Functional Brachyury Binding Sites Establish a Temporal Read-out of Gene Expression in the Ciona Notochord

Lavanya Katikala, Hitoshi Aihara, Yale J. Passamaneck, Stefan Gazdoiu, Diana S. José-Edwards, Jamie E. Kugler, Izumi Oda-Ishii, Janice H. Imai, Yutaka Nibu, Anna Di Gregorio

Research output: Contribution to journalArticle

Abstract

The appearance of the notochord represented a milestone in Deuterostome evolution. The notochord is necessary for the development of the chordate body plan and for the formation of the vertebral column and numerous organs. It is known that the transcription factor Brachyury is required for notochord formation in all chordates, and that it controls transcription of a large number of target genes. However, studies of the structure of the cis-regulatory modules (CRMs) through which this control is exerted are complicated in vertebrates by the genomic complexity and the pan-mesodermal expression territory of Brachyury. We used the ascidian Ciona, in which the single-copy Brachyury is notochord-specific and CRMs are easily identifiable, to carry out a systematic characterization of Brachyury-downstream notochord CRMs. We found that Ciona Brachyury (Ci-Bra) controls most of its targets directly, through non-palindromic binding sites that function either synergistically or individually to activate early- and middle-onset genes, respectively, while late-onset target CRMs are controlled indirectly, via transcriptional intermediaries. These results illustrate how a transcriptional regulator can efficiently shape a shallow gene regulatory network into a multi-tiered transcriptional output, and provide insights into the mechanisms that establish temporal read-outs of gene expression in a fast-developing chordate embryo.

Original languageEnglish (US)
Article numbere1001697
JournalPLoS Biology
Volume11
Issue number10
DOIs
StatePublished - 2013

Fingerprint

Notochord
Chordata
Gene expression
binding sites
Binding Sites
Gene Expression
gene expression
transcription factors
Genes
Ascidiacea
spine (bones)
embryo (animal)
genes
transcription (genetics)
Urochordata
vertebrates
Gene Regulatory Networks
genomics
Transcription
Vertebrates

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Immunology and Microbiology(all)
  • Neuroscience(all)

Cite this

Katikala, L., Aihara, H., Passamaneck, Y. J., Gazdoiu, S., José-Edwards, D. S., Kugler, J. E., ... Di Gregorio, A. (2013). Functional Brachyury Binding Sites Establish a Temporal Read-out of Gene Expression in the Ciona Notochord. PLoS Biology, 11(10), [e1001697]. https://doi.org/10.1371/journal.pbio.1001697

Functional Brachyury Binding Sites Establish a Temporal Read-out of Gene Expression in the Ciona Notochord. / Katikala, Lavanya; Aihara, Hitoshi; Passamaneck, Yale J.; Gazdoiu, Stefan; José-Edwards, Diana S.; Kugler, Jamie E.; Oda-Ishii, Izumi; Imai, Janice H.; Nibu, Yutaka; Di Gregorio, Anna.

In: PLoS Biology, Vol. 11, No. 10, e1001697, 2013.

Research output: Contribution to journalArticle

Katikala, L, Aihara, H, Passamaneck, YJ, Gazdoiu, S, José-Edwards, DS, Kugler, JE, Oda-Ishii, I, Imai, JH, Nibu, Y & Di Gregorio, A 2013, 'Functional Brachyury Binding Sites Establish a Temporal Read-out of Gene Expression in the Ciona Notochord', PLoS Biology, vol. 11, no. 10, e1001697. https://doi.org/10.1371/journal.pbio.1001697
Katikala L, Aihara H, Passamaneck YJ, Gazdoiu S, José-Edwards DS, Kugler JE et al. Functional Brachyury Binding Sites Establish a Temporal Read-out of Gene Expression in the Ciona Notochord. PLoS Biology. 2013;11(10). e1001697. https://doi.org/10.1371/journal.pbio.1001697
Katikala, Lavanya ; Aihara, Hitoshi ; Passamaneck, Yale J. ; Gazdoiu, Stefan ; José-Edwards, Diana S. ; Kugler, Jamie E. ; Oda-Ishii, Izumi ; Imai, Janice H. ; Nibu, Yutaka ; Di Gregorio, Anna. / Functional Brachyury Binding Sites Establish a Temporal Read-out of Gene Expression in the Ciona Notochord. In: PLoS Biology. 2013 ; Vol. 11, No. 10.
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