Cnidarian-bilaterian comparison reveals the ancestral regulatory logic of the β-catenin dependent axial patterning

Lebedeva, Tatiana; Aman, Andrew J.; Graf, Thomas; Niedermoser, Isabell; Zimmermann, Bob; Kraus, Yulia; Schatka, Magdalena; Demilly, Adrien; Technau, Ulrich; Genikhovich, Grigory

doi:10.1038/s41467-021-24346-8

Cited by 32 publications

(66 citation statements)

References 65 publications

(110 reference statements)

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“…3A). In summary, LRP5/6 RNAi phenocopied the outcome of dominant-negative Tcf ( dnTcf ) mRNA overexpression (Röttinger et al, 2012), and was strikingly similar to the effect of the combined KD of Bra, Lmx, FoxA , and FoxB - the four β-catenin-dependent transcription factors determining the oral molecular identity of the embryo (Lebedeva et al, 2021). LRP5/6 RNAi resulted in a typical β-catenin loss-of-function phenotype, apart from the obvious fact that the embryos gastrulated normally, which was also the case in dnTcf mRNA-injected embryos (Röttinger et al, 2012) but, curiously, not in β-catenin morphants (Leclère et al, 2016), or in embryos subjected to shRNA-mediated β-catenin RNAi (Karabulut et al, 2019).…”

Section: Resultsmentioning

confidence: 85%

“…We used Brachyury ( Bra ), Wnt2 and Six3/6 as markers of the oral, midbody and aboral domains respectively (Lebedeva et al, 2021), Axin as a β-catenin signaling target gene with broader expression (Kraus et al, 2016; Lebedeva et al, 2021), as well as several additional markers for specific areas in the embryo. Notably, the midbody marker Wnt2 is also positively regulated by β-catenin signaling but it gets suppressed orally by Bra (Lebedeva et al, 2021). At the late gastrula stage (30 hpf), LRP5/6 RNAi resulted in a strong suppression of the oral markers Bra, FoxA and FoxB , as well as Axin (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…In Cnidaria, the bilaterian sister group, the role of the cWnt pathway in gastrulation and oral-aboral (OA) axis patterning has been confirmed by functional analyses (Kraus et al, 2016;Lebedeva et al, 2021;Leclère et al, 2016;Marlow et al, 2013;Momose et al, 2008;Momose and Houliston, 2007;Röttinger et al, 2012;Wikramanayake et al, 2003). Recently, we demonstrated that the regulatory logic of the β-catenin-dependent OA patterning in the sea anemone Nematostella vectensis and the posterior-anterior (PA) patterning of deuterostome Bilateria is highly similar, suggesting a common evolutionary origin of the OA and the PA axes (Darras et al, 2018;Darras et al, 2011;Kiecker and Niehrs, 2001;Lebedeva et al, 2021;Nordström et al, 2002). Although the way Nematostella interprets different intensities of β-catenin signal is largely understood (Kraus et al, 2016;Lebedeva et al, 2021), we still have very little idea about which Wnt ligands and which Fz receptors are involved in the cWntdependent axial patterning in this morphologically simple model organism.…”

Section: Introductionmentioning

confidence: 95%

“…Localized expression of the Wnt signaling components along the main body axis has been documented in the earliest branching animal lineages such as ctenophores (Pang et al, 2010) and sponges (Adamska et al, 2010;Leininger et al, 2014). In Cnidaria, the bilaterian sister group, the role of the cWnt pathway in gastrulation and oral-aboral (OA) axis patterning has been confirmed by functional analyses (Kraus et al, 2016;Lebedeva et al, 2021;Leclère et al, 2016;Marlow et al, 2013;Momose et al, 2008;Momose and Houliston, 2007;Röttinger et al, 2012;Wikramanayake et al, 2003). Recently, we demonstrated that the regulatory logic of the β-catenin-dependent OA patterning in the sea anemone Nematostella vectensis and the posterior-anterior (PA) patterning of deuterostome Bilateria is highly similar, suggesting a common evolutionary origin of the OA and the PA axes (Darras et al, 2018;Darras et al, 2011;Kiecker and Niehrs, 2001;Lebedeva et al, 2021;Nordström et al, 2002).…”

Section: Introductionmentioning

confidence: 96%

“…Recently, we demonstrated that the regulatory logic of the β-catenin-dependent OA patterning in the sea anemone Nematostella vectensis and the posterior-anterior (PA) patterning of deuterostome Bilateria is highly similar, suggesting a common evolutionary origin of the OA and the PA axes (Darras et al, 2018; Darras et al, 2011; Kiecker and Niehrs, 2001; Lebedeva et al, 2021; Nordström et al, 2002). Although the way Nematostella interprets different intensities of β-catenin signal is largely understood (Kraus et al, 2016; Lebedeva et al, 2021), we still have very little idea about which Wnt ligands and which Fz receptors are involved in the cWnt-dependent axial patterning in this morphologically simple model organism. The complement of Wnt and Fz molecules in Nematostella is surprisingly large.…”

Section: Introductionmentioning

confidence: 99%

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Sea anemone Frizzled receptors play partially redundant roles in the oral-aboral axis patterning

Niedermoser

Lebedeva

Genikhovich

2022

Preprint

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Canonical Wnt (cWnt) signaling is involved in a plethora of basic developmental processes such as endomesoderm specification, gastrulation and patterning the main body axis. To activate the signal, Wnt ligands form complexes with LRP5/6 and Frizzled receptors, which leads to nuclear translocation of β-catenin and transcriptional response. In Bilateria, the expression of different Frizzled genes is often partially overlapping, and their functions are known to be redundant in several developmental contexts. Here we demonstrate that all four Frizzled receptors take part in the cWnt-mediated oral-aboral axis patterning in the cnidarian Nematostella vectensis but show partially redundant functions. However, we do not see evidence for their involvement in the specification of the endoderm - an earlier event likely relying on maternal, intracellular β-catenin signaling components. Finally, we demonstrate that the main Wnt ligands crucial for the early oral-aboral patterning are Wnt3 and Wnt4. Comparison of our data to the knowledge from other models suggests that distinct but overlapping expression domains and partial functional redundancy of cnidarian and bilaterian Frizzled genes may represent a shared ancestral trait.

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Section: Resultsmentioning

confidence: 85%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 95%

Section: Introductionmentioning

confidence: 96%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Sea anemone Frizzled receptors play partially redundant roles in the oral-aboral axis patterning

Niedermoser

Lebedeva

Genikhovich

2022

Preprint

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Highly conserved and extremely evolvable: BMP signalling in secondary axis patterning of Cnidaria and Bilateria

Mörsdorf,

Knabl,

Genikhovich

2024

Dev Genes Evol

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Bilateria encompass the vast majority of the animal phyla. As the name states, they are bilaterally symmetric, that is with a morphologically clear main body axis connecting their anterior and posterior ends, a second axis running between their dorsal and ventral surfaces, and with a left side being roughly a mirror image of their right side. Bone morphogenetic protein (BMP) signalling has widely conserved functions in the formation and patterning of the second, dorso-ventral (DV) body axis, albeit to different extents in different bilaterian species. Whilst initial findings in the fruit fly Drosophila and the frog Xenopus highlighted similarities amongst these evolutionarily very distant species, more recent analyses featuring other models revealed considerable diversity in the mechanisms underlying dorsoventral patterning. In fact, as phylogenetic sampling becomes broader, we find that this axis patterning system is so evolvable that even its core components can be deployed differently or lost in different model organisms. In this review, we will try to highlight the diversity of ways by which BMP signalling controls bilaterality in different animals, some of which do not belong to Bilateria. Future research combining functional analyses and modelling is bound to give us some understanding as to where the limits to the extent of the evolvability of BMP-dependent axial patterning may lie.

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The evolution of complex multicellularity in animals

Kourki

2022

Biol Philos

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The transition to multicellularity is perhaps the best-studied of the “major evolutionary transitions”. It has occurred independently multiple times within the eukaryotes alone, and multicellular organisms comprise virtually the entirety of Earth’s macrobiota. However, the theoretical framework used to study the major evolutionary transitions does not neatly accommodate the evolution of complex multicellularity as a process distinct from the evolution of multicellularity more generally. Here, I attempt to fill this explanatory gap. I will first give an overview of research on the major evolutionary transitions, focusing on multicellularity, and demonstrate that the theoretical framework so far utilised does not provide us with sufficient conceptual tools to explain crucial phenomena that call for explanation, such as the evolution of organs and organ systems. I will then discuss our current understanding of early metazoan evolution as paradigmatically exemplifying the evolution of complex organisation in a multicellular system, specifically regarding three core processes enabling it, namely modularisation, subfunctionalisation, and integration, allowing the provision of a general account of the evolution of complex from simple multicellularity that is potentially applicable to other such cases such as the evolution of land plants. This paves the way for a revised account of major evolutionary transitions which incorporates the evolution of complex organismal traits following the evolution of minimal autonomous reproducers while marking a shift of emphasis from reproducers to organisms.

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Cnidarian-bilaterian comparison reveals the ancestral regulatory logic of the β-catenin dependent axial patterning

Cited by 32 publications

References 65 publications

Sea anemone Frizzled receptors play partially redundant roles in the oral-aboral axis patterning

Sea anemone Frizzled receptors play partially redundant roles in the oral-aboral axis patterning

Highly conserved and extremely evolvable: BMP signalling in secondary axis patterning of Cnidaria and Bilateria

The evolution of complex multicellularity in animals

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