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Reporter Analyses Reveal Redundant Enhancers that Confer Robustness on Cis-Regulatory Mechanisms

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Transgenic Ascidians

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1029))

Abstract

Reporter analyses of Hox1 and Brachyury (Bra) genes have revealed examples of redundant enhancers that provide regulatory robustness. Retinoic acid (RA) activates through an RA-response element the transcription of Hox1 in the nerve cord of the ascidian Ciona intestinalis. We also found a weak RA-independent neural enhancer within the second intron of Hox1. The Hox1 gene in the larvacean Oikopleura dioica is also expressed in the nerve cord. The O. dioica genome, however, does not contain the RA receptor-encoding gene, and the expression of Hox1 has become independent of RA. We have found that the upstream sequence of the O. dioica Hox1 was able to activate reporter gene expression in the nerve cord of the C. intestinalis embryo, suggesting that an RA-independent regulatory system in the nerve cord might be common in larvaceans and ascidians. This RA-independent redundant regulatory system may have facilitated the Oikopleura ancestor losing RA signaling without an apparent impact on Hox1 expression domains. On the other hand, vertebrate Bra is expressed in the ventral mesoderm and notochord, whereas its ascidian ortholog is exclusively expressed in the notochord. Fibroblast growth factor (FGF) induces Bra in the ventral mesoderm in vertebrates, whereas it induces Bra in the notochord in ascidians. Disruption of the FGF signal does not completely silence Bra expression in ascidians, suggesting that FGF-dependent and independent enhancers might comprise a redundant regulatory system in ascidians. The existence of redundant enhancers, therefore, provides regulatory robustness that may facilitate the acquisition of new expression domains.

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Acknowledgments

We thank Chikako Imaizumi, Reiko Yoshida, Yutaka Satou, Megumi Koutsuka, and Kazuko Hirayama (NBRP) for the animals. As this review includes our unpublished results, we thank members of our group, Miyuki Kanda, Minami Tagawa, and Adriana Rodriguez-Marí. This work was supported by a Grant-in-Aid for Scientific Research from the Japan Society for the Promotion of Science to SF, and by the grant BFU2016-80601-P from the Ministerio de Economía y Competitividad (Spain) and SGR2014-290 from Generalitat de Catalunya to CC. Our collaborative research was supported by the Heiwa Nakajima Foundation. We also thank Zenji Imoto, Kouki Tanaka, and other members of the Usa Marine Biological Institute of Kochi University for maintenance of the aquarium.

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Authors and Affiliations

  1. Department of Chemistry and Biotechnology, Faculty of Science and Technology, Kochi University, Kochi-shi, Kochi, Japan

    Shigeki Fujiwara

  2. Department de Genètica, Microbiologia i Estadística and Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, Barcelona, Spain

    Cristian Cañestro

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  1. Shigeki Fujiwara
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  2. Cristian Cañestro
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Correspondence to Shigeki Fujiwara .

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Editors and Affiliations

  1. Shimoda Marine Research Center, University of Tsukuba, Shimoda, Shizuoka, Japan

    Yasunori Sasakura

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Fujiwara, S., Cañestro, C. (2018). Reporter Analyses Reveal Redundant Enhancers that Confer Robustness on Cis-Regulatory Mechanisms. In: Sasakura, Y. (eds) Transgenic Ascidians . Advances in Experimental Medicine and Biology, vol 1029. Springer, Singapore. https://doi.org/10.1007/978-981-10-7545-2_7

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