Skip to main content
U.S. Department of Energy
Office of Scientific and Technical Information

Genomic Organization and Expression Demonstrate Spatial and Temporal Hox Gene Colinearity in the Lophotrochozoan Capitella sp. I

Journal Article · · PLoS ONE
 [1];  [2];  [2]
  1. University of Hawaii at Manoa, Honolulu, HI (United States); DOE/OSTI
  2. University of Hawaii at Manoa, Honolulu, HI (United States)

Hox genes define regional identities along the anterior–posterior axis in many animals. In a number of species, Hox genes are clustered in the genome, and the relative order of genes corresponds with position of expression in the body. Previous Hox gene studies in lophotrochozoans have reported expression for only a subset of the Hox gene complement and/or lack detailed genomic organization information, limiting interpretations of spatial and temporal colinearity in this diverse animal clade. We studied expression and genomic organization of the single Hox gene complement in the segmented polychaete annelid Capitella sp. I. Total genome searches identified 11 Hox genes in Capitella, representing 11 distinct paralog groups thought to represent the ancestral lophotrochozoan complement. At least 8 of the 11 Capitella Hox genes are genomically linked in a single cluster, have the same transcriptional orientation, and lack interspersed non-Hox genes. Studying their expression by situ hybridization, we find that the 11 Capitella Hox genes generally exhibit spatial and temporal colinearity. With the exception of CapI-Post1, Capitella Hox genes are all expressed in broad ectodermal domains during larval development, consistent with providing positional information along the anterior–posterior axis. The anterior genes CapIlab, CapI-pb, and CapI-Hox3 initiate expression prior to the appearance of segments, while more posterior genes appear at or soon after segments appear. Many of the Capitella Hox genes have either an anterior or posterior expression boundary coinciding with the thoracic–abdomen transition, a major body tagma boundary. Following metamorphosis, several expression patterns change, including appearance of distinct posterior boundaries and restriction to the central nervous system. Capitella Hox genes have maintained a clustered organization, are expressed in the canonical anterior–posterior order found in other metazoans, and exhibit spatial and temporal colinearity, reflecting Hox gene characteristics that likely existed in the protostome–deuterostome ancestor.

Research Organization:
University of Hawaii at Manoa, Honolulu, HI (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); Damon Runyon Cancer Research Foundation; National Science Foundation (NSF)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1627363
Journal Information:
PLoS ONE, Journal Name: PLoS ONE Journal Issue: 12 Vol. 3; ISSN 1932-6203
Publisher:
Public Library of ScienceCopyright Statement
Country of Publication:
United States
Language:
English

References (72)

The polychaetePlatynereis dumerilii (Annelida): a laboratory animal with spiralian cleavage, lifelong segment proliferation and a mixed benthic/pelagic life cycle journal January 2004
Primary structure and developmental expression pattern of Hox 3.1, a member of the murine Hox 3 homeobox gene cluster. journal May 1988
The structural and functional organization of the murine HOX gene family resembles that of Drosophila homeotic genes. journal May 1989
Expression Patterns of Anterior Hox Genes in the Polychaete Chaetopterus: Correlation with Morphological Boundaries journal January 2000
A Polychaete hunchback Ortholog journal July 2001
ParaHox gene expression in the polychaete annelid Capitella sp. I journal January 2006
Hox gene expression in larval development of the polychaetes Nereis virens and Platynereis dumerilii (Annelida, Lophotrochozoa) journal December 2006
Analysis of the Tribolium homeotic complex: insights into mechanisms constraining insect Hox clusters journal April 2008
Platyhelminthes have a Hox code differentially activated during regeneration, with genes closely related to those of spiralian protostomes journal October 1998
A Hox class 3 orthologue from the spider Cupiennius salei is expressed in a Hox-gene-like fashion journal November 1998
Ultrastructure and formation of hooded hooks in Capitella capitata (Annelida, Capitellida) journal June 1998
Hox genes in vertebrate development journal July 1994
HOM/Hox genes of Artemia: implications for the origin of insect and crustacean body plans journal February 1993
Expression of ‘segmentation’ genes during larval and juvenile development in the polychaetes Capitella sp. I and H. elegans journal January 2006
Notch signaling during larval and juvenile development in the polychaete annelid Capitella sp. I journal August 2008
Hox genes in evolution: protein surfaces and paralog groups journal April 1997
A homoeotic gene cluster in the red flour beetle journal May 1987
Characterization of a homologue of bithorax-complex genes in the leech Hirudo medicinalis journal October 1989
Homeotic genes and the evolution of arthropods and chordates journal August 1995
Cephalopod Hox genes and the origin of morphological novelties journal August 2003
HOX genes in the sepiolid squid Euprymna scolopes: Implications for the evolution of complex body plans journal February 2002
Organization of the Hox gene cluster in the grasshopper, Schistocerca gregaria journal November 1996
Homeobox genes in the ribbonworm Lineus sanguineus: Evolutionary implications journal March 1998
Organization of an echinoderm Hox gene cluster journal February 1999
MRBAYES: Bayesian inference of phylogenetic trees journal August 2001
ProtTest: selection of best-fit models of protein evolution journal January 2005
RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models journal August 2006
Sequence of the Tribolium castaneum Homeotic Complex: The Region Corresponding to the Drosophila melanogaster Antennapedia Complex journal March 2002
Hox gene expression in the hemichordate Saccoglossus kowalevskii and the evolution of deuterostome nervous systems journal October 2006
The Hox gene complement of a pelagic chaetognath, Flaccisagitta enflata journal May 2007
Evidence for a Dispersed Hox Gene Cluster in the Platyhelminth Parasite Schistosoma mansoni journal August 2005
The human HOX gene family journal January 1989
The proboscipedia locus of the Antennapedia complex: a molecular and genetic analysis. journal July 1988
Evolutionary Conservation of Regulatory Elements in Vertebrate Hox Gene Clusters journal May 2003
Growth patterns during segmentation in the two polychaete annelids, Capitella sp. I and Hydroides elegans: comparisons at distinct life history stages journal July 2005
Sibling species in the marine pollution indicator Capitella (polychaeta) journal May 1976
Molecular Genetics of the Bithorax Complex in Drosophila melanogaster journal July 1983
Expression of anterior Hox genes during larval development of the gastropod Haliotis asinina. text January 2003
Duplicated Hox genes in the spider Cupiennius salei journal January 2007
The rise and fall of Hox gene clusters journal June 2007
Retinoic acid signaling acts via Hox1 to establish the posterior limit of the pharynx in the chordate amphioxus journal December 2004
Planarian Hox genes: novel patterns of expression during regeneration journal January 1997
The leech homeobox gene Lox4 may determine segmental differentiation of identified neurons journal August 1995
Combined-method phylogenetic analysis of Hox and ParaHox genes of the metazoa journal January 2000
A new homeo-box is present in overlapping cosmid clones which define the mouse Hox-1 locus. journal August 1986
Unusual gene order and organization of the sea urchin hox cluster
  • Cameron, R. Andrew; Rowen, Lee; Nesbitt, Ryan
  • Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, Vol. 306B, Issue 1 https://doi.org/10.1002/jez.b.21070
journal January 2006
Antennapedia-Class homeobox genes define diverse neuronal sets in the embryonic CNS of the leech journal October 1993
Lox1, an Antennapedia-Class Homeobox Gene, Is Expressed during Leech Gangliogenesis in Both Transient and Stable Central Neurons journal February 1994
Conserved Anterior Boundaries of Hox Gene Expression in the Central Nervous System of the LeechHelobdella journal October 1997
HOM/Hox genes of Artemia: implications for the origin of insect and crustacean body plans journal February 1993
Molecular and Genetic Organization of The Antennapedia Gene Complex of Drosophila melanogaster book January 1990
Hox genes in evolution: protein surfaces and paralog groups journal April 1997
Evidence for the derivation of the Drosophila fushi tarazu gene from a Hox gene orthologous to lophotrochozoan Lox5 journal March 2000
Hox clusters and bilaterian phylogeny journal September 2002
Hox genes in brachiopods and priapulids and protostome evolution journal June 1999
Ancient origin of the Hox gene cluster journal January 2001
Archetypal organization of the amphioxus Hox gene cluster journal August 1994
Hox cluster disintegration with persistent anteroposterior order of expression in Oikopleura dioica journal September 2004
Species identification, phylogenetic analysis and detection of herbicide-resistant biotypes of Amaranthus based on ALS and ITS journal July 2020
Hox genes and the evolution of the arthropod body plan1 journal November 2002
Expression of anterior Hox genes during larval development of the gastropod Haliotis asinina journal September 2003
The amphioxus Hox cluster: deuterostome posterior flexibility and Hox14 journal September 2000
Identification of planarian homeobox sequences indicates the antiquity of most Hox/homeotic gene subclasses. journal August 1995
Hox Genes and Segmental Patterning of the Vertebrate Hindbrain journal September 1998
Characterization of a murine homeo box gene, Hox-2.6, related to the Drosophila Deformed gene. journal November 1988
The Hox gene complement of acoel flatworms, a basal bilaterian clade journal May 2004
Growth patterns during segmentation in the two polychaete annelids, Capitella sp. I and Hydroides elegans: comparisons at distinct life history stages journal July 2005
Developmental expression of foxA and gata genes during gut formation in the polychaete annelid, Capitella sp. I: Gut development in Capitella sp. I journal January 2008
The development of the central nervous system in Capitella capitata (Polychaeta, Annelida) journal October 1982
Expression of anterior Hox genes during larval development of the gastropod Haliotis asinina. text January 2003
Genesis and evolution of the Evx and Moxgenes and the extended Hox and ParaHox gene clusters journal January 2003
The leech homeobox gene Lox4 may determine segmental differentiation of identified neurons journal August 1995

Cited By (39)

Hox and ParaHox gene expression in early body plan patterning of polyplacophoran mollusks
  • Fritsch, Martin; Wollesen, Tim; Wanninger, Andreas
  • Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, Vol. 326, Issue 2 https://doi.org/10.1002/jez.b.22671
journal March 2016
Analysis of central Hox protein types across bilaterian clades: On the diversification of central Hox proteins from an Antennapedia/Hox7-like protein journal November 2013
Hox and Wnt pattern the primary body axis of an anthozoan cnidarian before gastrulation journal May 2018
A draft genome sequence of the elusive giant squid, Architeuthis dux journal January 2020
Staggered Hox expression is more widespread among molluscs than previously appreciated
  • Wollesen, Tim; Rodríguez Monje, Sonia Victoria; Luiz de Oliveira, André
  • Proceedings of the Royal Society B: Biological Sciences, Vol. 285, Issue 1888 https://doi.org/10.1098/rspb.2018.1513
journal October 2018
Hox genes pattern the primary body axis of an anthozoan cnidarian prior to gastrulation journal November 2017
Hox gene expression in postmetamorphic juveniles of the brachiopod Terebratalia transversa posted_content January 2018
Hox gene expression during the development of the phoronid Phoronopsis harmeri posted_content January 2019
A non-tree-based comprehensive study of metazoan Hox and ParaHox genes prompts new insights into their origin and evolution journal January 2010
Identification of an intact ParaHox cluster with temporal colinearity but altered spatial colinearity in the hemichordate Ptychodera flava journal June 2013
Coordinated spatial and temporal expression of Hox genes during embryogenesis in the acoel Convolutriloba longifissura journal October 2009
Expression of the pair-rule gene homologs runt, Pax3/7, even-skipped-1 and even-skipped-2 during larval and juvenile development of the polychaete annelid Capitella teleta does not support a role in segmentation journal January 2012
Hox gene expression during postlarval development of the polychaete Alitta virens journal January 2013
Molecular conservation of metazoan gut formation: evidence from expression of endomesoderm genes in Capitella teleta (Annelida) journal October 2014
Unexpected co-linearity of Hox gene expression in an aculiferan mollusk journal August 2015
Hox genes pattern the anterior-posterior axis of the juvenile but not the larva in a maximally indirect developing invertebrate, Micrura alaskensis (Nemertea) journal April 2015
A Stable Thoracic Hox Code and Epimorphosis Characterize Posterior Regeneration in Capitella teleta journal February 2016
Building a Robust A-P Axis journal May 2012
Additional file 1 of Hooked on zombie worms? Genetic blueprints of bristle formation in Osedax japonicus (Annelida) dataset January 2024
Evolution of homeobox genes: Evolution of homeobox genes journal September 2012
Expression of Hox genes during the larval development of the snail, Gibbula varia (L.)—further evidence of non-colinearity in molluscs journal October 2010
Activation of Hox genes during caudal regeneration of the polychaete annelid Platynereis dumerilii journal May 2012
DNA Methylation Is Crucial for the Early Development in the Oyster C. gigas journal July 2013
Segmental and Regional Differences in Neuronal Expression of the Leech Hox Genes Lox1 and Lox2 During Embryogenesis journal May 2012
Current status of annelid phylogeny journal January 2016
Rotiferan Hox genes give new insights into the evolution of metazoan bodyplans journal April 2017
Scallop genome provides insights into evolution of bilaterian karyotype and development journal April 2017
Nemertean and phoronid genomes reveal lophotrochozoan evolution and the origin of bilaterian heads journal December 2017
Dorsoventral decoupling of Hox gene expression underpins the diversification of molluscs journal December 2019
A Revised Spiralian Homeobox Gene Classification Incorporating New Polychaete Transcriptomes Reveals a Diverse TALE Class and a Divergent Hox Gene journal July 2018
Clustered brachiopod Hox genes are not expressed collinearly and are associated with lophotrochozoan novelties posted_content August 2016
Expression of vasa , piwi , and nanos during gametogenesis in Typosyllis antoni (Annelida, Syllidae) journal August 2018
The segmental pattern of otx, gbx, and Hox genes in the annelid Platynereis dumerilii: The segmental pattern of otx, gbx, and Hox genes journal January 2011
Evolutionary Trends in Hox Cluster Genes Utilization: Whether Common Genes Play by General Rules? journal December 2018
Hox-cluster and evolution of morphogeneses journal September 2010
Hox gene expression in postmetamorphic juveniles of the brachiopod Terebratalia transversa journal January 2019
Hox gene expression during development of the phoronid Phoronopsis harmeri journal February 2020
Hox gene expression during development of the phoronid Phoronopsis harmeri posted_content February 2020
An Overview of Hox Genes in Lophotrochozoa: Evolution and Functionality journal March 2016

Similar Records

Unusual Gene Order and Organization of the Sea Urchin HoxCluster
Journal Article · Tue May 10 00:00:00 EDT 2005 · Journal of Experimental Zoology · OSTI ID:878704

Unusual Gene Order and Organization of the Sea Urchin Hox Cluster
Journal Article · Tue Oct 11 00:00:00 EDT 2005 · Journal of Experimental Zoology Part B: Molecular and Developmental Evolution · OSTI ID:877934