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; Gregorio, Anna Di

doi:10.1371/journal.pbio.1001697

Cited by 46 publications

(49 citation statements)

References 69 publications

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“…Our results clearly illustrate that by manipulating Zld binding sites, the timing of NE gene activation can be altered. Temporal regulation by transcription factor binding sites has also been shown in Ciona where the number of Brachyury binding sites governs the timing of notochord gene expression [29]. …”

Section: Resultsmentioning

confidence: 99%

Zelda Potentiates Morphogen Activity by Increasing Chromatin Accessibility

et al. 2014

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Summary Zygotic genome activation (ZGA) is a major genome programming event whereby the cells of the embryo begin to adopt specified fates. Experiments in Drosophila and zebrafish revealed that ZGA depends on transcription factors that provide large-scale control of gene expression by direct and specific binding to gene regulatory sequences [1–5]. Zelda (Zld) plays such a role in the Drosophila embryo, where it was shown to control the action of patterning signals [1, 2], however the mechanisms underlying this effect remain largely unclear. A recent model proposed that Zld binding sites act as quantitative regulators of the spatiotemporal expression of genes activated by Dorsal (Dl), the morphogen that patterns the dorsoventral (DV) axis [6]. We test this model experimentally, using enhancers of brinker (brk) and short gastrulation (sog), both of which are directly activated by Dl, but at different concentration thresholds [7–9]. In agreement with the model, we show that there is a clear positive correlation between the number of Zld binding sites and the spatial domain of enhancer activity. Likewise, the timing of expression could be advanced or delayed. We present evidence that Zld facilitates binding of Dl to regulatory DNA, and that this is associated with increased chromatin accessibility. Importantly, the change in chromatin accessibility is strongly correlated with the change in Zld binding, but not Dl. We propose that the ability of genome activators to facilitate read-out of transcriptional input is key to widespread transcriptional induction during ZGA.

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Section: Resultsmentioning

confidence: 99%

Zelda Potentiates Morphogen Activity by Increasing Chromatin Accessibility

et al. 2014

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“…Foxa.a, Zic-r.b and Fgf signaling combinatorially activate Brachyury at the 44-cell stage (Imai et al, 2002a(Imai et al, , 2006Yagi et al, 2004;Yasuo and Hudson, 2007). Brachyury encodes a key transcription factor for specifying the notochord, and activates notochord-specific genes directly and indirectly (Chiba et al, 2009;Hotta et al, 2000;Katikala et al, 2013;Kubo et al, 2010;Takahashi et al, 1999). Indeed, in another ascidian species, Halocynthia roretzi, overlapping expression of Foxa and ZicN (an ortholog of Zic-r.b) and activation of Ets by Fgf signaling have been reported to be required for Brachyury expression (Kumano et al, 2006;Matsumoto et al, 2007;Miya and Nishida, 2003).…”

Section: Introductionmentioning

confidence: 99%

Differential temporal control of Foxa.a and Zic-r.b specifies brain versus notochord fate in the ascidian embryo

Ikeda

Satou

2016

Development

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In embryos of an invertebrate chordate, Ciona intestinalis, two transcription factors, Foxa.a and Zic-r.b, are required for specification of the brain and the notochord, which are derived from distinct cell lineages. In the brain lineage, Foxa.a and Zic-r.b are expressed with no temporal overlap. In the notochord lineage, Foxa.a and Zic-r.b are expressed simultaneously. In the present study, we found that the temporally non-overlapping expression of Foxa.a and Zic-r.b in the brain lineage was regulated by three repressors: Prdm1-r.a (formerly called BZ1), Prdm1-r.b (BZ2) and Hes.a. In morphant embryos of these three repressor genes, Foxa.a expression was not terminated at the normal time, and Zic-r.b was precociously expressed. Consequently, Foxa.a and Zic-r.b were expressed simultaneously, which led to ectopic activation of Brachyury and its downstream pathways for notochord differentiation. Thus, temporal controls by transcriptional repressors are essential for specification of the two distinct fates of brain and notochord by Foxa.a and Zic-r.b. Such a mechanism might enable the repeated use of a limited repertoire of transcription factors in developmental gene regulatory networks.

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“…Of these, some are direct targets of Bra, with earlier-activated targets containing more Bra binding sites in upstream cis-regulatory sequences than targets activated later, which typically contain only one binding site (Katikala et al 2013 ). There are also indirect targets of Bra, mediated by transcription factors that are direct Bra targets (Katikala et al 2013 ). All in all, the notochord genes constitute a diverse group of proteins involved in several steps of notochord morphogenesis and differentiation.…”

Section: Notochord Formationmentioning

confidence: 99%