title: Evolution of an ancient protein function involved in organized multicellularity in animals.
abstract: To form and maintain organized tissues, multicellular organisms orient their mitotic spindles relative to neighboring cells. A molecular complex scaffolded by the GK protein-interaction domain (GKPID) mediates spindle orientation in diverse animal taxa by linking microtubule motor proteins to a marker protein on the cell cortex localized by external cues. Here we illuminate how this complex evolved and commandeered control of spindle orientation from a more ancient mechanism. The complex was assembled through a series of molecular exploitation events, one of which - the evolution of GKPID's capacity to bind the cortical marker protein - can be recapitulated by reintroducing a single historical substitution into the reconstructed ancestral GKPID. This change revealed and repurposed an ancient molecular surface that previously had a radically different function. We show how the physical simplicity of this binding interface enabled the evolution of a new protein function now essential to the biological complexity of many animals.
authors.affiliation: Institute of Ecology and Evolution, University of Oregon, Eugene, United States.|Department of Chemistry and Biochemistry, University of Oregon, Eugene, United States.|Institute of Molecular Biology, University of Oregon, Eugene, United States.
authors.forename: Douglas P
authors.initials: DP
authors.lastname: Anderson
authors.affiliation: Department of Biochemistry, Medical College of Wisconsin, Milwaukee, United States.
authors.forename: Dustin S
authors.initials: DS
authors.lastname: Whitney
authors.affiliation: Institute of Ecology and Evolution, University of Oregon, Eugene, United States.
authors.forename: Victor
authors.initials: V
authors.lastname: Hanson-Smith
authors.affiliation: Department of Molecular and Cellular Biology, Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, United States.
authors.forename: Arielle
authors.initials: A
authors.lastname: Woznica
authors.affiliation: Department of Chemistry and Biochemistry, University of Oregon, Eugene, United States.|Institute of Molecular Biology, University of Oregon, Eugene, United States.
authors.forename: William
authors.initials: W
authors.lastname: Campodonico-Burnett
authors.affiliation: Department of Biochemistry, Medical College of Wisconsin, Milwaukee, United States.
authors.forename: Brian F
authors.initials: BF
authors.lastname: Volkman
authors.affiliation: Department of Molecular and Cellular Biology, Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, United States.
authors.forename: Nicole
authors.initials: N
authors.lastname: King
authors.forename: Joseph W
authors.initials: JW
authors.lastname: Thornton
authors.affiliation: Department of Chemistry and Biochemistry, University of Oregon, Eugene, United States.|Institute of Molecular Biology, University of Oregon, Eugene, United States.
authors.forename: Kenneth E
authors.initials: KE
authors.lastname: Prehoda
mesh_terms: D000818:Animals; D002453:Cell Cycle; D018797:Cell Cycle Proteins / Q000737:chemistry / Q000235:genetics* / Q000378:metabolism*; D019143:Evolution, Molecular; D051528:Guanylate Kinases / Q000737:chemistry / Q000235:genetics* / Q000378:metabolism*; D008958:Models, Molecular; D011485:Protein Binding; D055503:Protein Multimerization; D008941:Spindle Apparatus / Q000378:metabolism*
chemical_list: D018797:Cell Cycle Proteins; D051528:Guanylate Kinases
keywords: Salpingea rosetta; ancestral protein reconstruction; cell biology; evolutionary biochemistry; evolutionary biology; evolutionary cell biology; genomics; mitotic spindle; protein evolution