Literature DB >> 20222951

A non-tree-based comprehensive study of metazoan Hox and ParaHox genes prompts new insights into their origin and evolution.

Morgane Thomas-Chollier1, Valérie Ledent, Luc Leyns, Michel Vervoort.   

Abstract

BACKGROUND: Hox and the closely-related ParaHox genes, which emerged prior to the divergence between cnidarians and bilaterians, are the most well-known members of the ancient genetic toolkit that controls embryonic development across all metazoans. Fundamental questions relative to their origin and evolutionary relationships remain however unresolved. We investigate here the evolution of metazoan Hox and ParaHox genes using the HoxPred program that allows the identification of Hox genes without the need of phylogenetic tree reconstructions.
RESULTS: We show that HoxPred provides an efficient and accurate classification of Hox and ParaHox genes in their respective homology groups, including Hox paralogous groups (PGs). We analyzed more than 10,000 sequences from 310 metazoan species, from 6 genome projects and the complete UniProtKB database. The HoxPred program and all results arranged in the Datab'Hox database are freely available at http://cege.vub.ac.be/hoxpred/. Results for the genome-scale studies are coherent with previous studies, and also brings knowledge on the Hox repertoire and clusters for newly-sequenced species. The unprecedented scale of this study and the use of a non-tree-based approach allows unresolved key questions about Hox and ParaHox genes evolution to be addressed.
CONCLUSIONS: Our analysis suggests that the presence of a single type of Posterior Hox genes (PG9-like) is ancestral to bilaterians, and that new Posterior PGs would have arisen in deuterostomes through independent gene duplications. Four types of Central genes would also be ancestral to bilaterians, with two of them, PG6- and PG7-like that gave rise, in protostomes, to the UbdA- and ftz/Antp/Lox5-type genes, respectively. A fifth type of Central genes (PG8) would have emerged in the vertebrate lineage. Our results also suggest the presence of Anterior (PG1 and PG3), Central and Posterior Hox genes in the cnidarians, supporting an ancestral four-gene Hox cluster. In addition, our data support the relationship of the bilaterian ParaHox genes Gsx and Xlox with PG3, and Cdx with the Central genes. Our study therefore indicates three possible models for the origin of Hox and ParaHox in early metazoans, a two-gene (Anterior/PG3--Central/Posterior), a three-gene (Anterior/PG1, Anterior/PG3 and Central/Posterior), or a four-gene (Anterior/PG1--Anterior/PG3--Central--Posterior) ProtoHox cluster.

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Year:  2010        PMID: 20222951      PMCID: PMC2842273          DOI: 10.1186/1471-2148-10-73

Source DB:  PubMed          Journal:  BMC Evol Biol        ISSN: 1471-2148            Impact factor:   3.260


  64 in total

Review 1.  Ancient origin of the Hox gene cluster.

Authors:  D E Ferrier; P W Holland
Journal:  Nat Rev Genet       Date:  2001-01       Impact factor: 53.242

2.  Combined-method phylogenetic analysis of Hox and ParaHox genes of the metazoa.

Authors:  M J Kourakis; M Q Martindale
Journal:  J Exp Zool       Date:  2000-08-15

3.  More constraint on ParaHox than Hox gene families in early metazoan evolution.

Authors:  Manon Quiquand; Nathalie Yanze; Jürgen Schmich; Volker Schmid; Brigitte Galliot; Stefano Piraino
Journal:  Dev Biol       Date:  2009-01-27       Impact factor: 3.582

4.  Phylogenomics revives traditional views on deep animal relationships.

Authors:  Hervé Philippe; Romain Derelle; Philippe Lopez; Kerstin Pick; Carole Borchiellini; Nicole Boury-Esnault; Jean Vacelet; Emmanuelle Renard; Evelyn Houliston; Eric Quéinnec; Corinne Da Silva; Patrick Wincker; Hervé Le Guyader; Sally Leys; Daniel J Jackson; Fabian Schreiber; Dirk Erpenbeck; Burkhard Morgenstern; Gert Wörheide; Michaël Manuel
Journal:  Curr Biol       Date:  2009-04-02       Impact factor: 10.834

Review 5.  The evolution and maintenance of Hox gene clusters in vertebrates and the teleost-specific genome duplication.

Authors:  Shigehiro Kuraku; Axel Meyer
Journal:  Int J Dev Biol       Date:  2009       Impact factor: 2.203

Review 6.  Hox genes and chordate evolution.

Authors:  P W Holland; J Garcia-Fernàndez
Journal:  Dev Biol       Date:  1996-02-01       Impact factor: 3.582

7.  The amphioxus Hox cluster: deuterostome posterior flexibility and Hox14.

Authors:  D E Ferrier; C Minguillón; P W Holland; J Garcia-Fernàndez
Journal:  Evol Dev       Date:  2000 Sep-Oct       Impact factor: 1.930

8.  Turning Hox "signatures" into synapomorphies.

Authors:  M J Telford
Journal:  Evol Dev       Date:  2000 Nov-Dec       Impact factor: 1.930

9.  Uncoupling time and space in the collinear regulation of Hox genes.

Authors:  Patrick Tschopp; Basile Tarchini; François Spitz; Jozsef Zakany; Denis Duboule
Journal:  PLoS Genet       Date:  2009-03-06       Impact factor: 5.917

10.  Features of the ancestral bilaterian inferred from Platynereis dumerilii ParaHox genes.

Authors:  Jerome H L Hui; Florian Raible; Natalia Korchagina; Nicolas Dray; Sylvie Samain; Ghislaine Magdelenat; Claire Jubin; Béatrice Segurens; Guillaume Balavoine; Detlev Arendt; David E K Ferrier
Journal:  BMC Biol       Date:  2009-07-23       Impact factor: 7.431

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  11 in total

Review 1.  Evolutionary crossroads in developmental biology: Cnidaria.

Authors:  Ulrich Technau; Robert E Steele
Journal:  Development       Date:  2011-03-09       Impact factor: 6.868

2.  Molecular phylogeny of four homeobox genes from the purple sea star Pisaster ochraceus.

Authors:  Giorgio Matassi; Janice Hitomi Imai; Anna Di Gregorio
Journal:  Dev Genes Evol       Date:  2015-10-02       Impact factor: 0.900

3.  Identical genomic organization of two hemichordate hox clusters.

Authors:  Robert Freeman; Tetsuro Ikuta; Michael Wu; Ryo Koyanagi; Takeshi Kawashima; Kunifumi Tagawa; Tom Humphreys; Guang-Chen Fang; Asao Fujiyama; Hidetoshi Saiga; Christopher Lowe; Kim Worley; Jerry Jenkins; Jeremy Schmutz; Marc Kirschner; Daniel Rokhsar; Nori Satoh; John Gerhart
Journal:  Curr Biol       Date:  2012-10-11       Impact factor: 10.834

4.  The genetic factors of bilaterian evolution.

Authors:  Peter Heger; Wen Zheng; Anna Rottmann; Kristen A Panfilio; Thomas Wiehe
Journal:  Elife       Date:  2020-07-16       Impact factor: 8.140

5.  Evolution of coding and non-coding genes in HOX clusters of a marsupial.

Authors:  Hongshi Yu; James Lindsay; Zhi-Ping Feng; Stephen Frankenberg; Yanqiu Hu; Dawn Carone; Geoff Shaw; Andrew J Pask; Rachel O'Neill; Anthony T Papenfuss; Marilyn B Renfree
Journal:  BMC Genomics       Date:  2012-06-18       Impact factor: 3.969

6.  Hox proteins display a common and ancestral ability to diversify their interaction mode with the PBC class cofactors.

Authors:  Bruno Hudry; Sophie Remacle; Marie-Claire Delfini; René Rezsohazy; Yacine Graba; Samir Merabet
Journal:  PLoS Biol       Date:  2012-06-26       Impact factor: 8.029

7.  Hox gene cluster of the ascidian, Halocynthia roretzi, reveals multiple ancient steps of cluster disintegration during ascidian evolution.

Authors:  Yuka Sekigami; Takuya Kobayashi; Ai Omi; Koki Nishitsuji; Tetsuro Ikuta; Asao Fujiyama; Noriyuki Satoh; Hidetoshi Saiga
Journal:  Zoological Lett       Date:  2017-09-15       Impact factor: 2.836

Review 8.  Evolution of Hox gene clusters in deuterostomes.

Authors:  Juan Pascual-Anaya; Salvatore D'Aniello; Shigeru Kuratani; Jordi Garcia-Fernàndez
Journal:  BMC Dev Biol       Date:  2013-07-02       Impact factor: 1.978

9.  Solving Classification Problems for Large Sets of Protein Sequences with the Example of Hox and ParaHox Proteins.

Authors:  Stefanie D Hueber; Tancred Frickey
Journal:  J Dev Biol       Date:  2016-02-04

10.  Molecular insights into the origin of the Hox-TALE patterning system.

Authors:  Bruno Hudry; Morgane Thomas-Chollier; Yael Volovik; Marilyne Duffraisse; Amélie Dard; Dale Frank; Ulrich Technau; Samir Merabet
Journal:  Elife       Date:  2014-03-18       Impact factor: 8.140

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