Hox genes and the crustacean body plan

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.

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Exploring the myriapod body plan: expression patterns of the ten Hox genes in a centipede

Development ◽

10.1242/dev.129.5.1225 ◽

2002 ◽

Vol 129 (5) ◽

pp. 1225-1238 ◽

Cited By ~ 1

Author(s):

Cynthia L. Hughes ◽

Thomas C. Kaufman

Keyword(s):

Gene Expression ◽

Hox Genes ◽

Expression Patterns ◽

Body Plan ◽

Phylogenetic Position ◽

The Novel ◽

Fushi Tarazu ◽

Hox Gene ◽

Insight Into ◽

Gaining Insight

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.

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Hox genes and the evolution of diverse body plans

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.1995.0119 ◽

1995 ◽

Vol 349 (1329) ◽

pp. 313-319 ◽

Cited By ~ 69

Keyword(s):

Transcription Factors ◽

Hox Genes ◽

Body Plan ◽

The Body ◽

Chromosomal Organization ◽

Hox Gene ◽

Body Regions ◽

Taxonomic Groups ◽

Novel Model ◽

Sequence Characteristics

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.

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Changes in Hox genes’ structure and function during the evolution of the squamate body plan

Nature ◽

10.1038/nature08789 ◽

2010 ◽

Vol 464 (7285) ◽

pp. 99-103 ◽

Cited By ~ 110

Author(s):

Nicolas Di-Poï ◽

Juan I. Montoya-Burgos ◽

Hilary Miller ◽

Olivier Pourquié ◽

Michel C. Milinkovitch ◽

...

Keyword(s):

Hox Genes ◽

Structure And Function ◽

Body Plan ◽

And Function

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Hox genes and evolution

F1000Research ◽

10.12688/f1000research.7663.1 ◽

2016 ◽

Vol 5 ◽

pp. 859 ◽

Cited By ~ 14

Author(s):

Steven M. Hrycaj ◽

Deneen M. Wellik

Keyword(s):

Hox Genes ◽

Expression Patterns ◽

Critical Role ◽

Body Plan ◽

Functional Conservation ◽

Fresh Perspective ◽

Numerous Data ◽

Segmental Identity ◽

Putative Mechanism

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.

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Evolution of a pentameral body plan was not linked to translocation of anterior Hox genes: the echinoderm HOX cluster revisited

Evolution & Development ◽

10.1111/ede.12172 ◽

2016 ◽

Vol 18 (2) ◽

pp. 137-143 ◽

Cited By ~ 13

Author(s):

Maria Byrne ◽

Pedro Martinez ◽

Valerie Morris

Keyword(s):

Hox Genes ◽

Body Plan ◽

Hox Cluster

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Spatial expression of Hox cluster genes in the ontogeny of a sea urchin

Development ◽

10.1242/dev.127.21.4631 ◽

2000 ◽

Vol 127 (21) ◽

pp. 4631-4643 ◽

Cited By ~ 1

Author(s):

C. Arenas-Mena ◽

A.R. Cameron ◽

E.H. Davidson

Keyword(s):

Sea Urchin ◽

Larval Stage ◽

Hox Genes ◽

Expression Patterns ◽

Evolutionary Process ◽

Body Plan ◽

Hox Cluster ◽

Spatial Expression ◽

Neural Tissues ◽

Adult Body

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.

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