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TRF2 and the Evolution of the Bilateria Downloaded from genesdev.cshlp.org on September 26, 2021 - Published by Cold Spring Harbor Laboratory Press HYPOTHESIS TRF2 and the evolution of the bilateria Sascha H.C. Duttke,1 Russell F. Doolittle,1,2 Yuan-Liang Wang,1 and James T. Kadonaga1 1Section of Molecular Biology, University of California at San Diego, La Jolla, California 92093, USA; 2Department of Chemistry and Biochemistry, University of California at San Diego, La Jolla, California 92093, USA The development of a complex body plan requires a di- addition, TFIIA has been found to enhance the binding of versity of regulatory networks. Here we consider the TBP to DNA. TBP (as well as the TATA box), TFIIB, TFIIE, concept of TATA-box-binding protein (TBP) family pro- TFIIS, and Pol II are present in Archaea and eukaryotes teins as ‘‘system factors’’ that each supports a distinct set (for review, see Grohmann and Werner 2011). Moreover, of transcriptional programs. For instance, TBP activates many eukaryotes contain TBP as well as TBP-related TATA-box-dependent core promoters, whereas TBP-related factors (TRFs). factor 2 (TRF2) activates TATA-less core promoters that Here we consider the concept that TBP family proteins are dependent on a TCT or downstream core promoter function as ‘‘system factors’’ that support distinct transcrip- element (DPE) motif. These findings led us to investigate tional programs. TBP occurs in Archaea and eukaryotes, the evolution of TRF2. TBP occurs in Archaea and and TBP-related factor 1 (TRF1), TRF2, and TRF3 (for eukaryotes, but TRF2 evolved prior to the emergence reviews, see Goodrich and Tjian 2010; Akhtar and Veenstra of the bilateria and subsequent to the evolutionary split 2011) evolved independently via duplications of the between bilaterians and nonbilaterian animals. Unlike TBP gene. TRF1 has been found in insects, TRF3 appears TBP, TRF2 does not bind to the TATA box and could thus to be present mainly in vertebrates, and TRF2 has been function as a new system factor that is largely indepen- generally thought to be present in all metazoans (Dantonel dent of TBP. We postulate that this TRF2-based system et al. 1999; Goodrich and Tjian 2010; Akhtar and Veenstra served as the foundation for new transcriptional pro- 2011). Except for TRF2, members of the TBP family of grams, such as those involved in triploblasty and body proteins exhibit sequence-specific binding to DNA. plan development, that facilitated the evolution of Here we focus on two RNA Pol II transcriptional pro- bilateria. grams that are driven by the TBP or TRF2 system factors. We then analyze the characteristics and emergence of Supplemental material is available for this article. TRF2 and propose a role for the TRF2-based system in the evolution of the bilateria, triploblastic animals that The development of complex body plans requires a di- have bilateral symmetry and represent ;99% of all living verse range of transcriptional programs. The regulation of animals. these programs is often analyzed at the level of sequence- System factors function via the core promoter, which is specific DNA-binding proteins that interact with enhancers the segment of DNA that is sufficient to direct accurate and other important DNA elements. Indeed, sequence- initiation of transcription (for example, see Kadonaga 2012 specific factors, such as those that are used to create and references therein). The signals that regulate transcrip- induced pluripotent stem cells, play a critical and dom- tion must ultimately pass through the core promoter, and inant role in establishing the state of a cell. However, at it thus serves as the ‘‘gateway to transcription.’’ The RNA the same time, it might be imagined that the most far- Pol II core promoter is diverse in terms of its structure and reaching changes in an organism would involve alter- function, and its activity is regulated by the presence or ations of the basal transcriptional machinery. absence of specific DNA sequence motifs. These core In eukaryotes, the basic transcription reaction involves promoter elements include the TATA box, initiator (Inr), an RNA polymerase along with auxiliary factors that polypyrimidine initiator (TCT), and downstream core are required for accurate and efficient transcription. For promoter element (DPE). There are no universal core pro- transcription of the subset of promoters that contain moter motifs. TBP family system factors can act through a TATA box, RNA polymerase II (Pol II) functions with specific core promoter motifs, although in a manner that transcription factor IIB (TFIIB), TFIID, TFIIE, TFIIF, and may or may not involve direct binding to those DNA TFIIH (for review, see Thomas and Chiang 2006). TFIID sequence elements. comprises the TATA-box-binding protein (TBP) along with other TBP-associated factors known as TAFs. In Ó 2014 Duttke et al. This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue [Keywords: RNA polymerase II; TRF2; TBP; evolution; bilateria; publication date (see http://genesdev.cshlp.org/site/misc/terms.xhtml). regulatory systems] After six months, it is available under a Creative Commons License Corresponding author: [email protected] (Attribution-NonCommercial 4.0 International), as described at http:// Article is online at http://www.genesdev.org/cgi/doi/10.1101/gad.250563.114. creativecommons.org/licenses/by-nc/4.0/. GENES & DEVELOPMENT 28:2071–2076 Published by Cold Spring Harbor Laboratory Press; ISSN 0890-9369/14; www.genesdev.org 2071 Downloaded from genesdev.cshlp.org on September 26, 2021 - Published by Cold Spring Harbor Laboratory Press Duttke et al. Distinct transcriptional programs with TBP vs. TRF2 TRF2 (also known as TLP, TRP, TLF, and TBPL1) system factors (Maldonado 1999; Moore et al. 1999; Ohbayashi et al. 1999; Rabenstein et al. 1999; Teichmann et al. 1999) TBP can activate transcription via the TATA-box motif, contains two domains that are similar to those in TBP and and both TBP and the TATA box are conserved in Archaea interacts with TFIIA and TFIIB, as does TBP (Fig. 1A; and eukaryotes (Kosa et al. 1997; Patikoglou et al. 1999). Supplemental Fig. S1). In addition, the overall structures TBP binds to the TATA box with its core region, which of TBP and TRF2 are predicted to be conserved (Dantonel consists of two structurally repeated domains that form et al. 1999). Unlike TBP, however, TRF2 does not bind to a saddle-shaped structure. For the purposes of this dis- the TATA box and does not exhibit sequence-specific cussion, it is important to remember that the binding of binding to DNA in the presence or absence of all possible TBP to the TATA box includes the participation of two combinations of TFIIA and TFIIB (for example, see Wang pairs of conserved Phe residues (F193–F210 and F284–F301 et al. 2014). in human TBP) whose side chains intercalate between the TRF2, but not TBP, is required for transcription of core first and last base pairs of the TATA motif and kink the promoters, such as those of most ribosomal protein genes, DNA (Fig. 1A; Supplemental Fig. S1; Kim et al. 1993a,b). that lack a TATA box and are dependent on the TCT This interaction is highly conserved (Patikoglou et al. sequence motif (Wang et al. 2014). On the other hand, 1999). In addition, TBP binds to other basal transcription TBP, but not TRF2, is essential for the transcription of factors such as TFIIA and TFIIB as well as TAFs (for review, TATA-dependent core promoters. These findings revealed see Thomas and Chiang 2006). that TRF2, but not TBP, supports a TCT-dependent RNA Pol II transcription program that is dedicated to the pro- duction of ribosomal proteins. Notably, the TRF2-TCT transcriptional program complements the RNA Pol I and RNA Pol III transcriptional programs that are dedi- cated to the synthesis of rRNAs and tRNAs (Supplemen- tal Fig. S2). In addition, transcription from DPE-dependent core promoters requires TRF2 (Kedmi et al. 2014) but not TBP (Hsu et al. 2008). These TATA-less DPE-containing promoters include those of most of the homeotic genes (Juven-Gershon et al. 2008) as well as of many genes that are regulated by the Dorsal transcription factor (Zehavi et al. 2014). It is important to note that the DPE motif functions with the Inr element but not with the TCT motif (Parry et al. 2010; Kadonaga 2012). Thus, the TCT- dependent promoters are different from the DPE- dependent promoters. Hence, for RNA Pol II, these studies have revealed three distinct transcriptional pro- grams: the TBP-based transcription of TATA-dependent core promoters and the TRF2-based transcription of TCT-dependent core promoters and DPE-dependent core promoters. TRF2 evolved prior to the emergence of the bilateria The identification of distinct TBP- and TRF2-based tran- scriptional programs led us to investigate the evolution of TRF2. We found paralogs of TBP in several protist lineages and in plants and animals but not in yeast. It Figure 1. Evolution of the TRF2-based transcription system was necessary, however, to employ a distinct and reliable facilitated the emergence of complex animal body plans. signature for TRF2. To this end, we generated an align- (A) Alignment of TBP and TBP-related factors from Archaea ment of TBP and TBP-related factors (Fig. 1A; Supple- (a), Drosophila (d), and humans (h). The TATA-box-interacting mental Fig. S1). Many features, such as the TFIIA and Phe residues that are mutated in TRF2 are indicated with TFIIB interaction sites as well as most of the TATA-box- arrows. The amino acid numbers are those of human TBP. The interacting amino acid residues, are conserved among full amino acid sequences of the repeated core domains of these TBP and TBP-related factors.
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