Comprehensive analysis of Hox gene expression in the amphipod crustacean Parhyale hawaiensis

Hox genes play crucial roles in establishing regional identity along the anterior–posterior axis in bilaterian animals, and have been implicated in generating morphological diversity throughout evolution. Here we report the identification, expression, and initial genomic characterization of the complete set of Hox genes from the amphipod crustacean Parhyale hawaiensis. Parhyale is an emerging model system that is amenable to experimental manipulations and evolutionary comparisons among the arthropods. Our analyses indicate that the Parhyale genome contains a single copy of each canonical Hox gene with the exception of fushi tarazu, and preliminary mapping suggests that at least some of these genes are clustered together in the genome. With few exceptions, Parhyale Hox genes exhibit both temporal and spatial colinearity, and expression boundaries correlate with morphological differences between segments and their associated appendages. This work represents the most comprehensive analysis of Hox gene expression in a crustacean to date, and provides a foundation for functional studies aimed at elucidating the role of Hox genes in arthropod development and evolution. & 2015 Elsevier Inc. All rights reserved.

[1]  Thomas K. F. Wong,et al.  Phylogenomics resolves the timing and pattern of insect evolution , 2014, Science.

[2]  Galina A. Erikson,et al.  The First Myriapod Genome Sequence Reveals Conservative Arthropod Gene Content and Genome Organisation in the Centipede Strigamia maritima , 2014, PLoS biology.

[3]  Andrew R. Bassett,et al.  CRISPR/Cas9 mediated genome engineering in Drosophila. , 2014, Methods.

[4]  L. Pick,et al.  Variation and constraint in Hox gene evolution , 2013, Proceedings of the National Academy of Sciences.

[5]  F. Diao,et al.  A Novel Approach for Directing Transgene Expression in Drosophila: T2A-Gal4 In-Frame Fusion , 2012, Genetics.

[6]  P. Beldade,et al.  Involvement of the conserved Hox gene Antennapedia in the development and evolution of a novel trait , 2011, EvoDevo.

[7]  N. Patel,et al.  A prominent requirement for single-minded and the ventral midline in patterning the dorsoventral axis of the crustacean Parhyale hawaiensis , 2010, Development.

[8]  R. Janssen,et al.  Gene expression suggests conserved aspects of Hox gene regulation in arthropods and provides additional support for monophyletic Myriapoda , 2010, EvoDevo.

[9]  C. Amemiya,et al.  BAC library for the amphipod crustacean, Parhyale hawaiensis. , 2010, Genomics.

[10]  J. Shultz,et al.  Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding sequences , 2010, Nature.

[11]  L. Pick,et al.  Surprising flexibility in a conserved Hox transcription factor over 550 million years of evolution , 2010, Proceedings of the National Academy of Sciences.

[12]  Meredith E. Protas,et al.  Knockdown of Parhyale Ultrabithorax recapitulates evolutionary changes in crustacean appendage morphology , 2009, Proceedings of the National Academy of Sciences.

[13]  N. Patel,et al.  Probing the evolution of appendage specialization by Hox gene misexpression in an emerging model crustacean , 2009, Proceedings of the National Academy of Sciences.

[14]  N. Patel,et al.  Investigating divergent mechanisms of mesoderm development in arthropods: the expression of Ph-twist and Ph-mef2 in Parhyale hawaiensis. , 2008, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[15]  M. Telford,et al.  Evolution of Hox3 and ftz in arthropods: insights from the crustacean Daphnia pulex , 2007, Development Genes and Evolution.

[16]  B. Negre,et al.  HOM-C evolution in Drosophila: is there a need for Hox gene clustering? , 2007, Trends in genetics : TIG.

[17]  G. Scholtz,et al.  Cell lineage analysis of the mandibular segment of the amphipod Orchestia cavimana reveals that the crustacean paragnaths are sternal outgrowths and not limbs , 2006, Frontiers in Zoology.

[18]  S. Hayashi,et al.  Transcriptional readthrough of Hox genes Ubx and Antp and their divergent post‐transcriptional control during crustacean evolution , 2006, Evolution & development.

[19]  R. Janssen,et al.  The ten Hox genes of the millipede Glomeris marginata , 2006, Development Genes and Evolution.

[20]  T. Kaufman,et al.  Oncopeltus fasciatus zen is essential for serosal tissue function in katatrepsis. , 2006, Developmental biology.

[21]  T. Kaufman,et al.  Insect appendages and comparative ontogenetics. , 2005, Developmental biology.

[22]  N. Patel,et al.  Stages of embryonic development in the amphipod crustacean, Parhyale hawaiensis , 2005, Genesis.

[23]  T. Kaufman,et al.  Abd‐B expression in Porcellio scaber Latreille, 1804 (Isopoda: Crustacea): conserved pattern versus novel roles in development and evolution , 2005, Evolution & development.

[24]  T. Kaufman,et al.  Expression patterns of the rogue Hox genes Hox3/zen and fushi tarazu in the apterygote insect Thermobia domestica , 2004, Evolution & development.

[25]  K. Mita,et al.  Organization of the Hox gene cluster of the silkworm, Bombyx mori: a split of the Hox cluster in a non-Drosophila insect , 2004, Development Genes and Evolution.

[26]  A. Popadic,et al.  Differential expression patterns of the hox gene are associated with differential growth of insect hind legs. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[27]  S. Celniker,et al.  Posterior patterning genes and the identification of a unique body region in the brine shrimp Artemia franciscana , 2003, Development.

[28]  Maryline Blin,et al.  Possible implication of Hox genes Abdominal-B and abdominal-A in the specification of genital and abdominal segments in cirripedes , 2003, Development Genes and Evolution.

[29]  T. Kaufman,et al.  Hox genes and the evolution of the arthropod body plan 1 , 2002, Evolution & development.

[30]  W. Damen fushi tarazu: A Hox gene changes its role , 2002, BioEssays : news and reviews in molecular, cellular and developmental biology.

[31]  S. Hayashi,et al.  Evolving role of Antennapedia protein in arthropod limb patterning. , 2002, Development.

[32]  Maryline Blin,et al.  Expression of a homologue of the fushi tarazu (ftz) gene in a cirripede crustacean , 2002, Evolution & development.

[33]  T. Kaufman,et al.  Exploring the myriapod body plan: expression patterns of the ten Hox genes in a centipede. , 2002, Development.

[34]  William McGinnis,et al.  Hox protein mutation and macroevolution of the insect body plan , 2002, Nature.

[35]  A. Abzhanov,et al.  Embryonic expression patterns of the Hox genes of the crayfish Procambarus clarkii (Crustacea, Decapoda) , 2000, Evolution & development.

[36]  A. Abzhanov,et al.  Crustacean (malacostracan) Hox genes and the evolution of the arthropod trunk. , 2000, Development.

[37]  A. Abzhanov,et al.  Homeotic genes and the arthropod head: expression patterns of the labial, proboscipedia, and Deformed genes in crustaceans and insects. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[38]  A. Abzhanov,et al.  Novel regulation of the homeotic gene Scr associated with a crustacean leg-to-maxilliped appendage transformation. , 1999, Development.

[39]  T. Kaufman,et al.  The embryonic expression pattern of labial, posterior homeotic complex genes and the teashirt homologue in an apterygote insect , 1999, Development Genes and Evolution.

[40]  M. Telford,et al.  Of mites and zen: expression studies in a chelicerate arthropod confirm zen is a divergent Hox gene , 1998, Development Genes and Evolution.

[41]  N. Patel,et al.  Crustacean appendage evolution associated with changes in Hox gene expression , 1997, Nature.

[42]  Susan J. Brown,et al.  Class 3 Hox genes in insects and the origin of zen. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[43]  M. Akam,et al.  Hox genes and the diversification of insect and crustacean body plans , 1995, Nature.

[44]  N. Patel,et al.  Expression of engrailed during segmentation in grasshopper and crayfish. , 1989, Development.

[45]  M. Krasnow,et al.  An Ultrabithorax protein binds sequences near its own and the Antennapedia P1 promoters , 1988, Cell.

[46]  Yacine Graba,et al.  Hox Genes , 2014, Methods in Molecular Biology.

[47]  M. Blum,et al.  The isopod Asellus aquaticus : A novel arthropod model organism to study evolution of segment identity and patterning 1 , 2010 .

[48]  N. Patel,et al.  In situ hybridization of labeled RNA probes to fixed Parhyale hawaiensis embryos. , 2009, Cold Spring Harbor protocols.

[49]  N. Patel,et al.  Fixation and dissection of Parhyale hawaiensis embryos. , 2009, Cold Spring Harbor protocols.

[50]  N. Patel,et al.  The crustacean Parhyale hawaiensis: a new model for arthropod development. , 2009, Cold Spring Harbor protocols.

[51]  N. Patel,et al.  Antibody staining of Parhyale hawaiensis embryos. , 2009, Cold Spring Harbor protocols.

[52]  T. Kaufman,et al.  Evolution of the insect body plan as revealed by the Sex combs reduced expression pattern. , 1997, Development.

[53]  N. Patel,et al.  Sequence and expression of grasshopper antennapedia: comparison to Drosophila. , 1995, Developmental biology.

[54]  N. Patel,et al.  Imaging neuronal subsets and other cell types in whole-mount Drosophila embryos and larvae using antibody probes. , 1994, Methods in cell biology.

[55]  L. Wolpert Developmental Biology , 1968, Nature.