Isolation and characterization of two T-box genes from sponges, the phylogenetically oldest metazoan taxon

Adell, Teresa; Grebenjuk, Vladislav A.; Wiens, Matthias; Müller, Wernér E.G.

doi:10.1007/s00427-003-0345-5

Cited by 56 publications

(67 citation statements)

References 77 publications

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“…S1). This result supports the notion that Brachyury is the most ancient member of the T-box family (11,13). Moreover, fungal, and especially filasterean, Brachyury genes have most of the T-box key DNA-binding and dimerization amino acids, as well as conserved exclusive amino acid motifs of the Brachyury class (Fig.…”

Section: Resultssupporting

confidence: 86%

“…Previous studies have identified T-box genes in nonbilaterian metazoans (11)(12)(13)(14). This knowledge has enabled a reconstruction of the Urmetazoan T-box complement, which putatively included three classes (Tbx4/5, Brachyury, and a putative Tbx1/15/20), with other classes being added in a stepwise manner through the evolution of metazoans.…”

Section: Resultsmentioning

confidence: 99%

“…With only a few exceptions (8), all classes of T-box genes are widespread among bilaterian animals, with a handful being identified and studied in nonbilaterian metazoans, such as cnidarians (5,9), ctenophores (7,10), and sponges (11)(12)(13)(14). T-box genes were initially thought to be specific to metazoans (13,15), but two recent studies revealed the presence of T-box genes in nonmetazoan lineages (14,16), including the unicellular filose amoeba Capsaspora owczarzaki, a close relative of animals, and the chytrid fungus Spizellomyces punctatus.…”

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confidence: 99%

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Early evolution of the T-box transcription factor family

Sebé-Pedrós

Ariza-Cosano

Weirauch

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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Developmental transcription factors are key players in animal multicellularity, being members of the T-box family that are among the most important. Until recently, T-box transcription factors were thought to be exclusively present in metazoans. Here, we report the presence of T-box genes in several nonmetazoan lineages, including ichthyosporeans, filastereans, and fungi. Our data confirm that Brachyury is the most ancient member of the T-box family and establish that the T-box family diversified at the onset of Metazoa. Moreover, we demonstrate functional conservation of a homolog of Brachyury of the protist Capsaspora owczarzaki in Xenopus laevis. By comparing the molecular phenotype of C. owczarzaki Brachyury with that of homologs of early branching metazoans, we define a clear difference between unicellular holozoan and metazoan Brachyury homologs, suggesting that the specificity of Brachyury emerged at the origin of Metazoa. Experimental determination of the binding preferences of the C. owczarzaki Brachyury results in a similar motif to that of metazoan Brachyury and other T-box classes. This finding suggests that functional specificity between different T-box classes is likely achieved by interaction with alternative cofactors, as opposed to differences in binding specificity.origin multicellularity | premetazoan evolution | subfunctionalization | Porifera | Holozoa T ranscriptional regulation is a central aspect of animal development. Thus, deciphering the early evolution of metazoan transcription factors is vital for achieving a better understanding of the origin of animals. The T-box family of genes is among the most important developmental transcription factors present in Metazoa. This family is characterized by an evolutionary conserved DNA-binding domain of 180-200 amino acids, known as the T-box domain (1-3). Brachyury is the founding and best-characterized member of the T-box family, with well-established roles in blastopore specification, mesoderm differentiation and, in chordates, notochord formation (4-6). It has been hypothesized that the ancestral role of Brachyury was primarily that of blastopore determination and gastrulation (5, 7).Other T-box classes include Tbx4/5, Tbx6, Tbx2/3, Eomes, and Tbx1/15/20. With only a few exceptions (8), all classes of T-box genes are widespread among bilaterian animals, with a handful being identified and studied in nonbilaterian metazoans, such as cnidarians (5, 9), ctenophores (7, 10), and sponges (11-14). T-box genes were initially thought to be specific to metazoans (13, 15), but two recent studies revealed the presence of T-box genes in nonmetazoan lineages (14, 16), including the unicellular filose amoeba Capsaspora owczarzaki, a close relative of animals, and the chytrid fungus Spizellomyces punctatus. T-box genes were not identified in any other sequenced eukaryote, suggesting that T-box genes were secondarily lost in choanoflagellates (both in unicellular and colonial species) and most fungi. Interestingly, one of the T-box genes identified in C. ow...

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Section: Resultssupporting

confidence: 86%

Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

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Early evolution of the T-box transcription factor family

Sebé-Pedrós

Ariza-Cosano

Weirauch

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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“…This toolkit has been suggested to be based on genes required for signaling and regulation (44) and, more specifically, homeotic genes (45,46), which direct the building of multicellular bodies according to a master plan through genetic regulation. We propose an expanded developmental toolkit that includes alternative splicing, acting especially on genes encoding for intrinsically disordered proteins, which, as we have shown, are predominantly involved in signaling and regulation.…”

Section: Discussionmentioning

confidence: 99%

“…We propose an expanded developmental toolkit that includes alternative splicing, acting especially on genes encoding for intrinsically disordered proteins, which, as we have shown, are predominantly involved in signaling and regulation. Indeed, developmental regulation genes have been shown to generate isoforms through alternative splicing: In a particular example, a T-box gene of a sponge, considered the earliest example of metazoans, has been shown to produce isoforms through alternative splicing that affect phosphorylation and glycosylation states, which, in turn, affect gene regulation (46). The combination of these mechanisms also could have facilitated explosive speciation events in the evolutionary history of multicellular organisms, by tolerating multiple mutations that led to changes in regulation and in signaling networks.…”

Section: Discussionmentioning

confidence: 99%

Alternative splicing in concert with protein intrinsic disorder enables increased functional diversity in multicellular organisms

Romero

Zaidi

Fang

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

429

387

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Alternative splicing of pre-mRNA generates two or more protein isoforms from a single gene, thereby contributing to protein diversity. Despite intensive efforts, an understanding of the protein structure-function implications of alternative splicing is still lacking. Intrinsic disorder, which is a lack of equilibrium 3D structure under physiological conditions, may provide this understanding. Intrinsic disorder is a common phenomenon, particularly in multicellular eukaryotes, and is responsible for important protein functions including regulation and signaling. We hypothesize that polypeptide segments affected by alternative splicing are most often intrinsically disordered such that alternative splicing enables functional and regulatory diversity while avoiding structural complications. We analyzed a set of 46 differentially spliced genes encoding experimentally characterized human proteins containing both structured and intrinsically disordered amino acid segments. We show that 81% of 75 alternatively spliced fragments in these proteins were associated with fully (57%) or partially (24%) disordered protein regions. Regions affected by alternative splicing were significantly biased toward encoding disordered residues, with a vanishingly small P value. A larger data set composed of 558 SwissProt proteins with known isoforms produced by 1,266 alternatively spliced fragments was characterized by applying the PONDR VSL1 disorder predictor. Results from prediction data are consistent with those obtained from experimental data, further supporting the proposed hypothesis. Associating alternative splicing with protein disorder enables the time-and tissue-specific modulation of protein function needed for cell differentiation and the evolution of multicellular organisms.evolution ͉ natively unfolded ͉ intrinsically unstructured ͉ protein structure T he splicing of pre-mRNA (1) was first described in 1977. Soon thereafter, Gilbert (2) coined the terms ''intron'' (intragenic region) and ''exon'' (expressed region) for the noncoding and coding regions, respectively. Alternative splicing occurs when different mRNAs are assembled from a single gene by joining exons in different ways. Alternative splicing is proposed to generate complexity in multicellular eukaryotes by increasing protein diversity, and thus proteome size, from a relatively small number of genes (3). Estimates indicate that between 35 and 60% of human genes yield protein isoforms by means of alternatively spliced (AS) mRNA (4). Furthermore, complexity in higher organisms is also brought about by signaling and regulatory networks that enable robustness (5). The importance of alternative splicing as a regulatory process (3, 6) has been highlighted by the high occurrence of such splicing in the pre-mRNAs of regulatory and signaling proteins (7).Alternative splicing can bolster organism complexity, not only by effectively increasing proteome size and regulatory and signaling network complexity, but also by doing so in a time-and tissue-specific manner, supporting ...

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Spatial and Temporal Expression Patterns in Animals

Müller

2006

Encyclopedia of Molecular Cell Biology and Molecular Medicine

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Isolation and characterization of two T-box genes from sponges, the phylogenetically oldest metazoan taxon

Cited by 56 publications

References 77 publications

Early evolution of the T-box transcription factor family

Early evolution of the T-box transcription factor family

Alternative splicing in concert with protein intrinsic disorder enables increased functional diversity in multicellular organisms

Spatial and Temporal Expression Patterns in Animals

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