scholarly journals Hex Hox: De Novo Transcriptome Assembly and Embryonic Hox Gene Expression in the Burrowing Mayfly Hexagenia Limbata (Ephemeridae)

Author(s):  
Christopher J Gonzalez ◽  
Tobias R Hildebrandt ◽  
Brigid C O'Donnell

Abstract Background: Hox genes are key regulators of appendage development in the insect body plan. The body plan of Mayfly (Ephemeroptera) nymphs differs due to the presence of evolutionarily significant abdominal appendages called gills. Despite mayflies’ basal phylogenetic position and novel morphology amongst insects, little is known of their developmental genetics. Here we present an annotated transcriptome for the mayfly Hexagenia limbata, with annotated sequences for putative Hox peptides and embryonic expression profiles for the Hox genes Antp and Ubx/abd-A. Results: Transcriptomic sequencing of early instar H. limbata nymphs yielded a high-quality assembly of 83,795 contigs, of which 22,975 were annotated against Folsomia candida, Nilaparvata lugens, Zootermopsis nevadensis and UniRef90 protein databases. Peptide annotations included eight of the ten canonical Hox genes (lab, pb, Dfd, Scr, Antp, Ubx, abd-A and Abd-B), most of which contained all functional domains and motifs conserved in insects. Expression patterns of Antp and Ubx/abd-A in H. limbata were visualized from early to late embryogenesis, and are also highly conserved with patterns reported for other non-holometabolous insects.Conclusions: We present evidence that both H. limbata Hox peptide sequences and embryonic expression patterns for Antp and Ubx/abd-A are extensively conserved with other insects. These findings suggest mayfly Antp and Ubx/abd-A play similar appendage promoting and repressing roles in the thorax and abdomen, respectively. The identified expression of Ubx and abd-A in early instar nymphs further suggests that mayfly gill development is not subject to Ubx or abd-A repression. Previous studies have shown that insect Ubx and abd-A repress appendages by inhibiting their distal structures, which can permit the development of proximal appendage types. In line with past morphology-based work, we propose that mayfly gills are proximal appendage structures, possibly homologous to the proximal appendage structures of crustaceans.

Development ◽  
2002 ◽  
Vol 129 (5) ◽  
pp. 1225-1238 ◽  
Author(s):  
Cynthia L. Hughes ◽  
Thomas C. Kaufman

The diversity of the arthropod body plan has long been a fascinating subject of study. A flurry of recent research has analyzed Hox gene expression in various arthropod groups, with hopes of gaining insight into the mechanisms that underlie their evolution. The Hox genes have been analyzed in insects, crustaceans and chelicerates. However, the expression patterns of the Hox genes have not yet been comprehensively analyzed in a myriapod. We present the expression patterns of the ten Hox genes in a centipede, Lithobius atkinsoni, and compare our results to those from studies in other arthropods. We have three major findings. First, we find that Hox gene expression is remarkably dynamic across the arthropods. The expression patterns of the Hox genes in the centipede are in many cases intermediate between those of the chelicerates and those of the insects and crustaceans, consistent with the proposed intermediate phylogenetic position of the Myriapoda. Second, we found two ‘extra’ Hox genes in the centipede compared with those in Drosophila. Based on its pattern of expression, Hox3 appears to have a typical Hox-like role in the centipede, suggesting that the novel functions of the Hox3 homologs zen and bicoid were adopted somewhere in the crustacean-insect clade. In the centipede, the expression of the gene fushi tarazu suggests that it has both a Hox-like role (as in the mite), as well as a role in segmentation (as in insects). This suggests that this dramatic change in function was achieved via a multifunctional intermediate, a condition maintained in the centipede. Last, we found that Hox expression correlates with tagmatic boundaries, consistent with the theory that changes in Hox genes had a major role in evolution of the arthropod body plan.


Author(s):  
Ruben Plöger ◽  
Christoph Viebahn

AbstractThe anterior-posterior axis is a central element of the body plan and, during amniote gastrulation, forms through several transient domains with specific morphogenetic activities. In the chick, experimentally proven activity of signalling molecules and transcription factors lead to the concept of a ‘global positioning system’ for initial axis formation whereas in the (mammotypical) rabbit embryo, a series of morphological or molecular domains are part of a putative ‘three-anchor-point model’. Because circular expression patterns of genes involved in axis formation exist in both amniote groups prior to, and during, gastrulation and may thus be suited to reconcile these models, the expression patterns of selected genes known in the chick, namely the ones coding for the transcription factors eomes and tbx6, the signalling molecule wnt3 and the wnt inhibitor pkdcc, were analysed in the rabbit embryonic disc using in situ hybridisation and placing emphasis on their germ layer location. Peripheral wnt3 and eomes expression in all layers is found initially to be complementary to central pkdcc expression in the hypoblast during early axis formation. Pkdcc then appears — together with a posterior-anterior gradient in wnt3 and eomes domains — in the epiblast posteriorly before the emerging primitive streak is marked by pkdcc and tbx6 at its anterior and posterior extremities, respectively. Conserved circular expression patterns deduced from some of this data may point to shared mechanisms in amniote axis formation while the reshaping of localised gene expression patterns is discussed as part of the ‘three-anchor-point model’ for establishing the mammalian body plan.


2019 ◽  
Vol 10 (2) ◽  
pp. 443-454
Author(s):  
Chang Liu ◽  
Cornelius Tlotliso Sello ◽  
Yujian Sui ◽  
Jingtao Hu ◽  
Shaokang Chen ◽  
...  

In order to enrich the Anser cygnoides genome and identify the gene expression profiles of primary and secondary feather follicles development, de novo transcriptome assembly of skin tissues was established by analyzing three developmental stages at embryonic day 14, 18, and 28 (E14, E18, E28). Sequencing output generated 436,730,608 clean reads from nine libraries and de novo assembled into 56,301 unigenes. There were 2,298, 9,423 and 12,559 unigenes showing differential expression in three stages respectively. Furthermore, differentially expressed genes (DEGs) were functionally classified according to genes ontology (GO), Kyoto Encyclopedia of Genes and Genomes (KEGG), and series-cluster analysis. Relevant specific GO terms such as epithelium development, regulation of keratinocyte proliferation, morphogenesis of an epithelium were identified. In all, 15,144 DEGs were clustered into eight profiles with distinct expression patterns and 2,424 DEGs were assigned to 198 KEGG pathways. Skin development related pathways (mitogen-activated protein kinase signaling pathway, extra-cellular matrix -receptor interaction, Wingless-type signaling pathway) and genes (delta like canonical Notch ligand 1, fibroblast growth factor 2, Snail family transcriptional repressor 2, bone morphogenetic protein 6, polo like kinase 1) were identified, and eight DEGs were selected to verify the reliability of transcriptome results by real-time quantitative PCR. The findings of this study will provide the key insights into the complicated molecular mechanism and breeding techniques underlying the developmental characteristics of skin and feather follicles in Anser cygnoides.


2018 ◽  
Vol 285 (1881) ◽  
pp. 20180296 ◽  
Author(s):  
Pei-Yun Cong ◽  
Thomas H. P. Harvey ◽  
Mark Williams ◽  
David J. Siveter ◽  
Derek J. Siveter ◽  
...  

Chancelloriids are an extinct group of spiny Cambrian animals of uncertain phylogenetic position. Despite their sponge-like body plan, their spines are unlike modern sponge spicules, but share several features with the sclerites of certain Cambrian bilaterians, notably halkieriids. However, a proposed homology of these ‘coelosclerites' implies complex transitions in body plan evolution. A new species of chancelloriid, Allonnia nuda , from the lower Cambrian (Stage 3) Chengjiang Lagerstätte is distinguished by its large size and sparse spination, with modified apical sclerites surrounding an opening into the body cavity. The sclerite arrangement in A. nuda and certain other chancelloriids indicates that growth involved sclerite addition in a subapical region, thus maintaining distinct zones of body sclerites and apical sclerites. This pattern is not seen in halkieriids, but occurs in some modern calcarean sponges. With scleritome assembly consistent with a sponge affinity, and in the absence of cnidarian- or bilaterian-grade features, it is possible to interpret chancelloriids as sponges with an unusually robust outer epithelium, strict developmental control of body axis formation, distinctive spicule-like structures and, by implication, minute ostia too small to be resolved in fossils. In this light, chancelloriids may contribute to the emerging picture of high disparity among early sponges.


1995 ◽  
Vol 349 (1329) ◽  
pp. 313-319 ◽  

Homeobox genes encode transcription factors that carry out diverse roles during development. They are widely distributed among eukaryotes, but appear to have undergone an extensive radiation in the earliest metazoa, to generate a range of homeobox subclasses now shared between diverse metazoan phyla. The Hox genes comprise one of these subfamilies, defined as much by conserved chromosomal organization and expression as by sequence characteristics. These Hox genes act as markers of position along the antero—posterior axis of the body in nematodes, arthropods, chordates, and by implication, most other triploblastic phyla. In the arthropods this role is visualized most clearly in the control of segment identity. Exactly how Hox genes control the structure of segments is not yet understood, but their differential deployment between segments provides a model for the basis of segment diversity. Within the arthropods, distantly related taxonomic groups with very different body plans (insects, crustaceans) may share the same set of Hox genes. The expression of these Hox genes provides a new character to define the homology of different body regions. Comparisons of Hox gene deployment between insects and a branchiopod crustacean suggest a novel model for the derivation of the insect body plan.


F1000Research ◽  
2016 ◽  
Vol 5 ◽  
pp. 859 ◽  
Author(s):  
Steven M. Hrycaj ◽  
Deneen M. Wellik

Hox proteins are a deeply conserved group of transcription factors originally defined for their critical roles in governing segmental identity along the antero-posterior (AP) axis in Drosophila. Over the last 30 years, numerous data generated in evolutionarily diverse taxa have clearly shown that changes in the expression patterns of these genes are closely associated with the regionalization of the AP axis, suggesting that Hox genes have played a critical role in the evolution of novel body plans within Bilateria. Despite this deep functional conservation and the importance of these genes in AP patterning, key questions remain regarding many aspects of Hox biology. In this commentary, we highlight recent reports that have provided novel insight into the origins of the mammalian Hox cluster, the role of Hox genes in the generation of a limbless body plan, and a novel putative mechanism in which Hox genes may encode specificity along the AP axis. Although the data discussed here offer a fresh perspective, it is clear that there is still much to learn about Hox biology and the roles it has played in the evolution of the Bilaterian body plan.


Development ◽  
2000 ◽  
Vol 127 (21) ◽  
pp. 4631-4643 ◽  
Author(s):  
C. Arenas-Mena ◽  
A.R. Cameron ◽  
E.H. Davidson

The Hox cluster of the sea urchin Strongylocentrous purpuratus contains ten genes in a 500 kb span of the genome. Only two of these genes are expressed during embryogenesis, while all of eight genes tested are expressed during development of the adult body plan in the larval stage. We report the spatial expression during larval development of the five ‘posterior’ genes of the cluster: SpHox7, SpHox8, SpHox9/10, SpHox11/13a and SpHox11/13b. The five genes exhibit a dynamic, largely mesodermal program of expression. Only SpHox7 displays extensive expression within the pentameral rudiment itself. A spatially sequential and colinear arrangement of expression domains is found in the somatocoels, the paired posterior mesodermal structures that will become the adult perivisceral coeloms. No such sequential expression pattern is observed in endodermal, epidermal or neural tissues of either the larva or the presumptive juvenile sea urchin. The spatial expression patterns of the Hox genes illuminate the evolutionary process by which the pentameral echinoderm body plan emerged from a bilateral ancestor.


Development ◽  
2000 ◽  
Vol 127 (11) ◽  
pp. 2239-2249 ◽  
Author(s):  
A. Abzhanov ◽  
T.C. Kaufman

Representatives of the Insecta and the Malacostraca (higher crustaceans) have highly derived body plans subdivided into several tagma, groups of segments united by a common function and/or morphology. The tagmatization of segments in the trunk, the part of the body between head and telson, in both lineages is thought to have evolved independently from ancestors with a distinct head but a homonomous, undifferentiated trunk. In the branchiopod crustacean, Artemia franciscana, the trunk Hox genes are expressed in broad overlapping domains suggesting a conserved ancestral state (Averof, M. and Akam, M. (1995) Nature 376, 420–423). In comparison, in insects, the Antennapedia-class genes of the homeotic clusters are more regionally deployed into distinct domains where they serve to control the morphology of the different trunk segments. Thus an originally Artemia-like pattern of homeotic gene expression has apparently been modified in the insect lineage associated with and perhaps facilitating the observed pattern of tagmatization. Since insects are the only arthropods with a derived trunk tagmosis tested to date, we examined the expression patterns of the Hox genes Antp, Ubx and abd-A in the malacostracan crustacean Porcellio scaber (Oniscidae, Isopoda). We found that, unlike the pattern seen in Artemia, these genes are expressed in well-defined discrete domains coinciding with tagmatic boundaries which are distinct from those of the insects. Our observations suggest that, during the independent tagmatization in insects and malacostracan crustaceans, the homologous ‘trunk’ genes evolved to perform different developmental functions. We also propose that, in each lineage, the changes in Hox gene expression pattern may have been important in trunk tagmatization.


Blood ◽  
2005 ◽  
Vol 106 (11) ◽  
pp. 2989-2989
Author(s):  
Harry A. Drabkin ◽  
Vivian Ruvolo ◽  
Sharvari Gadgil ◽  
Wenjing Chen ◽  
Chan Zeng ◽  
...  

Abstract The homeodomain genes comprise a set of transcription factors that determine cell fate by regulating proliferation, development, and apoptosis. Humans have 39 class I homeodomain genes (HOX) that occur in four clusters (HOXA, HOXB, HOXC, and HOXD). During development HOX expression takes place according to the position of a gene within its cluster and the position of the cell along the anterior - posterior axis. Some HOX genes are expressed in adult tissues, where they are thought to regulate the regenerative differentiation of cells. If one were to view leukemia as a disorder of regenerative hematopoesis, one could hypothesize that dysregulation of HOX expression promotes leukemogenesis. The role of some homeodomain genes in acute leukemia has been especially well studied. In mouse model systems, overexpression of HOXA7, HOXA9 and Meis1 lead to AML. Chromosomal translocations targeting HOX and other homeodomain genes are associated with acute myeloid and lymphoid leukemias. Previous results have suggested that HOX expression patterns might define certain AML subsets. In the present study, we analyzed the expression of 40 homeodomain genes, among them 25 of the HOXA-D genes, in leukemic enriched samples from 66 patients with de novo AML and in sorted CD34+ cells derived from four healthy bone marrow donors. Also, in order to integrate any effects of mutations in FLT3, C/EBPa, and nucleophosmin (NPM) on HOX expression, we assessed the presence of mutations in these three genes. Our results demonstrate that HOX expression patterns are intimately linked to particular cytogenetic abnormalities. The most striking overall findings were the overexpression of HOXA and HOXB genes in AMLs with NPM mutations, the similarity of HOX expression in AMLs with unfavorable cytogenetics to that of AMLs with intermediate cytogenetics, and the downregulation of HOXA genes in core binding factor (CBF) AMLs. Moreover, AMLs with translocations involving CBFbeta had distinctly higher expression of HOXB2, HOXB3, HOXB4, and Meis 1 than did patients with translocations involving CBFalpha. Some HOX genes displayed no heterogeneity of expression and are thus likely unrelated to leukemogenesis. Other genes, particularly HOXA and HOXB genes, displayed marked heterogeneity of expression and thus may have a role in leukemogenesis. However, every AML had substantial differences in the expression of at least one HOX gene compared to normal CD34+ cells. In addition, levels of HOX expression distinguished within individual cytogenetic groups certain subsets, including cases with inv(16) and cases that phenotypically resembled NPM mutations. Based on these results and the causative nature of HOX deregulation in some acute leukemias, we postulate that the HOX expression patterns exemplified here may be responsible for some (or many) of the biologic differences observed among the major cytogenetic prognostic groups.


2019 ◽  
Vol 9 (1) ◽  
Author(s):  
Chase D. Brownstein

Abstract The evolution of birds from dinosaurs is a subject that has received great attention among vertebrate paleontologists. Nevertheless, the early evolution of the paravians, the group that contains birds and their closest non-avian dinosaur relatives, remains very poorly known. Even the most basal members of one paravian lineage, the Dromaeosauridae, already show a body plan that differs substantially from their closest non-paravian relatives. Recently, the dromaeosaurid Halszkaraptor escuilliei was described from the Cretaceous of Mongolia. Halszkaraptor possesses numerous unserrated premaxillary teeth, a platyrostral rostrum with a developed neurovascular system, an elongate neck, bizarrely-proportioned forearms, and a foreword-shifted center of mass, differing markedly from other paravians. A reevaluation of the anatomy, taphonomy, environmental setting, and phylogenetic position of H. escuilliei based on additional comparisons with other maniraptorans suggests that, rather than indicating it was a semiaquatic piscivore, the body plan of this dinosaur bears features widely distributed among maniraptorans and in some cases intermediate between the conditions in dromaeosaurids and related clades. I find no evidence for a semiaquatic lifestyle in Halszkaraptor. A phylogenetic reevaluation of Halszkaraptorinae places it as the sister clade to Unenlagiinae, indicating the bizarre features of unenlagiines previously interpreted as evidence of piscivory may also represent a mosaic of plesiomorphic, derived, and intermediate features. The anatomy of Halszkaraptor reveals that dromaeosaurids still possessed many features found in more basal maniraptoran and coelurosaur clades, including some that may have been tied to herbivory. Rather than being a semiaquatic piscavore, Halszkaraptor was a basal dromaeosaurid showing transitional features.


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