Connectivity of vertebrate genomes: Paired-related homeobox (Prrx) genes in spotted gar, basal teleosts, and tetrapods.
Teleost fish are important models for human biology, health, and disease. Because genome duplication in a teleost ancestor (TGD) impacts the evolution of teleost genome structure and gene repertoires, we must discriminate gene functions that are shared and ancestral from those that are lineage-specific in teleosts or tetrapods to accurately apply inferences from teleost disease models to human health. Generalizations must account both for the TGD and for divergent evolution between teleosts and tetrapods after the likely two rounds of genome duplication shared by all vertebrates. Progress in sequencing techniques provides new opportunities to generate genomic and transcriptomic information from a broad range of phylogenetically informative taxa that facilitate detailed understanding of gene family and gene function evolution. We illustrate here the use of new sequence resources from spotted gar (Lepisosteus oculatus), a rayfin fish that diverged from teleosts before the TGD, as well as RNA-Seq data from gar and multiple teleost lineages to reconstruct the evolution of the Paired-related homeobox (Prrx) transcription factor gene family, which is involved in the development of mesoderm and neural crest-derived mesenchyme. We show that for Prrx genes, the spotted gar genome and gene expression patterns mimic mammals better than teleosts do. Analyses force the seemingly paradoxical conclusion that regulatory mechanisms for the limb expression domains of Prrx genes existed before the evolution of paired appendages. Detailed evolutionary analyses like those reported here are required to identify fish species most similar to the human genome to optimally connect fish models to human gene functions in health and disease.
Institute of Neuroscience, University of Oregon, Eugene, 97403-1254 OR, USA. Electronic address: ibraasch@uoneuro.uoregon.edu.
Ingo
I
Braasch
INRA, UR1037 LPGP, Campus de Beaulieu, F-35000 Rennes, France. Electronic address: yann.guiguen@rennes.inra.fr.
Yann
Y
Guiguen
Institute of Neuroscience, University of Oregon, Eugene, 97403-1254 OR, USA. Electronic address: loker@uoregon.edu.
Ryan
R
Loker
Institute of Neuroscience, University of Oregon, Eugene, 97403-1254 OR, USA. Electronic address: letaw@ohsu.edu.
John H
JH
Letaw
Department of Biological Sciences, Nicholls State University, Thibodaux, LA 70310, USA. Electronic address: allyse.ferrara@nicholls.edu.
Allyse
A
Ferrara
INRA, UR1037 LPGP, Campus de Beaulieu, F-35000 Rennes, France. Electronic address: Julien.Bobe@rennes.inra.fr.
Julien
J
Bobe
Institute of Neuroscience, University of Oregon, Eugene, 97403-1254 OR, USA. Electronic address: jpostle@uoneuro.uoregon.edu.
John H
JH
Postlethwait
D000818:Animals; D019143:Evolution, Molecular; D005399:Fishes / Q000235:genetics*; D005801:Genes, Homeobox; D016678:Genome; D018398:Homeodomain Proteins / Q000235:genetics; D006801:Humans
D018398:Homeodomain Proteins; C082157:PRRX1 protein, human; C512693:PRRX2 protein, human
Craniofacial; Fin/limb bud; Genome duplication; Ohnolog; Paired appendages; Prrx1; Prrx2; RNA-Seq