Connectivity of vertebrate genomes: Paired-related homeobox (Prrx) genes in spotted gar, basal teleosts, and tetrapods

• DOI: 10.1016/j.cbpc.2014.01.005
• Publication Date: 2014-02-01T01:30:41Z
• Authors: Ingo Braasch; Yann Guiguen; Ryan Loker; John H. Letaw; Allyse Ferrara; Julien Bobe; John H. Postlethwait
• Keywords: 570; craniofacial; Prrx1;Prrx2;RNA-Seq;aquatic medical model;craniofacial;fin/limb bud;genome duplication;ohnolog;paired appendages;vertebrate; Evolution, Molecular; 03 medical and health sciences; poisson; vertebrate; genome duplication; Biologie de la reproduction; Animals; Humans; fin/limb bud; RNA-Seq; 14. Life underwater; duplication des génomes; ohnolog; Homeodomain Proteins; Reproductive Biology; 0303 health sciences; Genome; Fishes; Genes, Homeobox; [SDV.BDLR]Life Sciences [q-bio]/Reproductive Biology; Prrx2; santé humaine; Prrx1; tétrapode; gène prrx; vertébré; lepisosteus oculatus; 3. Good health; lépisosté tacheté; séquence d'arn; paired appendages; teleosteen; facteur de transcription; aquatic medical model; expression des gènes

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.