474
McGinnis W, Krumlauf R (1992) Homeobox genes and axial patterning. Cell 68:283–302
Mendez AT, Roig-Lopez JL, Santiago P, Santiago C, Garcia-Arraras JE (2000) Identification of Hox gene sequences in the Sea cucumber Holothuria glaberrima selenka (holothuroidea: echinodermata). Mar Biotechnol (NY) 2(3):231–240
Morris VB, Byrne M (2005) Involvement of Two Hox genes and Otx in echinoderm body-plan morphogenesis in the Sea urchin Holopneustes purpurescens. J Exp Zool B Mol Dev Evol 304B:456–467
Morris VB, Byrne M (2014) Oral–aboral identity displayed in the expression of HpHox3 and HpHox11/13 in the adult rudiment of the sea urchin Holopneustes purpurescens. Dev Genes Evol 224:1–11
Omori A, Akasaka K, Kurokawa D, Amemiya S (2011) Gene expression analysis of Six3, Pax6 and Otx in the early development of the stalked crinoid Metacrinus rotundus. Gene Expr Patterns 11:48–56
Peterson KJ (2003) Isolation of Hox and Parahox genes in the hemichordate Ptychodera flava and the evolution deuterostome Hox genes. Mol Phylogenet Evol 31:1208–1215
Peterson KJ, Cameron RA, Davidson EH (1997) Set-aside cells in maximal indirect development: evolutionary and developmental significance. BioEssays 19:623–631
Peterson KJ, Arenas-Mena C, Davidson EH (2000) The A/P axis in echinoderm ontogeny and evolution: evidence from fossils and molecules. Evol Dev 2:93–101
Popodi E, Kissinger JC, Andrews ME, Raff RA (1996) Sea urchin Hox genes: insights into the ancestral Hox cluster. Mol Biol Evol 13:1078–1086
Roberts DJ, Johnson RL, Burke AC, Nelson CE, Morgan BA (1995) Sonic hedgehog is an endodermal signal inducing BMP-4 and Hox genes during induction and regionalization of the chick hindgut. Development 121:3163–3174
Sakiyama J, Yokouchi Y, Kuroiwa A (2001) HoxA and HoxB cluster genes subdivide the digestive tract into morphological domains during chick development. Mech Dev 101:233–236
Schubert M, Yu J, Holland ND, Escriva H, Laudet V, Holland LZ (2005) Retinoic acid signaling acts via Hox1 to establish the posterior limit of the pharynx in the chordate amphioxus. Development 132:61–73
Sharkey M, Graba Y, Scott MP (1997) Hox genes in evolution: protein surfaces and paralog groups. Trends Genet 13:145–151
Shoguchi E, Harada Y, Numakunai T, Satoh N (2000) Expression of the Otx gene in the ciliary bands during Sea cucumber embryogenesis. Genesis 27:58–63
Tsuchimoto J, Yamaguchi M (2014) Hox expression in the direct-type developing sand dollar Peronella japonica. Dev Dyn 243:1020–1029
Wada H, Satoh N (1994) Details of the evolutionary history from invertebrates to vertebrates, as deduced from the sequences of 18S rDNA. Proc Natl Acad Sci U S A 91:1801–1804
Wada H, Garcia-Fernandez J, Holland PWH (1999) Colinear and segmental expression of amphioxus Hox genes. Dev Biol 213:131–141
Wilson KA, Andrews MA, Raff RA (2005) Dissociation of expression patterns of homeodomain transcription factors in the evolution of developmental mode in the sea urchins Heliocidaris tuberculata and H. erythrogramma. Evol Dev 7:401–415
Yokouchi Y, Sakiyama J, Kuroiwa A (1995) Coordinated expression of Abd-B subfamily genes of the HoxA cluster in the developing digestive tract of chick embryo. Dev Biol 169:76–89
Yoshida W, Tamai A, Yanaka T, Ishida S (2001) Normal development and artificial breeding of sea cucumber (Stichopus japonicus Selenka) from Mutsu Bay. Bull Fac Agric Life Sci Hirosaki Univ 4:16–23 [In Japanese with English summary]
Zakany J, Duboule D (1999) Hox genes and the making of sphincters. Nature 401:761–762
The authors express their thanks to Dr. Michiyasu Yoshikuni for generously providing cubifrin. We also thank Dr. Fred H. Wilt for his advice in preparation and critical reading of the manuscript. This work was supported in part by Grants-in-Aid for Scientific Research (No. 23570248) to Koji Akasaka from the Ministry of Education, Culture, Sports and Technology of Japan.
Conflict of interest
The authors declare that they have no competing interest.
All institutional and national guidelines for the care and use of laboratory animals were followed.
Communicated by Hiroki Nishida
Electronic supplementary material
Below is the link to the electronic supplementary material.
(PDF 4350 kb)
About this article
Cite this article
Kikuchi, M., Omori, A., Kurokawa, D. et al. Patterning of anteroposterior body axis displayed in the expression of Hox genes in sea cucumber Apostichopus japonicus . Dev Genes Evol 225, 275–286 (2015). https://doi.org/10.1007/s00427-015-0510-7
- Anteroposterior axis
- Sea cucumber