title: New gene evolution in the bonus-TIF1-γ/TRIM33 family impacted the architecture of the vertebrate dorsal-ventral patterning network.
abstract: Uncovering how a new gene acquires its function and understanding how the function of a new gene influences existing genetic networks are important topics in evolutionary biology. Here, we demonstrate nonconservation for the embryonic functions of Drosophila Bonus and its newest vertebrate relative TIF1-γ/TRIM33. We showed previously that TIF1-γ/TRIM33 functions as an ubiquitin ligase for the Smad4 signal transducer and antagonizes the Bone Morphogenetic Protein (BMP) signaling network underlying vertebrate dorsal-ventral axis formation. Here, we show that Bonus functions as an agonist of the Decapentaplegic (Dpp) signaling network underlying dorsal-ventral axis formation in flies. The absence of conservation for the roles of Bonus and TIF1-γ/TRIM33 reveals a shift in the dorsal-ventral patterning networks of flies and mice, systems that were previously considered wholly conserved. The shift occurred when the new gene TIF1-γ/TRIM33 replaced the function of the ubiquitin ligase Nedd4L in the lineage leading to vertebrates. Evidence of this replacement is our demonstration that Nedd4 performs the function of TIF1-γ/TRIM33 in flies during dorsal-ventral axis formation. The replacement allowed vertebrate Nedd4L to acquire novel functions as a ubiquitin ligase of vertebrate-specific Smad proteins. Overall our data reveal that the architecture of the Dpp/BMP dorsal-ventral patterning network continued to evolve in the vertebrate lineage, after separation from flies, via the incorporation of new genes.
authors.affiliation: Department of Biological Sciences, California State University, East Bay.
authors.forename: Robert G
authors.initials: RG
authors.lastname: Wisotzkey
authors.affiliation: Department of Biological Sciences, California State University, East BaySchool of Life Sciences, Arizona State University.
authors.forename: Janine C
authors.initials: JC
authors.lastname: Quijano
authors.affiliation: School of Life Sciences, Arizona State University.
authors.forename: Michael J
authors.initials: MJ
authors.lastname: Stinchfield
authors.affiliation: School of Life Sciences, Arizona State University newfeld@asu.edu.
authors.forename: Stuart J
authors.initials: SJ
authors.lastname: Newfeld
mesh_terms: D000818:Animals; D001499:Bayes Theorem; D019521:Body Patterning; D029721:Drosophila Proteins / Q000819:agonists / Q000235:genetics / Q000378:metabolism; D004331:Drosophila melanogaster / Q000196:embryology* / Q000235:genetics* / Q000378:metabolism; D056827:Endosomal Sorting Complexes Required for Transport / Q000235:genetics / Q000378:metabolism; D019143:Evolution, Molecular; D006801:Humans; D051379:Mice; D000075702:Nedd4 Ubiquitin Protein Ligases; D010802:Phylogeny; D015398:Signal Transduction; D014157:Transcription Factors / Q000235:genetics* / Q000378:metabolism; D044767:Ubiquitin-Protein Ligases / Q000235:genetics / Q000378:metabolism; D014714:Vertebrates / Q000196:embryology* / Q000235:genetics*
chemical_list: C502013:Bon protein, Drosophila; D029721:Drosophila Proteins; D056827:Endosomal Sorting Complexes Required for Transport; D014157:Transcription Factors; C064196:dpp protein, Drosophila; D000075702:Nedd4 Ubiquitin Protein Ligases; C000618483:Nedd4 protein, human; C000618485:Nedd4L protein, human; C000618461:Nedd4l protein, mouse; D044767:Ubiquitin-Protein Ligases
keywords: Bonus/TIF1/TRIM; Dorsal/NF-κB; Dpp/BMP/TGF-β; Drosophila; dorsal–ventral axis; embryonic development