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Iñaki Ruiz-trillo - One of the best experts on this subject based on the ideXlab platform.
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Filastereans and Ichthyosporeans: Models to Understand the Origin of Metazoan Multicellularity
Evolutionary Transitions to Multicellular Life, 2015Co-Authors: Hiroshi Suga, Iñaki Ruiz-trilloAbstract:The origin of animals or Metazoans from their unicellular ancestors is one of the most important evolutionary transitions in the history of life. To decipher the molecular mechanisms involved in this transition, it is crucial to understand both the early evolution of animals and their unicellular prehistory. Recent phylogenomic analyses have shown that there are at least three distinct unicellular or colonial lineages closely related to Metazoans: choanoflagellates, ichthyosporeans and filastereans. However, until recently, choanoflagellates had been the only lineage for which an entire genome sequence was available. Moreover, the lack of transgenesis tools in any of these unicellular lineages had precluded the possibility of performing functional analyses. To better understand the unicellular prehistory of animals, we have recently obtained the genome sequences of both filastereans and ichthyosporeans. Analyses of their genomes identified many important genes for Metazoan multicellularity and development, some of which are absent from the choanoflagellate genomes and thus were thought to be Metazoan-specific. We have also established methods for transgenesis and gene silencing in ichthyosporeans. The combination of genomic information and molecular tools in filastereans and ichthyosporeans facilitate efficient functional analyses to understand how the key genes in the evolution of multicellularity were co-opted during the unicellular-tomulticellular transition that gave rise to Metazoans. We propose that filastereans and ichthyosporeans are ideal model organisms for investigating the origin of Metazoan multicellularity.
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Earliest Holozoan Expansion of Phosphotyrosine Signaling
Molecular biology and evolution, 2013Co-Authors: Hiroshi Suga, Guifré Torruella, Gertraud Burger, Matthew W. Brown, Iñaki Ruiz-trilloAbstract:Phosphotyrosine (pTyr) signaling is involved in development and maintenance of Metazoans’ multicellular body through cell-to-cell communication. Tyrosine kinases (TKs), tyrosine phosphatases, and other proteins relaying the signal compose the cascade. Domain architectures of the pTyr signaling proteins are diverse in Metazoans, reflecting their complex intercellular communication. Previous studies had shown that the Metazoan-type TKs, as well as other pTyr signaling proteins, were already diversified in the common ancestor of Metazoans, choanoflagellates, and filastereans (which are together included in the clade Holozoa) whereas they are absent in fungi and other nonholozoan lineages. However, the earliest-branching holozoans Ichthyosporea and Corallochytrea, as well as the two fungi-related amoebae Fonticula and Nuclearia, have not been studied. Here, we analyze the complete genome sequences of two ichthyosporeans and Fonticula, and RNAseq data of three additional ichthyosporeans, one corallochytrean, and Nuclearia. Both the ichthyosporean and corallochytrean genomes encode a large variety of receptor TKs (RTKs) and cytoplasmic TKs (CTKs), as well as other pTyr signaling components showing highly complex domain architectures. However, Nuclearia and Fonticula have no TK, and show much less diversity in other pTyr signaling components. The CTK repertoires of both Ichthyosporea and Corallochytrea are similar to those of Metazoa, Choanoflagellida, and Filasterea, but the RTK sets are totally different from each other. The complex pTyr signaling equipped with positive/negative feedback mechanism likely emerged already at an early stage of holozoan evolution, yet keeping a high evolutionary plasticity in extracellular signal reception until the co-option of the system for cell-to-cell communication in Metazoans.
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Transcription factor evolution in eukaryotes and the assembly of the regulatory toolkit in multicellular lineages
Proceedings of the National Academy of Sciences of the United States of America, 2013Co-Authors: Alex De Mendoza, Arnau Sebé-pedrós, Martin Sebastijan Šestak, Marija Matejčić, Guifré Torruella, Tomislav Domazet-lošo, Iñaki Ruiz-trilloAbstract: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.
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Insights into the Origin of Metazoan Filopodia and Microvilli
Molecular Biology and Evolution, 2013Co-Authors: Arnau Sebé-pedrós, Pawel Burkhardt, Stephen R Fairclough, Nicole King, Núria Sánchez-pons, B. Franz Lang, Iñaki Ruiz-trilloAbstract:Filopodia are fine actin-based cellular projections used for both environmental sensing and cell motility, and they are essential organelles for Metazoan cells. In this study, we reconstruct the origin of Metazoan filopodia and microvilli. We first report on the evolutionary assembly of the filopodial molecular toolkit and show that homologs of many Metazoan filopodial components, including fascin and myosin X, were already present in the unicellular or colonial progenitors of Metazoans. Furthermore, we find that the actin crosslinking protein fascin localizes to filopodia-like structures and microvilli in the choanoflagellate Salpingoeca rosetta. In addition, homologs of filopodial genes in the holozoan Capsaspora owczarzaki are upregulated in filopodia-bearing cells relative to those that lack them. Therefore, our findings suggest that proteins essential for Metazoan filopodia and microvilli are functionally conserved in unicellular and colonial holozoans and that the last common ancestor of Metazoans bore a complex and specific filopodial machinery.
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Development of ichthyosporeans sheds light on the origin of Metazoan multicellularity
Developmental biology, 2013Co-Authors: Hiroshi Suga, Iñaki Ruiz-trilloAbstract:To understand the mechanisms involved in the transition from protists to multicellular animals (Metazoans), studying unicellular relatives of Metazoans is as important as studying Metazoans themselves. However, investigations remain poor on the closest unicellular (or colonial) relatives of Metazoa, i.e., choanoflagellates, filastereans and ichthyosporeans. Molecular-level analyses on these protists have been severely limited by the lack of transgenesis tools. Their genomes, however, contain several key genes encoding proteins important for Metazoan development and multicellularity, including those involved in cell–cell communication, cell proliferation, cell differentiation, and tissue growth control. Tools to analyze their functions in a molecular level are awaited. Here we report techniques of cell transformation and gene silencing developed for the first time in a close relative of Metazoans, the ichthyosporean Creolimax fragrantissima. We propose C. fragrantissima as a model organism to investigate the origin of Metazoan multicellularity. By transgenesis, we demonstrate that its colony develops from a fully-grown multinucleate syncytium, in which nuclear divisions are strictly synchronized. It has been hypothesized that Metazoan multicellular development initially occurred in the course of evolution through successive rounds of cell division, which were not necessarily be synchronized, or alternatively through cell aggregation. Our findings point to another possible mechanism for the evolution of animal multicellularity, namely, cellularization of a syncytium in which nuclear divisions are synchronized. We believe that further studies on the development of ichthyosporeans by the use of our methodologies will provide novel insights into the origin of Metazoan multicellularity.
Nicole King - One of the best experts on this subject based on the ideXlab platform.
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Evolutionary Insights into PreMetazoan Functions of the Neuronal Protein Homer
Molecular Biology and Evolution, 2014Co-Authors: Pawel Burkhardt, Kent L. Mcdonald, Mads Grønborg, Tara Sulur, Qi Wang, Nicole KingAbstract:Reconstructing the evolution and ancestral functions of synaptic proteins promises to shed light on how neurons first evolved. The postsynaptic density (PSD) protein Homer scaffolds membrane receptors and regulates Ca(2+) signaling in diverse Metazoan cell types (including neurons and muscle cells), yet its ancestry and core functions are poorly understood. We find that the protein domain organization and essential biochemical properties of Metazoan Homer proteins, including their ability to tetramerize, are conserved in the choanoflagellate Salpingoeca rosetta, one of the closest living relatives of Metazoans. Unlike in neurons, Homer localizes to the nucleoplasm in S. rosetta and interacts directly with Flotillin, a protein more commonly associated with cell membranes. Surprisingly, we found that the Homer/Flotillin interaction and its localization to the nucleus are conserved in Metazoan astrocytes. These findings suggest that Homer originally interacted with Flotillin in the nucleus of the last common ancestor of Metazoans and choanoflagellates and was later co-opted to function as a membrane receptor scaffold in the PSD.
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Insights into the Origin of Metazoan Filopodia and Microvilli
Molecular Biology and Evolution, 2013Co-Authors: Arnau Sebé-pedrós, Pawel Burkhardt, Stephen R Fairclough, Nicole King, Núria Sánchez-pons, B. Franz Lang, Iñaki Ruiz-trilloAbstract:Filopodia are fine actin-based cellular projections used for both environmental sensing and cell motility, and they are essential organelles for Metazoan cells. In this study, we reconstruct the origin of Metazoan filopodia and microvilli. We first report on the evolutionary assembly of the filopodial molecular toolkit and show that homologs of many Metazoan filopodial components, including fascin and myosin X, were already present in the unicellular or colonial progenitors of Metazoans. Furthermore, we find that the actin crosslinking protein fascin localizes to filopodia-like structures and microvilli in the choanoflagellate Salpingoeca rosetta. In addition, homologs of filopodial genes in the holozoan Capsaspora owczarzaki are upregulated in filopodia-bearing cells relative to those that lack them. Therefore, our findings suggest that proteins essential for Metazoan filopodia and microvilli are functionally conserved in unicellular and colonial holozoans and that the last common ancestor of Metazoans bore a complex and specific filopodial machinery.
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origin of Metazoan cadherin diversity and the antiquity of the classical cadherin β catenin complex
Proceedings of the National Academy of Sciences of the United States of America, 2012Co-Authors: Scott A. Nichols, Stephen R Fairclough, Daniel J Richter, Brock Roberts, Nicole KingAbstract:The evolution of cadherins, which are essential for Metazoan multicellularity and restricted to Metazoans and their closest relatives, has special relevance for understanding Metazoan origins. To reconstruct the ancestry and evolution of cadherin gene families, we analyzed the genomes of the choanoflagellate Salpingoeca rosetta, the unicellular outgroup of choanoflagellates and Metazoans Capsaspora owczarzaki, and a draft genome assembly from the homoscleromorph sponge Oscarella carmela. Our finding of a cadherin gene in C. owczarzaki reveals that cadherins predate the divergence of the C. owczarzaki, choanoflagellate, and Metazoan lineages. Data from these analyses also suggest that the last common ancestor of Metazoans and choanoflagellates contained representatives of at least three cadherin families, lefftyrin, coherin, and hedgling. Additionally, we find that an O. carmela classical cadherin has predicted structural features that, in bilaterian classical cadherins, facilitate binding to the cytoplasmic protein β-catenin and, thereby, promote cadherin-mediated cell adhesion. In contrast with preMetazoan cadherin families (i.e., those conserved between choanoflagellates and Metazoans), the later appearance of classical cadherins coincides with Metazoan origins.
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Origin of Metazoan cadherin diversity and the antiquity of the classical cadherin/β-catenin complex
Proceedings of the National Academy of Sciences of the United States of America, 2012Co-Authors: Scott A. Nichols, Stephen R Fairclough, Daniel J Richter, Brock Roberts, Nicole KingAbstract:The evolution of cadherins, which are essential for Metazoan multicellularity and restricted to Metazoans and their closest relatives, has special relevance for understanding Metazoan origins. To reconstruct the ancestry and evolution of cadherin gene families, we analyzed the genomes of the choanoflagellate Salpingoeca rosetta, the unicellular outgroup of choanoflagellates and Metazoans Capsaspora owczarzaki, and a draft genome assembly from the homoscleromorph sponge Oscarella carmela. Our finding of a cadherin gene in C. owczarzaki reveals that cadherins predate the divergence of the C. owczarzaki, choanoflagellate, and Metazoan lineages. Data from these analyses also suggest that the last common ancestor of Metazoans and choanoflagellates contained representatives of at least three cadherin families, lefftyrin, coherin, and hedgling. Additionally, we find that an O. carmela classical cadherin has predicted structural features that, in bilaterian classical cadherins, facilitate binding to the cytoplasmic protein β-catenin and, thereby, promote cadherin-mediated cell adhesion. In contrast with preMetazoan cadherin families (i.e., those conserved between choanoflagellates and Metazoans), the later appearance of classical cadherins coincides with Metazoan origins.
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PreMetazoan Ancestry of the Myc-Max Network
Molecular Biology and Evolution, 2011Co-Authors: Susan L Young, Daniel Diolaiti, Maralice Conacci-sorrell, Iñaki Ruiz-trillo, Robert N Eisenman, Nicole KingAbstract:The origin of Metazoans required the evolution of mechanisms for maintaining differentiated cell types within a multicellular individual, in part through spatially differentiated patterns of gene transcription. The unicellular ancestor of Metazoans was presumably capable of regulating gene expression temporally in response to changing environmental conditions, and spatial cell differentiation in Metazoans may represent a co-option of preexisting regulatory mechanisms. Myc is a critical regulator of cell growth, proliferation, and death that is found in all Metazoans but absent in other multicellular lineages, including fungi and plants. Homologs of Myc and its binding partner, Max, exist in two of the closest living relatives of animals, the choanoflagellate Monosiga brevicollis (Mb) and Capsaspora owczarzaki, a unicellular opisthokont that is closely related to Metazoans and choanoflagellates. We find that Myc and Max from M. brevicollis heterodimerize and bind to both canonical and noncanonical E-boxes, the DNA-binding sites through which Metazoan Myc proteins act. Moreover, in M. brevicollis, MbMyc protein can be detected in nuclear and flagellar regions. Like Metazoan Max proteins, MbMax can form homodimers that bind to E-boxes. However, cross-species dimerization between Mb and human Myc and Max proteins was not observed, suggesting that the binding interface has diverged. Our results reveal that the Myc/Max network arose before the divergence of the choanoflagellate and Metazoan lineages. Furthermore, core features of Metazoan Myc function, including heterodimerization with Max, binding to E-box sequences in DNA, and localization to the nucleus, predate the origin of Metazoans.
Athula H. Wikramanayake - One of the best experts on this subject based on the ideXlab platform.
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Strabismus-mediated primary archenteron invagination is uncoupled from Wnt/β-catenin-dependent endoderm cell fate specification in Nematostella vectensis (Anthozoa, Cnidaria): Implications for the evolution of gastrulation.
Evodevo, 2011Co-Authors: Shalika Kumburegama, Naveen M. Wijesena, Ronghui Xu, Athula H. WikramanayakeAbstract:Background Gastrulation is a uniquely Metazoan character, and its genesis was arguably the key step that enabled the remarkable diversification within this clade. The process of gastrulation involves two tightly coupled events during embryogenesis of most Metazoans. Morphogenesis produces a distinct internal epithelial layer in the embryo, and this epithelium becomes segregated as an endoderm/endomesodermal germ layer through the activation of a specific gene regulatory program. The developmental mechanisms that induced archenteron formation and led to the segregation of germ layers during Metazoan evolution are unknown. But an increased understanding of development in early diverging taxa at the base of the Metazoan tree may provide insights into the origins of these developmental mechanisms.
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strabismus mediated primary archenteron invagination is uncoupled from wnt β catenin dependent endoderm cell fate specification in nematostella vectensis anthozoa cnidaria implications for the evolution of gastrulation
Evodevo, 2011Co-Authors: Shalika Kumburegama, Naveen M. Wijesena, Ronghui Xu, Athula H. WikramanayakeAbstract:Background Gastrulation is a uniquely Metazoan character, and its genesis was arguably the key step that enabled the remarkable diversification within this clade. The process of gastrulation involves two tightly coupled events during embryogenesis of most Metazoans. Morphogenesis produces a distinct internal epithelial layer in the embryo, and this epithelium becomes segregated as an endoderm/endomesodermal germ layer through the activation of a specific gene regulatory program. The developmental mechanisms that induced archenteron formation and led to the segregation of germ layers during Metazoan evolution are unknown. But an increased understanding of development in early diverging taxa at the base of the Metazoan tree may provide insights into the origins of these developmental mechanisms.
Shalika Kumburegama - One of the best experts on this subject based on the ideXlab platform.
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Strabismus-mediated primary archenteron invagination is uncoupled from Wnt/β-catenin-dependent endoderm cell fate specification in Nematostella vectensis (Anthozoa, Cnidaria): Implications for the evolution of gastrulation.
Evodevo, 2011Co-Authors: Shalika Kumburegama, Naveen M. Wijesena, Ronghui Xu, Athula H. WikramanayakeAbstract:Background Gastrulation is a uniquely Metazoan character, and its genesis was arguably the key step that enabled the remarkable diversification within this clade. The process of gastrulation involves two tightly coupled events during embryogenesis of most Metazoans. Morphogenesis produces a distinct internal epithelial layer in the embryo, and this epithelium becomes segregated as an endoderm/endomesodermal germ layer through the activation of a specific gene regulatory program. The developmental mechanisms that induced archenteron formation and led to the segregation of germ layers during Metazoan evolution are unknown. But an increased understanding of development in early diverging taxa at the base of the Metazoan tree may provide insights into the origins of these developmental mechanisms.
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strabismus mediated primary archenteron invagination is uncoupled from wnt β catenin dependent endoderm cell fate specification in nematostella vectensis anthozoa cnidaria implications for the evolution of gastrulation
Evodevo, 2011Co-Authors: Shalika Kumburegama, Naveen M. Wijesena, Ronghui Xu, Athula H. WikramanayakeAbstract:Background Gastrulation is a uniquely Metazoan character, and its genesis was arguably the key step that enabled the remarkable diversification within this clade. The process of gastrulation involves two tightly coupled events during embryogenesis of most Metazoans. Morphogenesis produces a distinct internal epithelial layer in the embryo, and this epithelium becomes segregated as an endoderm/endomesodermal germ layer through the activation of a specific gene regulatory program. The developmental mechanisms that induced archenteron formation and led to the segregation of germ layers during Metazoan evolution are unknown. But an increased understanding of development in early diverging taxa at the base of the Metazoan tree may provide insights into the origins of these developmental mechanisms.
Patricia J. Johnson - One of the best experts on this subject based on the ideXlab platform.
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A Metazoan/plant-like capping enzyme and cap modified nucleotides in the unicellular eukaryote Trichomonas vaginalis.
PLoS Pathogens, 2010Co-Authors: Augusto Simoes-barbosa, Robert P. Hirt, Patricia J. JohnsonAbstract:The cap structure of eukaryotic messenger RNAs is initially elaborated through three enzymatic reactions: hydrolysis of the 5′-triphosphate, transfer of guanosine through a 5′-5′ triphosphate linkage and N7-methylation of the guanine cap. Three distinctive enzymes catalyze each reaction in various microbial eukaryotes, whereas the first two enzymes are fused into a single polypeptide in Metazoans and plants. In addition to the guanosine cap, adjacent nucleotides are 2′-O-ribose methylated in metazoa and plants, but not in yeast. Analyses of various cap structures have suggested a linear phylogenetic trend of complexity. These findings have led to a model in which plants and metazoa evolved a two-component capping apparatus and modification of adjacent nucleotides while many microbial eukaryotes maintained the three-component system and did not develop modification of adjacent nucleotides. Here, we have characterized a bifunctional capping enzyme in the divergent microbial eukaryote Trichomonas vaginalis using biochemical and phylogenetic analyses. This unicellular parasite was found to harbor a Metazoan/plant-like capping apparatus that is represented by a two-domain polypeptide containing a C-terminus guanylyltransferase and a cysteinyl phosphatase triphosphatase, distinct from its counterpart in other microbial eukaryotes. In addition, T. vaginalis mRNAs contain a cap 1 structure represented by m7GpppAmpUp or m7GpppCmpUp; a feature typical of Metazoan and plant mRNAs but absent in yeast mRNAs. Phylogenetic and biochemical analyses of the origin of the T. vaginalis capping enzyme suggests a complex evolutionary model where differential gene loss and/or acquisition occurred in the development of the RNA capping apparatus and cap modified nucleotides during eukaryote diversification.
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a Metazoan plant like capping enzyme and cap modified nucleotides in the unicellular eukaryote trichomonas vaginalis
PLOS Pathogens, 2010Co-Authors: Augusto Simoesbarbosa, Robert P. Hirt, Patricia J. JohnsonAbstract:The cap structure of eukaryotic messenger RNAs is initially elaborated through three enzymatic reactions: hydrolysis of the 5′-triphosphate, transfer of guanosine through a 5′-5′ triphosphate linkage and N7-methylation of the guanine cap. Three distinctive enzymes catalyze each reaction in various microbial eukaryotes, whereas the first two enzymes are fused into a single polypeptide in Metazoans and plants. In addition to the guanosine cap, adjacent nucleotides are 2′-O-ribose methylated in metazoa and plants, but not in yeast. Analyses of various cap structures have suggested a linear phylogenetic trend of complexity. These findings have led to a model in which plants and metazoa evolved a two-component capping apparatus and modification of adjacent nucleotides while many microbial eukaryotes maintained the three-component system and did not develop modification of adjacent nucleotides. Here, we have characterized a bifunctional capping enzyme in the divergent microbial eukaryote Trichomonas vaginalis using biochemical and phylogenetic analyses. This unicellular parasite was found to harbor a Metazoan/plant-like capping apparatus that is represented by a two-domain polypeptide containing a C-terminus guanylyltransferase and a cysteinyl phosphatase triphosphatase, distinct from its counterpart in other microbial eukaryotes. In addition, T. vaginalis mRNAs contain a cap 1 structure represented by m7GpppAmpUp or m7GpppCmpUp; a feature typical of Metazoan and plant mRNAs but absent in yeast mRNAs. Phylogenetic and biochemical analyses of the origin of the T. vaginalis capping enzyme suggests a complex evolutionary model where differential gene loss and/or acquisition occurred in the development of the RNA capping apparatus and cap modified nucleotides during eukaryote diversification.