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First published online 13 May 2009
doi: 10.1242/dev.028530


Development 136, 2005-2014 (2009)
Published by The Company of Biologists 2009


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Evolutionary origins of blastoporal expression and organizer activity of the vertebrate gastrula organizer gene lhx1 and its ancient metazoan paralog lhx3

Yuuri Yasuoka1, Masaaki Kobayashi2, Daisuke Kurokawa3, Koji Akasaka3, Hidetoshi Saiga2 and Masanori Taira1,*

1 Department of Biological Sciences, Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan.
2 Department of Biological Sciences, Graduate School of Science and Engineering, Tokyo Metropolitan University, 1-1 Minamiohsawa, Hachiohji, Tokyo 192-0397, Japan.
3 Misaki Marine Biological Station, Graduate School of Science, University of Tokyo, 1024 Koajiro, Misaki, Miura Kanagawa, 238-0225, Japan.

* Author for correspondence (e-mail: m_taira{at}biol.s.u-tokyo.ac.jp)

Accepted 8 April 2009

Expression of the LIM homeobox gene lhx1 (lim1) is specific to the vertebrate gastrula organizer. Lhx1 functions as a transcriptional regulatory core protein to exert `organizer' activity in Xenopus embryos. Its ancient paralog, lhx3 (lim3), is expressed around the blastopore in amphioxus and ascidian, but not vertebrate, gastrulae. These two genes are thus implicated in organizer evolution, and we addressed the evolutionary origins of their blastoporal expression and organizer activity. Gene expression analysis of organisms ranging from cnidarians to chordates suggests that blastoporal expression has its evolutionary root in or before the ancestral eumetazoan for lhx1, but possibly in the ancestral chordate for lhx3, and that in the ascidian lineage, blastoporal expression of lhx1 ceased, whereas endodermal expression of lhx3 has persisted. Analysis of organizer activity using Xenopus embryos suggests that a co-factor of LIM homeodomain proteins, Ldb, has a conserved function in eumetazoans to activate Lhx1, but that Lhx1 acquired organizer activity in the bilaterian lineage, Lhx3 acquired organizer activity in the deuterostome lineage and ascidian Lhx3 acquired a specific transactivation domain to confer organizer activity on this molecule. Knockdown analysis using cnidarian embryos suggests that Lhx1 is required for chordin expression in the blastoporal region. These data suggest that Lhx1 has been playing fundamental roles in the blastoporal region since the ancestral eumetazoan arose, that it contributed as an `original organizer gene' to the evolution of the vertebrate gastrula organizer, and that Lhx3 could be involved in the establishment of organizer gene networks.

Key words: Evolution, Lhx1, Lhx3, Nematostella, Spemann-Mangold organizer, Xenopus


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