Click
here to close Hello! We notice that
you are using Internet Explorer, which is not supported by Echinobase
and may cause the site to display incorrectly. We suggest using a
current version of Chrome,
FireFox,
or Safari.
BMC Evol Biol
2018 Dec 27;181:203. doi: 10.1186/s12862-018-1307-x.
Show Gene links
Show Anatomy links
Two more Posterior Hox genes and Hox cluster dispersal in echinoderms.
Szabó R
,
Ferrier DEK
.
???displayArticle.abstract???
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 stars, sea cucumbers, feather stars and brittle stars) possess one of the most unusual body plans in the animal kingdom with pronounced pentameral symmetry in the adults. Consequently, much interest has focused on their development, evolution and the role of the Hox genes in these processes. In this context, the organisation of echinoderm Hox gene clusters is distinctive. Within the classificatory system of Duboule, echinoderms constitute one of the clearest examples of Disorganized (D) clusters (i.e. intact clusters but with a gene order or orientation rearranged relative to the ancestral state).
RESULTS: Here we describe two Hox genes (Hox11/13d and e) that have been overlooked in most previous work and have not been considered in reconstructions of echinoderm Hox complements and cluster organisation. The two genes are related to Posterior Hox genes and are present in all classes of echinoderm. Importantly, they do not reside in the Hox cluster of any species for which genomic linkage data is available.
CONCLUSION: Incorporating the two neglected Posterior Hox genes into assessments of echinoderm Hox gene complements and organisation shows that these animals in fact have Split (S) Hox clusters rather than simply Disorganized (D) clusters within the Duboule classification scheme. This then has implications for how these genes are likely regulated, with them no longer covered by any potential long-range Hox cluster-wide, or multigenic sub-cluster, regulatory mechanisms.
Fig. 1. Schematic phylogenetic tree of Ambulacraria with chordates shown as the outgroup. Species used in this study are indicated in brackets next to their respective clades. Species abbreviations: Acpl, Acanthaster planci, Anja, Anneissia japonica, Apja, Apostichopus japonicus, Basi, Balanoglossus simodensis, Brfl, Branchiostoma floridae, Cami, Callorhinchus milii, Lame, Latimeria menadoensis, Lyva, Lytechinus variegatus, Mero, Metacrinus rotundus, Opsp, Ophiothrix spiculata, Pami, Patiria miniata, Papa, Parastichopus parvimensis, Peja, Peronella japonica, Ptfl, Ptychodera flava, Sako, Saccoglossus kowalevskii, Stpu, Strongylocentrotus purpuratus. Tree topology follows [61]
Fig. 2. Alignment of echinoderm Hox11/13b+ homeodomains and flanking sequences. Identities to S. purpuratus are marked with dots. Potentially diagnostic residues within the homeodomain are highlighted in grey. Flanking sequences (N- and C-peptides) are separated from the homeodomain by a space. The misidentified “Hox11/13c†sequence from ref. [30] is boxed. Species abbreviations: Anja = Anneissia japonica, Mero = Metacrinus rotundus, Opsp = Ophiothrix spiculata, Pami = Patiria miniata, Papa = Parastichopus parvimensis, Peja = Peronella japonica, Stpu = Strongylocentrotus purpuratus
Fig. 3. Bayesian tree of ANTP class homeodomains from amphioxus, beetle and sea urchin. The dark grey box indicates the Hox/ParaHox clade; Posterior Hox genes are highlighted in light grey and Hox11/13d and e are bolded and boxed. Support values above 50% from the Bayesian, maximum likelihood and NJ analyses are indicated next to the branches. Species abbreviations as before; Trca = Tribolium castaneum
Fig. 4. Bayesian tree of selected deuterostome Posterior Hox homeodomains and flanking sequences. Grey highlights indicate Hox11/13d and e, and the box shows the position of “Hox11/13c†from P. japonica within our Hox11/13d clade
Fig. 5. Non-Hox neighbours of Hox11/13d-e. a. Genomic scaffolds containing Hox11/13d. b. Genomic scaffolds containing Hox11/13e. Scale is indicated by the rulers on each scaffold. Scaffolds with reversed rulers have been flipped so that all Hox genes are shown in the same orientation. For sea cucumbers, the species with the most conserved neighbours is shown. The neighbourhood shown for Opsp-Hox11/13d is a composite of two overlapping scaffolds. Gene names prefixed with two-letter species abbreviations are taken directly from Echinobase annotations. Other gene names are based on Genbank annotations, BLAST hits and conserved domain content
Fig. 6. Potential diagnostic motifs from the non-homeodomain exons of echinoderm Hox11/13b-d. a. Motifs specific to Hox11/13b. b. Motif specific to Hox11/13c. c. Motifs specific to Hox11/13d. Logos were constructed from curated alignments of all echinoderm examples of each motif. For more information see Results and Additional files 3 and 4
Arenas-Mena,
Expression of the Hox gene complex in the indirect development of a sea urchin.
1998, Pubmed,
Echinobase
Arenas-Mena,
Expression of the Hox gene complex in the indirect development of a sea urchin.
1998,
Pubmed
,
Echinobase
Arenas-Mena,
Spatial expression of Hox cluster genes in the ontogeny of a sea urchin.
2000,
Pubmed
,
Echinobase
Aronowicz,
Hox gene expression in the hemichordate Saccoglossus kowalevskii and the evolution of deuterostome nervous systems.
2006,
Pubmed
Bailey,
Fitting a mixture model by expectation maximization to discover motifs in biopolymers.
1994,
Pubmed
Bailey,
MEME SUITE: tools for motif discovery and searching.
2009,
Pubmed
Baughman,
Genomic organization of Hox and ParaHox clusters in the echinoderm, Acanthaster planci.
2014,
Pubmed
,
Echinobase
Brauchle,
Xenacoelomorpha Survey Reveals That All 11 Animal Homeobox Gene Classes Were Present in the First Bilaterians.
2018,
Pubmed
Byrne,
Evolution of a pentameral body plan was not linked to translocation of anterior Hox genes: the echinoderm HOX cluster revisited.
2016,
Pubmed
,
Echinobase
Cameron,
Unusual gene order and organization of the sea urchin hox cluster.
2006,
Pubmed
,
Echinobase
Cannon,
Phylogenomic resolution of the hemichordate and echinoderm clade.
2014,
Pubmed
,
Echinobase
Cannon,
Xenacoelomorpha is the sister group to Nephrozoa.
2016,
Pubmed
Cook,
The Hox gene complement of acoel flatworms, a basal bilaterian clade.
2004,
Pubmed
Crooks,
WebLogo: a sequence logo generator.
2004,
Pubmed
David,
How Hox genes can shed light on the place of echinoderms among the deuterostomes.
2014,
Pubmed
,
Echinobase
Delroisse,
De Novo Adult Transcriptomes of Two European Brittle Stars: Spotlight on Opsin-Based Photoreception.
2016,
Pubmed
,
Echinobase
Duboule,
The rise and fall of Hox gene clusters.
2007,
Pubmed
DuBuc,
Hox and Wnt pattern the primary body axis of an anthozoan cnidarian before gastrulation.
2018,
Pubmed
Ferrier,
The origin of the Hox/ParaHox genes, the Ghost Locus hypothesis and the complexity of the first animal.
2016,
Pubmed
Ferrier,
The amphioxus Hox cluster: deuterostome posterior flexibility and Hox14.
2000,
Pubmed
Freeman,
Identical genomic organization of two hemichordate hox clusters.
2012,
Pubmed
,
Echinobase
Fritzsch,
PCR survey of Xenoturbella bocki Hox genes.
2008,
Pubmed
Guindon,
New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0.
2010,
Pubmed
Hara,
Expression patterns of Hox genes in larvae of the sea lily Metacrinus rotundus.
2006,
Pubmed
,
Echinobase
Hejnol,
Coordinated spatial and temporal expression of Hox genes during embryogenesis in the acoel Convolutriloba longifissura.
2009,
Pubmed
Holland,
The amphioxus genome illuminates vertebrate origins and cephalochordate biology.
2008,
Pubmed
Howard-Ashby,
Identification and characterization of homeobox transcription factor genes in Strongylocentrotus purpuratus, and their expression in embryonic development.
2006,
Pubmed
,
Echinobase
Hui,
Extensive chordate and annelid macrosynteny reveals ancestral homeobox gene organization.
2012,
Pubmed
Ikuta,
Ambulacrarian prototypical Hox and ParaHox gene complements of the indirect-developing hemichordate Balanoglossus simodensis.
2009,
Pubmed
,
Echinobase
Jimenez-Guri,
Hox and ParaHox genes in Nemertodermatida, a basal bilaterian clade.
2006,
Pubmed
Jo,
Erratum to: Draft genome of the sea cucumber Apostichopus japonicus and genetic polymorphism among color variants.
2017,
Pubmed
,
Echinobase
Katoh,
Parallelization of the MAFFT multiple sequence alignment program.
2010,
Pubmed
Keane,
Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified.
2006,
Pubmed
Kudtarkar,
Echinobase: an expanding resource for echinoderm genomic information.
2017,
Pubmed
Kumar,
MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets.
2016,
Pubmed
Kuraku,
Noncanonical role of Hox14 revealed by its expression patterns in lamprey and shark.
2008,
Pubmed
Lanfear,
Are the deuterostome posterior Hox genes a fast-evolving class?
2010,
Pubmed
Marchler-Bauer,
CDD/SPARCLE: functional classification of proteins via subfamily domain architectures.
2017,
Pubmed
Monteiro,
Hox genes are not always Colinear.
2006,
Pubmed
Moreno,
Tracking the origins of the bilaterian Hox patterning system: insights from the acoel flatworm Symsagittifera roscoffensis.
2009,
Pubmed
Pascual-Anaya,
Broken colinearity of the amphioxus Hox cluster.
2012,
Pubmed
Peterson,
Isolation of Hox and Parahox genes in the hemichordate Ptychodera flava and the evolution of deuterostome Hox genes.
2004,
Pubmed
Philippe,
Acoelomorph flatworms are deuterostomes related to Xenoturbella.
2011,
Pubmed
,
Echinobase
Philippe,
Acoel flatworms are not platyhelminthes: evidence from phylogenomics.
2007,
Pubmed
Powers,
Evidence for a Hox14 paralog group in vertebrates.
2004,
Pubmed
Ronquist,
MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space.
2012,
Pubmed
Seo,
Hox cluster disintegration with persistent anteroposterior order of expression in Oikopleura dioica.
2004,
Pubmed
Shen,
The Abd-B-like Hox homeodomain proteins can be subdivided by the ability to form complexes with Pbx1a on a novel DNA target.
1997,
Pubmed
Simakov,
Hemichordate genomes and deuterostome origins.
2015,
Pubmed
,
Echinobase
Stewart,
De novo assembly of the transcriptome of Acanthaster planci testes.
2015,
Pubmed
,
Echinobase
Thomas-Chollier,
A non-tree-based comprehensive study of metazoan Hox and ParaHox genes prompts new insights into their origin and evolution.
2010,
Pubmed
Tsuchimoto,
Hox expression in the direct-type developing sand dollar Peronella japonica.
2014,
Pubmed
,
Echinobase
Tu,
Quantitative developmental transcriptomes of the sea urchin Strongylocentrotus purpuratus.
2014,
Pubmed
,
Echinobase
Tu,
Gene structure in the sea urchin Strongylocentrotus purpuratus based on transcriptome analysis.
2012,
Pubmed
,
Echinobase
Waterhouse,
Jalview Version 2--a multiple sequence alignment editor and analysis workbench.
2009,
Pubmed
Zhang,
The sea cucumber genome provides insights into morphological evolution and visceral regeneration.
2017,
Pubmed
,
Echinobase
Zhong,
HomeoDB2: functional expansion of a comparative homeobox gene database for evolutionary developmental biology.
2011,
Pubmed
