Early evolution of metazoan transcription factors

Degnan, Bernard M.; Vervoort, Michel; Larroux, Claire; Richards, Gemma S.

doi:10.1016/j.gde.2009.09.008

Cited by 130 publications

(135 citation statements)

References 70 publications

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“…Similarly, genome data from unicellular metazoan-related lineages is pushing back the times of origin of many gene families formerly believed to be metazoan specific to well into the Proterozoic. Such is the case, for example, of tyrosine kinases (14,50,51), some transcription factors (12,52), membrane-associated guanylate kinases (53), or cadherines (13). The integrin-mediated signaling and adhesion machinery here presented add another striking example to this pattern and suggest that some of these protein families may have emerged even earlier in eukaryote evolution before the divergence of opisthokonts.…”

Section: Discussionmentioning

confidence: 75%

Ancient origin of the integrin-mediated adhesion and signaling machinery

Sebé-Pedrós

Roger

Lang

et al. 2010

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

226

276

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The evolution of animals (metazoans) from their unicellular ancestors required the emergence of novel mechanisms for cell adhesion and cell-cell communication. One of the most important cell adhesion mechanisms for metazoan development is integrinmediated adhesion and signaling. The integrin adhesion complex mediates critical interactions between cells and the extracellular matrix, modulating several aspects of cell physiology. To date this machinery has been considered strictly metazoan specific. Here we report the results of a comparative genomic analysis of the integrin adhesion machinery, using genomic data from several unicellular relatives of Metazoa and Fungi. Unexpectedly, we found that core components of the integrin adhesion complex are encoded in the genome of the apusozoan protist Amastigomonas sp., and therefore their origins predate the divergence of Opisthokonta, the clade that includes metazoans and fungi. Furthermore, our analyses suggest that key components of this apparatus have been lost independently in fungi and choanoflagellates. Our data highlight the fact that many of the key genes that had formerly been cited as crucial for metazoan origins have a much earlier origin. This underscores the importance of gene cooption in the unicellular-to-multicellular transition that led to the emergence of the Metazoa.cell adhesion | lateral gene transfer | metazoan origins | multicellularity

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Section: Discussionmentioning

confidence: 75%

Ancient origin of the integrin-mediated adhesion and signaling machinery

Sebé-Pedrós

Roger

Lang

et al. 2010

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

226

276

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“…Indeed, research into the origins of animal multicellularity have been transformed by investigating their closest unicellular ancestors including choanoflagellates and others (King et al 2008;Fairclough et al 2013;SebePedros et al 2013;Alegado and King 2014). Gene family expansion and novel protein domain organization are observed in metazoans and embryophytes and associated with some key innovations Degnan et al 2009;Srivastava et al 2010). However, wholesale changes in numbers or types of protein families and domain structures need not underlie the innovations required to achieve multicellularity as evidenced by the similarity between the C. reinhardtii and V. carteri genomes , and shared origins with C. reinhardtii of key developmental regulators in V. carteri.…”

Section: Discussionmentioning

confidence: 99%

Green Algae and the Origins of Multicellularity in the Plant Kingdom

Umen

2014

Cold Spring Harbor Perspectives in Biology

118

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The green lineage of chlorophyte algae and streptophytes form a large and diverse clade with multiple independent transitions to produce multicellular and/or macroscopically complex organization. In this review, I focus on two of the best-studied multicellular groups of green algae: charophytes and volvocines. Charophyte algae are the closest relatives of land plants and encompass the transition from unicellularity to simple multicellularity. Many of the innovations present in land plants have their roots in the cell and developmental biology of charophyte algae. Volvocine algae evolved an independent route to multicellularity that is captured by a graded series of increasing cell-type specialization and developmental complexity. The study of volvocine algae has provided unprecedented insights into the innovations required to achieve multicellularity.

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“…These studies have also shown that evolutionarily younger genes tend to be expressed at earlier and later stages of development, whereas the transcriptomes of the middle stages (the phylotypic stage) are dominated by ancient genes (10, 13). It remains to be investigated how the evolutionary age and the expression patterns of the different TFs shift throughout the ontogeny of these lineages and whether TF expression profiles correlate with the general transcriptome profiles.Previous studies have analyzed the evolutionary history and phylogenetic distribution of TFs in various branches of the tree of life (6,(15)(16)(17)(18)(19)(20)(21)(22). However, it is not yet clear whether the evolutionary scenarios previously proposed are robust to the incorporation of genome data from key phylogenetic taxa that were previously unavailable.…”

mentioning

confidence: 99%

“…Previous studies have analyzed the evolutionary history and phylogenetic distribution of TFs in various branches of the tree of life (6,(15)(16)(17)(18)(19)(20)(21)(22). However, it is not yet clear whether the evolutionary scenarios previously proposed are robust to the incorporation of genome data from key phylogenetic taxa that were previously unavailable.…”

mentioning

confidence: 99%

Transcription factor evolution in eukaryotes and the assembly of the regulatory toolkit in multicellular lineages

Mendoza

Sebé-Pedrós

Šestak

et al. 2013

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

200

224

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Transcription factors (TFs) are the main players in transcriptional regulation in eukaryotes. However, it remains unclear what role TFs played in the origin of all of the different eukaryotic multicellular lineages. In this paper, we explore how the origin of TF repertoires shaped eukaryotic evolution and, in particular, their role into the emergence of multicellular lineages. We traced the origin and expansion of all known TFs through the eukaryotic tree of life, using the broadest possible taxon sampling and an updated phylogenetic background. Our results show that the most complex multicellular lineages (i.e., those with embryonic development, Metazoa and Embryophyta) have the most complex TF repertoires, and that these repertoires were assembled in a stepwise manner. We also show that a significant part of the metazoan and embryophyte TF toolkits evolved earlier, in their respective unicellular ancestors. To gain insights into the role of TFs in the development of both embryophytes and metazoans, we analyzed TF expression patterns throughout their ontogeny. The expression patterns observed in both groups recapitulate those of the whole transcriptome, but reveal some important differences. Our comparative genomics and expression data reshape our view on how TFs contributed to eukaryotic evolution and reveal the importance of TFs to the origins of multicellularity and embryonic development.phylotypic stage | Holozoa | LECA T ranscription factors (TFs) are proteins that bind to DNA in a sequence-specific manner (1) and enhance or repress gene expression (2-4). In response to a broad range of stimuli, TFs coordinate many important biological processes, from cell cycle progression and physiological responses, to cell differentiation and development (5, 6). Thus, TFs have a central role in the transcriptional regulation of all cellular organisms, being present in all branches of the tree of life (bacteria, archaea, and eukaryotes). There appears to be a correlation between elaborate regulation of gene expression and the complexity of organisms (7), such that the amount (as a proportion of an organism's total gene content) and diversity of TF proteins is expected to be directly correlated with this complexity (8). Indeed, TFs play a crucial role in multicellular eukaryotes. For example, TFs are the master regulators of embryonic development in embryophytes and metazoans (9), and analyses of their embryonic transcriptional profiles support the presence of a phylotypic stage in both lineages (10-14). These studies have also shown that evolutionarily younger genes tend to be expressed at earlier and later stages of development, whereas the transcriptomes of the middle stages (the phylotypic stage) are dominated by ancient genes (10, 13). It remains to be investigated how the evolutionary age and the expression patterns of the different TFs shift throughout the ontogeny of these lineages and whether TF expression profiles correlate with the general transcriptome profiles.Previous studies have analyzed the evolutionary ...

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Early evolution of metazoan transcription factors

Cited by 130 publications

References 70 publications

Ancient origin of the integrin-mediated adhesion and signaling machinery

Ancient origin of the integrin-mediated adhesion and signaling machinery

Green Algae and the Origins of Multicellularity in the Plant Kingdom

Transcription factor evolution in eukaryotes and the assembly of the regulatory toolkit in multicellular lineages

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