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Hox and Wnt pattern the primary body axis of an anthozoan cnidarian before gastrulation

Published on Dec 1, 2018in Nature Communications 11.88
· DOI :10.1038/s41467-018-04184-x
Timothy Q. DuBuc7
Estimated H-index: 7
(National University of Ireland, Galway),
Thomas B. Stephenson1
Estimated H-index: 1
(UF: University of Florida)
+ 1 AuthorsMark Q. Martindale58
Estimated H-index: 58
(UF: University of Florida)
Cite
Abstract
Hox gene transcription factors are important regulators of positional identity along the anterior–posterior axis in bilaterian animals. Cnidarians (e.g., sea anemones, corals, and hydroids) are the sister group to the Bilateria and possess genes related to both anterior and central/posterior class Hox genes. Here we report a previously unrecognized domain of Hox expression in the starlet sea anemone, Nematostella vectensis, beginning at early blastula stages. We explore the relationship of two opposing Hox genes (NvAx6/NvAx1) expressed on each side of the blastula during early development. Functional perturbation reveals that NvAx6 and NvAx1 not only regulate their respective expression domains, but also interact with Wnt genes to pattern the entire oral–aboral axis. These findings suggest an ancient link between Hox/Wnt patterning during axis formation and indicate that oral–aboral domains are likely established during blastula formation in anthozoan cnidarians.
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  • References (68)
  • Citations (9)
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References68
Newest
Published on Aug 15, 2017in Development 5.76
Marc D. Servetnick2
Estimated H-index: 2
(UW: University of Washington),
Bailey Steinworth1
Estimated H-index: 1
(Whitney Laboratory for Marine Bioscience)
+ 3 AuthorsMark Q. Martindale58
Estimated H-index: 58
(Whitney Laboratory for Marine Bioscience)
The mesoderm was a key novelty in animal evolution, though we understand little of how mesoderm arose. brachyury , the founding member of the T-box gene family, is a key gene in chordate mesoderm development. However, the brachyury gene was present in the common ancestor of fungi and animals, long before mesoderm appeared. To explore ancestral roles of brachyury prior to the evolution of definitive mesoderm, we excised the gene using CRISPR/Cas9 in the diploblastic cnidarian Nematostella vectens...
Naveen Wijesena1
Estimated H-index: 1
(UF: University of Florida),
David Simmons43
Estimated H-index: 43
(UF: University of Florida),
Mark Q. Martindale58
Estimated H-index: 58
(UF: University of Florida)
Abstract Gastrulation was arguably the key evolutionary innovation that enabled metazoan diversification, leading to the formation of distinct germ layers and specialized tissues. Differential gene expression specifying cell fate is governed by the inputs of intracellular and/or extracellular signals. Beta-catenin/Tcf and the TGF-beta bone morphogenetic protein (BMP) provide critical molecular signaling inputs during germ layer specification in bilaterian metazoans, but there has been no direct ...
Sabrina M. Schiemann2
Estimated H-index: 2
(University of Bergen),
José M. Martín-Durán14
Estimated H-index: 14
(University of Bergen)
+ 3 AuthorsAndreas Hejnol25
Estimated H-index: 25
(University of Bergen)
Temporal collinearity is often considered the main force preserving Hox gene clusters in animal genomes. Studies that combine genomic and gene expression data are scarce, however, particularly in invertebrates like the Lophotrochozoa. As a result, the temporal collinearity hypothesis is currently built on poorly supported foundations. Here we characterize the complement, cluster, and expression of Hox genes in two brachiopod species, Terebratalia transversa and Novocrania anomala . T. transversa...
Published on Nov 1, 2016in Current Biology 9.19
Yuuri Yasuoka8
Estimated H-index: 8
(OIST: Okinawa Institute of Science and Technology),
Chuya Shinzato17
Estimated H-index: 17
(OIST: Okinawa Institute of Science and Technology),
Noriyuki Satoh47
Estimated H-index: 47
(OIST: Okinawa Institute of Science and Technology)
Summary Blastoporal expression of the T-box transcription factor gene brachyury is conserved in most metazoans [1, 2]. Its role in mesoderm formation has been intensively studied in vertebrates [3–6]. However, its fundamental function near the blastopore is poorly understood in other phyla. Cnidarians are basal metazoans that are important for understanding evolution of metazoan body plans [7, 8]. Because they lack mesoderm, they have been used to investigate the evolutionary origins of mesoderm...
Published on May 15, 2016in Development 5.76
Lucas Leclère14
Estimated H-index: 14
(University of Bergen),
Markus Bause1
Estimated H-index: 1
(University of Bergen)
+ 2 AuthorsFabian Rentzsch23
Estimated H-index: 23
(University of Bergen)
The development of the oral pole in cnidarians and the posterior pole in bilaterians is regulated by canonical Wnt signaling, whereas a set of transcription factors, including Six3/6 and FoxQ2, controls aboral development in cnidarians and anterior identity in bilaterians. However, it is poorly understood how these two patterning systems are initially set up in order to generate correct patterning along the primary body axis. Investigating the early steps of aboral pole formation in the sea anem...
Published on Jan 1, 2016in Nature Reviews Neuroscience 33.16
Detlev Arendt45
Estimated H-index: 45
,
Maria Antonietta Tosches7
Estimated H-index: 7
,
Heather Marlow5
Estimated H-index: 5
The evolution of complex nervous systems is not well understood. In this Opinion article, Arendt and colleagues discuss comparative gene-expression data that suggest that the bilaterian brain emerged from the integration of distinct integrative centres present on opposite sides of a nerve net.
Published on Dec 1, 2015in Evodevo 2.12
Johanna E. M. Kraus4
Estimated H-index: 4
(University of Vienna),
David Fredman24
Estimated H-index: 24
(University of Bergen)
+ 2 AuthorsUlrich Technau39
Estimated H-index: 39
(University of Vienna)
Background The metagenesis of sessile polyps into pelagic medusae in cnidarians represents one of the most ancient complex life cycles in animals. Interestingly, scyphozoans and hydrozoans generate medusae by apparently fundamentally different processes. It is therefore unclear whether medusa formation has evolved independently in different medusozoans. To this end, a thorough understanding of the correspondence of polyp and medusa is required.
Sebastian Baumgarten11
Estimated H-index: 11
(KAUST: King Abdullah University of Science and Technology),
Oleg Simakov18
Estimated H-index: 18
(Heidelberg University)
+ 12 AuthorsMatt E. Oates12
Estimated H-index: 12
(UoB: University of Bristol)
The most diverse marine ecosystems, coral reefs, depend upon a functional symbiosis between a cnidarian animal host (the coral) and intracellular photosynthetic dinoflagellate algae. The molecular and cellular mechanisms underlying this endosymbiosis are not well understood, in part because of the difficulties of experimental work with corals. The small sea anemone Aiptasia provides a tractable laboratory model for investigating these mechanisms. Here we report on the assembly and analysis of th...
Published on Feb 26, 2015in eLife 7.55
Nicolas Denans1
Estimated H-index: 1
(UDS: University of Strasbourg),
Tadahiro Iimura21
Estimated H-index: 21
(Ehime University),
Olivier Pourquié55
Estimated H-index: 55
In humans and other vertebrates, the number of bones (vertebrae) in the spine is determined early in development. The vertebrae form from blocks of tissue called somites that make segments along the body axis—a virtual line running from the head to the tail-end—of the embryo. The somites form as the embryo increases in length, with new somites forming periodically at the back near the embryo's tail-end. A family of genes called the Hox genes are involved in controlling the formation of the somit...
Published on Sep 1, 2014in Nature Communications 11.88
Sven Leininger10
Estimated H-index: 10
,
Marcin Adamski22
Estimated H-index: 22
+ 9 AuthorsSigne Jordal2
Estimated H-index: 2
The current prevailing view is that body plans of sponges and other animals cannot be compared. Here, the authors identify developmental regulatory genes in the calcisponge, Sycon ciliatum, and report similar developmental gene expression between sponges and cnidarians, which suggests that their body plans are homologous.
Cited By9
Newest
Published on Jul 18, 2019in Mitochondrial DNA
Raissa I. Hogan (National University of Ireland, Galway), Kevin Hopkins2
Estimated H-index: 2
(ZSL: Zoological Society of London)
+ 2 AuthorsChris Yesson17
Estimated H-index: 17
(ZSL: Zoological Society of London)
Published on May 1, 2019in Russian Journal of Developmental Biology 0.52
A. M. Nesterenko (MSU: Moscow State University), A. G. Zaraisky (MSU: Moscow State University)
Published on Apr 9, 2019in bioRxiv
Pin Huan12
Estimated H-index: 12
(CAS: Chinese Academy of Sciences),
Qian Wang65
Estimated H-index: 65
(CAS: Chinese Academy of Sciences)
+ 1 AuthorsLIUBaozhong21
Estimated H-index: 21
(CAS: Chinese Academy of Sciences)
Unlike the Hox genes in arthropods and vertebrates, those in molluscs show diverse expression patterns and, with some exceptions, have generally been described as lacking the canonical staggered pattern along the anterior-posterior (AP) axis. This difference is unexpected given that almost all molluscs share highly conserved early development. Here, we show that molluscan Hox expression can undergo dynamic changes, which may explain why previous research observed different expression patterns. M...
Published on Dec 1, 2018in Nature Communications 11.88
Fabian Rentzsch23
Estimated H-index: 23
(University of Bergen),
Thomas W. Holstein34
Estimated H-index: 34
(Heidelberg University)
Distantly related animals have spectacularly different shapes and body plans, which can render it difficult to understand which of their body parts may have a shared evolutionary origin. Studying the molecular regulation of the development of these body parts during embryogenesis can help identifying commonalities that are not visible by eye.
Published on Dec 1, 2018in Genome Biology 14.03
Hua Ying11
Estimated H-index: 11
(ANU: Australian National University),
Ira R. Cooke12
Estimated H-index: 12
(JCU: James Cook University)
+ 7 AuthorsDavid S. Miller71
Estimated H-index: 71
(JCU: James Cook University)
Despite the biological and economic significance of scleractinian reef-building corals, the lack of large molecular datasets for a representative range of species limits understanding of many aspects of their biology. Within the Scleractinia, based on molecular evidence, it is generally recognised that there are two major clades, Complexa and Robusta, but the genomic bases of significant differences between them remain unclear. Draft genome assemblies and annotations were generated for three cor...
Published on Dec 1, 2018in BMC Evolutionary Biology 3.04
Réka Szabó2
Estimated H-index: 2
(St And: University of St Andrews),
David Ferrier33
Estimated H-index: 33
(St And: University of St Andrews)
Background Hox genes are key elements in patterning animal development. They are renowned for their, often, clustered organisation in the genome, with supposed mechanistic links between the organisation of the genes and their expression. The widespread distribution and comparable functions of Hox genes across the animals has led to them being a major study system for comparing the molecular bases for construction and divergence of animal morphologies. Echinoderms (including sea urchins, sea star...
Published on Nov 1, 2018in Current Biology 9.19
Ulrich Technau39
Estimated H-index: 39
(University of Vienna),
Grigory Genikhovich15
Estimated H-index: 15
(University of Vienna)
Summary A new study in a sea anemone shows that, as in bilaterian animals, an axis-patterning Hox code exists in cnidarians. Surprisingly, it acts along the directive axis, orthogonal to the oral–aboral axis.
Published on Sep 28, 2018in Science 41.04
Detlev Arendt45
Estimated H-index: 45