Fig 10 - uploaded by Alexander V Ereskovsky
Content may be subject to copyright.
Cladogram showing TF origin and evolution on phylogenetic hypothesis according to Sébé-Pedrós et al. (2011). Each color represents domain class. Origin of domain is indicated by a colored dot . Specific protein family appearance is indicated by a black-circled dot in our taxon sampling. Loss of the domain or specific protein family is indicated by a cross . Metazoan apomorphies are shown as black dots
Source publication
The emergence of multicellularity is regarded as one of the major evolutionary events of life. This transition unicellularity/pluricellularity was acquired independently several times (King 2004). The acquisition of multicellularity implies the emergence of cellular cohesion and means of communication, as well as molecular mechanisms enabling the c...
Contexts in source publication
Context 1
... homeobox gene superfamily encodes transcription factors that, in eumetazoans, act as master regulators of development through their ability to activate or repress a diverse range of downstream target genes. Classes are defined on the basis of conservation of the homeodomains (HD, a 60 amino acid DNA-binding proteic domain) they encode, as well as additional motifs that contribute to DNA binding and interactions with other proteins. Not only in metazoans but also in all multicellular Eukaryotes, these transcription factors are extensively used in fundamental development processes and are highly diversified. They are supposed to have played a key role in the acquisition of multicellularity in Eukaryota (Derelle et al. 2007; King 2004). A recent extensive phylogenetical study of HD at the eukaryotic scale showed that HDs can be grouped in two clades: TALE (three extra residues between helix 1 and helix 2 of the homeodomain) and non-TALE. Moreover, these results show that the last common ancestor of Eukaryotes (LECA) already possessed these two types of HDs, non-TALE genes being lost secondarily in Monosiga (Derelle et al. 2007; King et al. 2008; Larroux et al. 2008, Sebé-Pedrós et al. 2011). Later, duplications occurred independently during diversification of eukaryotic lineages. As a result of this very wide diversification (by duplication and divergence, or via domain shuffling), animal homeobox genes are at present divided into 11 classes and more than 125 gene families, non-TALE genes being more diversified than TALE ones (Holland et al. 2007; Mukherjee and Bürglin 2007; Ryan et al. 2010). Non-TALE genes Major diversification events of non- TALE genes occurred before metazoan radiation. Indeed, data on sponges revealed that many of non- TALE classes were already present in the metazoan ancestor, such as ANTP, PRD, POU, LIM, and SIX, and that others may have appeared later, after the Porifera – Eumetazoa divergence because, to date, no HNF, CUT, PROS, or CERS classes have been discovered in demosponges (Larroux et al. 2006, 2007, 2008; Ryan and Baxevanis 2007; Ryan et al. 2010; Degnan et al. 2009; Srivastava et al. 2010a, 2010b). Figure 9 gives a more detailed view of Non-TALE gene history. TALE genes The TALE category includes IRO, MEIS, PBX, and TGIF classes (Holland et al. 2007; Mukherjee and Bürglin 2007). In demosponges, several TALE genes have been characterized (Perovic et al. 2003; Larroux et al. 2006, 2008). All but one seem to be related to the IRO class. Larroux et al. (2008) proposed that the common ancestor of Metazoa may have possessed at least two genes, resulting from a ancestral MEIS-like gene (King et al. 2008). However, the data recently obtained on Capsaspora , although poorly supported, suggest the presence of a PBX class in the Holo- zoan ancestor and a secondary loss in Amphimedon and Monosiga (Sebé-Pedrós et al. 2011). The interpretation is thus, once again, pending the acquisition of other genomic data. Sponges also possess other TFs (Fig. 10), and evolutionary scenarios have been proposed for each of them. Generally, although many classes of transcription factors are older in origin (Derelle et al. 2007; King et al. 2008; Larroux et al. 2008; Shalchian-Tabrizi et al. 2008; Degnan et al. 2009; Mikhailov et al. 2009; Sebé-Pedrós et al. 2011), many other classes and families of transcription factors seem to be metazoan innovations. These animal genetic novelties are thought to have played an important role in animal evolution by providing new tools that increased morphogenetic possi- bilities. Nevertheless, as already mentioned, this impression of sudden emergence may only be the artificial result of insufficient sampling at the eukaryotic scale. In the same way, the lack of certain genes in the Amphimedon genome may not reflect the ancestral condition in sponges but rather specific gene losses (Peterson and Sperling 2007; Adamska et al. 2011). To resolve this question, the acquisition of genomic data from other sponge lineages is needed. The most recent study on the subject, using the newly available genome of the sporozoan Capsaspora , led Sebé-Pedrós et al. (2011) to propose a new very comprehensive evolutionary scenario (Fig. 10). In other animals, ten TFs have been identified to be involved in EMT regulation during embryogenesis and car- cinogenesis. Among them, some are direct repressors of the gene coding for E-cadherin (such as Snail, Twist, Fox, Gsc, and KLF). Interestingly, these TF are regulated by well- known signaling pathways Wnt, Notch, TGF- β , and Hh (Takebe et al. ...
Context 2
... homeobox gene superfamily encodes transcription factors that, in eumetazoans, act as master regulators of development through their ability to activate or repress a diverse range of downstream target genes. Classes are defined on the basis of conservation of the homeodomains (HD, a 60 amino acid DNA-binding proteic domain) they encode, as well as additional motifs that contribute to DNA binding and interactions with other proteins. Not only in metazoans but also in all multicellular Eukaryotes, these transcription factors are extensively used in fundamental development processes and are highly diversified. They are supposed to have played a key role in the acquisition of multicellularity in Eukaryota (Derelle et al. 2007; King 2004). A recent extensive phylogenetical study of HD at the eukaryotic scale showed that HDs can be grouped in two clades: TALE (three extra residues between helix 1 and helix 2 of the homeodomain) and non-TALE. Moreover, these results show that the last common ancestor of Eukaryotes (LECA) already possessed these two types of HDs, non-TALE genes being lost secondarily in Monosiga (Derelle et al. 2007; King et al. 2008; Larroux et al. 2008, Sebé-Pedrós et al. 2011). Later, duplications occurred independently during diversification of eukaryotic lineages. As a result of this very wide diversification (by duplication and divergence, or via domain shuffling), animal homeobox genes are at present divided into 11 classes and more than 125 gene families, non-TALE genes being more diversified than TALE ones (Holland et al. 2007; Mukherjee and Bürglin 2007; Ryan et al. 2010). Non-TALE genes Major diversification events of non- TALE genes occurred before metazoan radiation. Indeed, data on sponges revealed that many of non- TALE classes were already present in the metazoan ancestor, such as ANTP, PRD, POU, LIM, and SIX, and that others may have appeared later, after the Porifera – Eumetazoa divergence because, to date, no HNF, CUT, PROS, or CERS classes have been discovered in demosponges (Larroux et al. 2006, 2007, 2008; Ryan and Baxevanis 2007; Ryan et al. 2010; Degnan et al. 2009; Srivastava et al. 2010a, 2010b). Figure 9 gives a more detailed view of Non-TALE gene history. TALE genes The TALE category includes IRO, MEIS, PBX, and TGIF classes (Holland et al. 2007; Mukherjee and Bürglin 2007). In demosponges, several TALE genes have been characterized (Perovic et al. 2003; Larroux et al. 2006, 2008). All but one seem to be related to the IRO class. Larroux et al. (2008) proposed that the common ancestor of Metazoa may have possessed at least two genes, resulting from a ancestral MEIS-like gene (King et al. 2008). However, the data recently obtained on Capsaspora , although poorly supported, suggest the presence of a PBX class in the Holo- zoan ancestor and a secondary loss in Amphimedon and Monosiga (Sebé-Pedrós et al. 2011). The interpretation is thus, once again, pending the acquisition of other genomic data. Sponges also possess other TFs (Fig. 10), and evolutionary scenarios have been proposed for each of them. Generally, although many classes of transcription factors are older in origin (Derelle et al. 2007; King et al. 2008; Larroux et al. 2008; Shalchian-Tabrizi et al. 2008; Degnan et al. 2009; Mikhailov et al. 2009; Sebé-Pedrós et al. 2011), many other classes and families of transcription factors seem to be metazoan innovations. These animal genetic novelties are thought to have played an important role in animal evolution by providing new tools that increased morphogenetic possi- bilities. Nevertheless, as already mentioned, this impression of sudden emergence may only be the artificial result of insufficient sampling at the eukaryotic scale. In the same way, the lack of certain genes in the Amphimedon genome may not reflect the ancestral condition in sponges but rather specific gene losses (Peterson and Sperling 2007; Adamska et al. 2011). To resolve this question, the acquisition of genomic data from other sponge lineages is needed. The most recent study on the subject, using the newly available genome of the sporozoan Capsaspora , led Sebé-Pedrós et al. (2011) to propose a new very comprehensive evolutionary scenario (Fig. 10). In other animals, ten TFs have been identified to be involved in EMT regulation during embryogenesis and car- cinogenesis. Among them, some are direct repressors of the gene coding for E-cadherin (such as Snail, Twist, Fox, Gsc, and KLF). Interestingly, these TF are regulated by well- known signaling pathways Wnt, Notch, TGF- β , and Hh (Takebe et al. ...
Citations
... Cleavage in sponges followed by the cell differentiation and migration resulting in a larva or young sponge (in the case of direct development) formation. In poriferan embryogenesis different types of epithelial and mesenchymal morphogenesis occur (Ereskovsky et al., 2013). ...
... Some structures, usually the larval or provisional ones, disappear, the others, that were rudimentary, rapidly complete their development. Morphogenesis, accompanying sponge larvae metamorphosis could be epithelial type, epithelial-mesenchymal transitions or mesenchymal-epithelial transformations depending on the larval structure (Ereskovsky et al., 2013). The main feature of the metamorphosis of the sponge larvae is the acquisition of the sponge Bauplan, which is mainly represented by the aquiferous system (Ereskovsky, 2019). ...
... The study of natural processes related to embryonic development, cell communication, and cell grouping has always been a significant area of research. Scientists have extensively investigated the intricate mechanisms involved in these processes to better understand how organisms develop from embryos and how cells interact with each other [152,153]. Self-assembling materials functionalized with photoswitchable proteins have been extensively investigated as a means of replicating these complex biological processes. As an example of these materials, functionalized colloidal particles have been developed to self-sort and undergo reversible assembly when exposed to specific wavelengths. ...
... The study of natural processes related to embryonic development, cell communication, and cell grouping has always been a significant area of research. Scientists have extensively investigated the intricate mechanisms involved in these processes to better understand how organisms develop from embryos and how cells interact with each other [152,153]. Selfassembling materials functionalized with photoswitchable proteins have been extensively investigated as a means of replicating these complex biological processes. As an example of these materials, functionalized colloidal particles have been developed to self-sort and undergo reversible assembly when exposed to specific wavelengths. ...
Photoproteins, luminescent proteins or optoproteins are a kind of light-response protein responsible for the conversion of light into biochemical energy that is used by some bacteria or fungi to regulate specific biological processes. Within these specific proteins, there are groups such as the photoreceptors that respond to a given light wavelength and generate reactions susceptible to being used for the development of high-novel applications, such as the optocontrol of metabolic pathways. Photoswitchable proteins play important roles during the development of new materials due to their capacity to change their conformational structure by providing/eliminating a specific light stimulus. Additionally, there are bioluminescent proteins that produce light during a heatless chemical reaction and are useful to be employed as biomarkers in several fields such as imaging, cell biology, disease tracking and pollutant detection. The classification of these optoproteins from bacteria and fungi as photoreceptors or photoresponse elements according to the excitation-emission spectrum (UV-Vis-IR), as well as their potential use in novel applications, is addressed in this article by providing a structured scheme for this broad area of knowledge.
... As one of the best candidates for sister group to all other animals [4][5][6][7][8][9][10] (Fig. 1a), sponges (Porifera) are of particular interest. Although the biology of Porifera is still poorly known [11], their ancient origin (> 600 million years (Myrs)) [12] has given rise to a phylum with over 9500 described species [13] distributed among four classes, with diverse ecological, embryological, cellular, and morphological features [14][15][16][17] (Fig. 1a, b). ...
... The first sponge genome sequenced, from the demosponge Amphimedon queenslandica, revealed a larger size and gene content than expected [18][19][20]. However, transcriptomic data from other species indicated that A. queenslandica was not representative of the diversity of sponges [17,[21][22][23][24][25][26]. Several sponge genomes now sequenced [27][28][29][30][31] illustrate the disparity of sponge genomes in terms of size, features of noncoding regions, and gene repertoire [3,28]. ...
Background
Explaining the emergence of the hallmarks of bilaterians is a central focus of evolutionary developmental biology—evodevo—and evolutionary genomics. For this purpose, we must both expand and also refine our knowledge of non-bilaterian genomes, especially by studying early branching animals, in particular those in the metazoan phylum Porifera.
Results
We present a comprehensive analysis of the first whole genome of a glass sponge, Oopsacas minuta, a member of the Hexactinellida. Studying this class of sponge is evolutionary relevant because it differs from the three other Porifera classes in terms of development, tissue organization, ecology, and physiology. Although O. minuta does not exhibit drastic body simplifications, its genome is among the smallest of animal genomes sequenced so far, and surprisingly lacks several metazoan core genes (including Wnt and several key transcription factors). Our study also provides the complete genome of a symbiotic Archaea dominating the associated microbial community: a new Thaumarchaeota species.
Conclusions
The genome of the glass sponge O. minuta differs from all other available sponge genomes by its compactness and smaller number of encoded proteins. The unexpected loss of numerous genes previously considered ancestral and pivotal for metazoan morphogenetic processes most likely reflects the peculiar syncytial tissue organization in this group. Our work further documents the importance of convergence during animal evolution, with multiple convergent evolution of septate-like junctions, electrical-signaling and multiciliated cells in metazoans.
... Diverse taxa of animals (Opisthokonta, Holozoa) ( Fig. 1A) also exhibit cellular aggregation during fundamental processes to develop and maintain healthy multicellular tissues. From sponges and cnidarians to vertebrates, animal cells disaggregate and reaggregate for spatial organization of tissues during the early stages of embryonic development (23)(24)(25), during inflammatory processes (26,27), and for tissue regeneration (28)(29)(30)(31)(32)(33)(34)(35). A few animal species have been conclusively demonstrated to use soluble chemical cues to regulate their aggregation phenotypes (6,27,29,32,(36)(37)(38)(39)(40)(41)(42). ...
Regulated cellular aggregation is an essential process for development and healing in many animal tissues. In some animals and a few distantly related unicellular species, cellular aggregation is regulated by diffusible chemical cues. However, it is unclear whether regulated cellular aggregation was part of the life cycles of the first multicellular animals and/or their unicellular ancestors. To fill this gap, we investigated the triggers of cellular aggregation in one of animals' closest unicellular living relatives-the filasterean Capsaspora owczarzaki. We discovered that Capsaspora aggregation is induced by chemical cues, as observed in some of the earliest branching animals and other unicellular species. Specifically, we found that calcium ions and lipids present in lipoproteins function together to induce aggregation of viable Capsaspora cells. We also found that this multicellular stage is reversible as depletion of the cues triggers disaggregation, which can be overcome upon reinduction. Our finding demonstrates that chemically regulated aggregation is important across diverse members of the holozoan clade. Therefore, this phenotype was plausibly integral to the life cycles of the unicellular ancestors of animals.
... Genetic evidence suggests that most of the molecular toolkit necessary to create epithelial layers is already present in sponges (Ereskovsky et al., 2013) and probably precedes the evolution of metazoans (Renard et al., 2021). However, although the formation of some sponge larvae requires morphogenetic movements reminiscent of gastrulation, they are not associated with the segregation of proper embryonic layers with restricted cell fates (Ereskovsky and Dondua, 2006;Nakanishi et al., 2014). ...
During gastrulation, early embryos specify and reorganise the topology of their germ layers. Surprisingly, this fundamental and early process does not appear to be rigidly constrained by evolutionary pressures; instead, the morphology of gastrulation is highly variable throughout the animal kingdom. Recent experimental results demonstrate that it is possible to generate different alternative gastrulation modes in single organisms, such as in early cnidarian, arthropod and vertebrate embryos. Here, we review the mechanisms that underlie the plasticity of vertebrate gastrulation both when experimentally manipulated and during evolution. Using the insights obtained from these experiments we discuss the effects of the increase in yolk volume on the morphology of gastrulation and provide new insights into two crucial innovations during amniote gastrulation: the transition from a ring-shaped mesoderm domain in anamniotes to a crescent-shaped domain in amniotes, and the evolution of the reptilian blastoporal plate/canal into the avian primitive streak.
... These living fossils already carry some signalling pathways, including Wnt, TGF-Beta, and Hedgehog [10], which are conserved across metazoan life. The sponge's anatomy is formed by two distinct epithelial cell layers, with a few cell types showing different degrees of motility [11]. Indeed, sponges were the first organisms in evolution to show organ-type structures. ...
The earliest metazoans probably evolved from single-celled organisms which found the colonial system to be a beneficial organization. Over the course of their evolution, these primary colonial organisms increased in size, and division of labour among the cells became a remarkable feature, leading to a higher level of organization: the biological organs. Primitive metazoans were the first organisms in evolution to show organ-type structures, which set the grounds for complex organs to evolve. Throughout evolution, and concomitant with organogenesis, is the appearance of tissue-specific stem cells. Tissue-specific stem cells gave rise to multicellular living systems with distinct organs which perform specific physiological functions. This setting is a constructive role of evolution; however, rebel cells can take over the molecular mechanisms for other purposes: nowadays we know that cancer stem cells, which generate aberrant organ-like structures, are at the top of a hierarchy. Furthermore, cancer stem cells are the root of metastasis, therapy resistance, and relapse. At present, most therapeutic drugs are unable to target cancer stem cells and therefore, treatment becomes a challenging issue. We expect that future research will uncover the mechanistic “forces” driving organ growth, paving the way to the implementation of new strategies to impair human tumorigenesis.
... Previous in-depth discussions on the ratio of adult-to-larval features in the metazoan ontogenetic cycles provided evidence for highly conserved basic developmental pathways and molecular patterns and processes across all metazoans in both larval (Haszprunar et al., 1995;Nielsen, 2013) and adult stages (Sly et al., 2003;Wang et al., 2020), including sponges (Holstein, 2012;Leininger et al., 2014;Ereskovsky et al., 2013), cnidarians, and bilaterians (Sinigaglia et al., 2013;. Authors of the latter study indicate that it is "highly unlikely that a specific and partially nested pattern involving at least nine transcription factors … evolved convergently twice" (Marlow et al., 2014: 10). ...
Various evaluations of the last common bilaterian ancestor ( lcba ) currently suggest that it resembled either a microscopic, non-segmented motile adult; or, on the contrary, a complex segmented adult motile urbilaterian. These fundamental inconsistencies remain largely unexplained. A majority of multidisciplinary data regarding sedentary adult ancestral bilaterian organization is overlooked. The sedentary-pelagic model is supported now by a number of novel developmental, paleontological and molecular phylogenetic data: (1) data in support of sedentary sponges, in the adult stage, as sister to all other Metazoa; (2) a similarity of molecular developmental pathways in both adults and larvae across sedentary sponges, cnidarians, and bilaterians; (3) a cnidarian-bilaterian relationship, including a unique sharing of a bona fide Hox-gene cluster, of which the evolutionary appearance does not connect directly to a bilaterian motile organization; (4) the presence of sedentary and tube-dwelling representatives of the main bilaterian clades in the early Cambrian; (5) an absence of definite taxonomic attribution of Ediacaran taxa reconstructed as motile to any true bilaterian phyla; (6) a similarity of tube morphology (and the clear presence of a protoconch-like apical structure of the Ediacaran sedentary Cloudinidae) among shells of the early Cambrian, and later true bilaterians, such as semi-sedentary hyoliths and motile molluscs; (7) recent data that provide growing evidence for a complex urbilaterian, despite a continuous molecular phylogenetic controversy. The present review compares the main existing models and reconciles the sedentary model of an urbilaterian and the model of a larva-like lcba with a unified sedentary(adult)-pelagic(larva) model of the lcba .
... In sponges, cell communication occurs only directly, although it is not necessarily contacting. At the same time, the morphogenesis of sponges has some features in common with more complex («real») multicellular organisms (Ereskovsky et al., 2013;Borisenko et al., 2019). Thus, in the morphogenesis of sponges there is a pronounced differentiation of cell types, and transdifferentiation is also possible. ...
This is a translation of my book published in Russian a year earlier. Some changes have been made. The data on ultradian (circahoralian) rhythms are summarized: their distribution, nature, importance in biochemistry and physiology. Such rhythms of protein synthesis and cell mass, enzyme activity, ATP and cAMP concentration, pH, and cellular respiration are considered with examples from bacteria, protists, and mammalian cells, as well as integral rhythms of human respiration, pulse, and behavior. The fractal nature of ultradian rhythms is established as one of the intrinsic properties of the cell. Using ultradian rhythms in cell cultures, a model is created for studying the mechanisms of direct intercellular interactions. Signaling factors have been found − gangliosides, blood neurotransmitters and some peptides. The processes in the cytoplasm triggered by them, leading to synchronization of cell and organ functions as a result of interactions of cells in the population, are determined. The section of the book "Biomedical Supplements" analyzing the kinetics of the processes and their signaling factors contains new ideas about the origin of multicellularity, the possibility of compensation of some senile disorders, the diagnosis and prognosis of heart and intestinal diseases, the rhythms of mobility and behavior of animals and humans, previously unknown properties of drugs.
... Recently, this description has been disputed in light of data from morphological and lineage-tracing analyses (13,14), suggesting that sponges do not undergo gastrulation as commonly seen in triploblastic animals. Nevertheless, comparative genomics and molecular phylogeny studies have shown that most of the genes involved in epithelial organization are present in sponge genomes (15,16), as are some of the genes involved in germlayer formation in Bilateria (the protostomes and deuterostomes, including all vertebrate spe-cies) (14) and in the epithelial-to-mesenchymal transition (EMT) (17). In Cnidaria, a phylum of diploblastic animals most closely related to triploblastic Bilateria (Fig. 1, A and B), molecular tool kits for epithelial organization and EMT are present in genomes, and gastrulation generates mesendoderm-like cells that express mesoderm transcriptional regulators and mesoderm-specific lineage markers, despite their lack of a genuine mesoderm germ layer (18). ...
The nonconserved primitive streak
In human development, a linear structure called the primitive streak appears 14 days after fertilization. This structure marks the transition of the embryo from having radial to bilateral symmetry. The primitive streak also gives anterior-posterior and dorsal-ventral spatial information to cells undergoing gastrulation and forming the various body cell types. In a Review, Sheng et al . present a phylogenetic and ontogenetic overview of the primitive streak. They discuss organismal, cellular, and molecular features of the primitive streak and how it functions in amniote gastrulation. The observation that this structure is not conserved and is not required for development in vitro has implications for embryonic stem cell–based models and considerations about human development research. —BAP
... Additionally, as a direct consequence of internal fertiliza tion, O. lobularis is a "brooding" sponge. This means that the development from a zygote to a fully developed larva (cinctoblastula) occurs within the adult tissue ( Ereskovsky et al. 2013b;Leys and Ereskovsky 2006). As in all Metazoa, the first developmental step consists of the cleavage of the zygote. ...
... Despite the true multicellular and metazoan nature of sponges having been elucidated decades ago (reviewed in Schenkelaars et al. 2019), there is a longstanding debate in the spongiologist community on whether sponges gastrulate. Different points of view compete: i) for some authors, multi polar egression leading to the formation of the coeloblastula during embryogenesis marks the onset of polarization and regionalization processes, suggesting it may be similar to gastrulation (Maldonado and Riesgo 2008); ii) others con sider that this process differs from gastrulation in that the resulting embryo apparently consists of one uniform cell layer and lacks polarity (Ereskovsky 2010;Ereskovsky and Dondua 2006) and prefer to hypothesize the gastrulation during larval metamorphosis (reviewed in Ereskovsky 2010; Ereskovsky et al. 2013b;Lanna 2015;Leys 2004;Wörheide et al. 2012), when an "inversion of germ layers" results in the formation of the aquiferous system. In the last case, the term "inversion" means that external-most larval cells form the internal-most ("gut-like") structures of an adult sponge, namely the aquiferous system. ...
... As mentioned in the section on embryology and in the previous section, Oscarella lobularis (like other homo scleromorph) presents clear epithelial characteristics, and all morphogenetic processes (development, regeneration, budding) are based mainly on epithelial morphogenetic movements in contrast to demosponges (Boury-Esnault et al. 2003;Ereskovsky 2010;Ereskovsky et al. 2009b;Ereskovsky et al. 2013a ;Ereskovsky et al. 2013b;Ereskovsky et al. 2015). This feature is expected to result in the formation of more stable cell layers during embryogenesis compared to demosponges (Ereskovsky 2010;Lanna 2015). ...
