Development Genes and Evolution

, Volume 220, Issue 3–4, pp 107–115 | Cite as

Functional evolution of Ets in echinoderms with focus on the evolution of echinoderm larval skeletons

  • Hiroyuki Koga
  • Mioko Matsubara
  • Haruka Fujitani
  • Norio Miyamoto
  • Miéko Komatsu
  • Masato Kiyomoto
  • Koji Akasaka
  • Hiroshi Wada
Original Article


Convergent evolution of echinoderm pluteus larva was examined from the standpoint of functional evolution of a transcription factor Ets1/2. In sea urchins, Ets1/2 plays a central role in the differentiation of larval skeletogenic mesenchyme cells. In addition, Ets1/2 is suggested to be involved in adult skeletogenesis. Conversely, in starfish, although no skeletogenic cells differentiate during larval development, Ets1/2 is also expressed in the larval mesoderm. Here, we confirmed that the starfish Ets1/2 is indispensable for the differentiation of the larval mesoderm. This result led us to assume that, in the common ancestors of echinoderms, Ets1/2 activates the transcription of distinct gene sets, one for the differentiation of the larval mesoderm and the other for the development of the adult skeleton. Thus, the acquisition of the larval skeleton involved target switching of Ets1/2. Specifically, in the sea urchin lineage, Ets1/2 activated a downstream target gene set for skeletogenesis during larval development in addition to a mesoderm target set. We examined whether this heterochronic activation of the skeletogenic target set was achieved by the molecular evolution of the Ets1/2 transcription factor itself. We tested whether starfish Ets1/2 induced skeletogenesis when injected into sea urchin eggs. We found that, in addition to ectopic induction of mesenchyme cells, starfish Ets1/2 can activate some parts of the skeletogenic pathway in these mesenchyme cells. Thus, we suggest that the nature of the transcription factor Ets1/2 did not change, but rather that some unidentified co-factor(s) for Ets1/2 may distinguish between targets for the larval mesoderm and for skeletogenesis. Identification of the co-factor(s) will be key to understanding the molecular evolution underlying the evolution of the pluteus larvae.


Pluteus Echinoderm Skeleton Ets Starfish 



We thank Kyoko Uchi, Hidekazu Kuwayama, and Hideko Urushihara for their technical assistance of QRT-PCR. We also thank students in Komatsu lab (Toyama University) for their help in collecting brittle stars. This work is supported by Grants-in-Aid for Scientific Research (B) 21370105 to HW.


  1. Amore G, Davidson EH (2006) cis-Regulatory control of cyclophilin, a member of the ETS-DRI skeletogenic gene battery in the sea urchin embryo. Dev Biol 293:555–564CrossRefPubMedGoogle Scholar
  2. Amore G, Yavrouian RG, Peterson KJ, Ransick A, McClay DR, Davidson EH (2003) Spdeadringer, a sea urchin embryo gene required separately in skeletogenic and oral ectoderm gene regulatory networks. Dev Biol 261:55–81CrossRefPubMedGoogle Scholar
  3. Armstrong N, Hardin J, McClay DR (1993) Cell-cell interactions regulate skeleton formation in the sea urchin embryo. Development 119:833–840PubMedGoogle Scholar
  4. Di Bernardo M, Castagnetti S, Bellomonte D, Oliveri P, Melfi R, Palla F, Spinelli G (1999) Spatially restricted expression of PlOtp, a Paracentrotus lividus orthopedia-related homeobox gene, is correlated with oral ectodermal patterning and skeletal morphogenesis in late-cleavage sea urchin embryos. Development 126:2171–2179PubMedGoogle Scholar
  5. Duloquin L, Lhomon G, Gache C (2007) Localized VEGF signaling from ectoderm to mesenchyme cells controls morphogenesis of the sea urchin embryo skeleton. Development 134:2293–2302CrossRefPubMedGoogle Scholar
  6. Ettensohn CA (2009) Lessons from a gene regulatory network: echinoderm skeletogenesis provides insights into evolution, plasticity and morphogenesis. Development 136:11–21CrossRefPubMedGoogle Scholar
  7. Galant R, Carroll SB (2002) Evolution of a transcriptional repression domain in an insect Hox protein. Nature 415:910–913CrossRefPubMedGoogle Scholar
  8. Gao F, Davidson EH (2008) Transfer of a large gene regulatory apparatus to a new developmental address in echinoid evolution. Proc Natl Acad Sci USA 105:6091–6096CrossRefPubMedGoogle Scholar
  9. Guindon S, Gascuel O (2003) A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704CrossRefPubMedGoogle Scholar
  10. Hinman V, Davidson EH (2007) Evolutionary plasticity of developmental gene regulatory network architecture. Proc Natl Acad Sci USA 104:19404–19409CrossRefPubMedGoogle Scholar
  11. Hinman V, Yankura KA, McCauley BS (2009) Evolution of gene regulatory network architectures: examples of subcircuit conservation and plasticity between classes of echinoderms. Biochem Biophys Acta 1789:326–332PubMedGoogle Scholar
  12. Janies D (2001) Phylogenetic relationships of extant echinoderm classes. Can J Zool 79:1232–1250CrossRefGoogle Scholar
  13. Keane TM, Creevey CJ, Pentony MM, Naughton TJ, McInerney JO (2006) Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evol Biol 6:29CrossRefPubMedGoogle Scholar
  14. Kinoshita T, Okazaki K (1984) In vitro study on morphogenesis of sea urchin larval spicule: adhesiveness of cells. Zool Sci 1:433–443Google Scholar
  15. Kitajima T, Urakami H (2000) Differential distribution of spicule matrix proteins in the sea urchin embryo skeleton. Dev Growth Differ 42:295–306CrossRefPubMedGoogle Scholar
  16. Kurokawa D, Kitajima T, Mitsunaga-Nakatsubo K, Amemiya S, Shimada H, Akasaka K (1999) HpEts, an ets-related transcription factor implicated in primary mesenchyme cell differentiation in the sea urchin embryo. Mech Dev 80:41–52CrossRefPubMedGoogle Scholar
  17. Lemaire P, Garrett N, Gurdon JB (1995) Expression cloning of Siamois, a Xenopus homeobox gene expressed in dorsal vegetal cells of blastulae and able to induce a complete secondary axis. Cell 81:85–94CrossRefPubMedGoogle Scholar
  18. Littlewood DTJ, Smith AB, Clough KA, Emson RH (1997) The interrelationships of the echinoderm classes: morphological and molecular evidence. Biol J Linn Soc Lond 61:409–438CrossRefGoogle Scholar
  19. Lynch VJ, Tanzer A, Wang Y, Leung FC, Gellersen B, Emera D, Wagner GP (2008) Adaptive changes in the transcription factor HoxA-11 are essential for the evolution of pregnancy in mammals. Proc Natl Acad Sci USA 105:14928–14933CrossRefPubMedGoogle Scholar
  20. Maruyama YK (1980) Artificial induction of oocyte maturation and development in the sea cucumbers Holothuria leucospilota and Holothuria pardalis. Biol Bull 158:339–348CrossRefGoogle Scholar
  21. McCauley BS, Weideman EP, Hinman VF (2010) A conserved gene regulatory network subcircuit drives different developmental fates in the vegetal pole of highly divergent echinoderm embryos. Dev Biol 340:200–208CrossRefPubMedGoogle Scholar
  22. Paul CRC, Smith AB (1984) The early radiation and phylogeny of echinoderms. Biol Rev 59:443–481CrossRefGoogle Scholar
  23. Ronshaugen M, McGinnis N, McGinnis W (2002) Hox protein mutation and macroevolution of the insect body plan. Nature 415:914–917CrossRefPubMedGoogle Scholar
  24. Röttinger E, Besnardea L, Lepage T (2003) A Raf/MEK/ERK signaling pathway is required for development of the sea urchin embryo micromere lineage through phosphorylation of the transcription factor Ets. Development 131:1075–1087CrossRefGoogle Scholar
  25. Röttinger E, Saudemont A, Duboc V, Besnardeau L, McClay D, Lepage T (2008) FGF signals guide migration of mesenchymal cells, control skeletal morphogenesis and regulate gastrulation during sea urchin development. Development 135:353–365CrossRefPubMedGoogle Scholar
  26. Sharma T, Ettensohn CA (2010) Activation of the skeletogenic gene regulatory netwrok in the early sea urchin embryo. Development 137:1149–1157CrossRefPubMedGoogle Scholar
  27. Shoguchi E, Satoh N, Marukyama YK (2000) A starfish homolog of mouse T-brain-1 is expressed in the archenteron of Asterina pectinifera embryos: Possible involvement of two T-box genes in starfish gastrulation. Dev Growth Differ 42:61–68CrossRefPubMedGoogle Scholar
  28. Smith J, Davidson EH (2008) A new method, using cis-regulatory control, for blocking embryonic gene expression. Dev Biol 318:360–365CrossRefPubMedGoogle Scholar
  29. Sweet H, Amemiya S, Ransick A, Minokawa T, McClay DR, Wikramanayake A, Kuraishi R, Kiyomoto M, Nishida H, Henry J (2004) Blastomere isolation and transplantation. In: Ettensohn CA, Wessel GM, Wray GA (eds) Development of sea urchins, ascidianas, and other invertebrate deuterostomes: experimental approaches. Elsevier Academic Press, San DiegoGoogle Scholar
  30. Wada H, Satoh N (1994) Phylogenetic relationships among extant classes of echinoderms, as inferred from sequences of 18S rDNA, coincide with relationships deduced from the fossil records. J Mol Evol 38:41–49CrossRefPubMedGoogle Scholar
  31. Yajima M (2007) A switch in the cellular basis of skeletogenesis in late-stage sea urchin larvae. Dev Biol 307:272–281CrossRefPubMedGoogle Scholar
  32. Yamashita M (1985) Embryonic development of the brittle-star Amphipholis kochii in laboratory culture. Biol Bull 169:131–142CrossRefGoogle Scholar
  33. Yasuo H, Satoh N (1994) An ascidian homolog of the mouse Brachyury (T) gene is expressed exclusively in notochord cells at fate restricted stage. Dev Growth Differ 36:9–18CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Hiroyuki Koga
    • 1
  • Mioko Matsubara
    • 1
    • 2
  • Haruka Fujitani
    • 1
  • Norio Miyamoto
    • 1
  • Miéko Komatsu
    • 3
  • Masato Kiyomoto
    • 4
  • Koji Akasaka
    • 5
  • Hiroshi Wada
    • 1
  1. 1.Graduate School of Life and Environmental SciencesUniversity of TsukubaTsukubaJapan
  2. 2.Seto Marine Biological Laboratory, FSERCKyoto University459 ShirahamaJapan
  3. 3.Department of Biology, Faculty of ScienceToyama UniversityToyamaJapan
  4. 4.Tateyama Marine Laboratory, Marine Coastal Research CenterOchanomizu UniversityTateyamaJapan
  5. 5.Misaki Marine Biological Station, Graduate School of ScienceUniversity of TokyoMisakiJapan

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