title: Evolutionary Dynamics of Floral Homeotic Transcription Factor Protein-Protein Interactions.
abstract: Protein-protein interactions (PPIs) have widely acknowledged roles in the regulation of development, but few studies have addressed the timing and mechanism of shifting PPIs over evolutionary history. The B-class MADS-box transcription factors, PISTILLATA (PI) and APETALA3 (AP3) are key regulators of floral development. PI-like (PI(L)) and AP3-like (AP3(L)) proteins from a number of plants, including Arabidopsis thaliana (Arabidopsis) and the grass Zea mays (maize), bind DNA as obligate heterodimers. However, a PI(L) protein from the grass relative Joinvillea can bind DNA as a homodimer. To ascertain whether Joinvillea PI(L) homodimerization is an anomaly or indicative of broader trends, we characterized PI(L) dimerization across the Poales and uncovered unexpected evolutionary lability. Both obligate B-class heterodimerization and PI(L) homodimerization have evolved multiple times in the order, by distinct molecular mechanisms. For example, obligate B-class heterodimerization in maize evolved very recently from PI(L) homodimerization. A single amino acid change, fixed during domestication, is sufficient to toggle one maize PI(L) protein between homodimerization and obligate heterodimerization. We detected a signature of positive selection acting on residues preferentially clustered in predicted sites of contact between MADS-box monomers and dimers, and in motifs that mediate MADS PPI specificity in Arabidopsis. Changing one positively selected residue can alter PI(L) dimerization activity. Furthermore, ectopic expression of a Joinvillea PI(L) homodimer in Arabidopsis can homeotically transform sepals into petals. Our results provide a window into the evolutionary remodeling of PPIs, and show that novel interactions have the potential to alter plant form in a context-dependent manner.
authors.affiliation: Department of Biology, University of Massachusetts Amherst Department of Biology, Brigham Young University mbartlett@bio.umass.edu whipple@byu.edu.
authors.forename: Madelaine
authors.initials: M
authors.lastname: Bartlett
authors.affiliation: Department of Biology, East Carolina University.
authors.forename: Beth
authors.initials: B
authors.lastname: Thompson
authors.affiliation: Department of Biology, Brigham Young University.
authors.forename: Holly
authors.initials: H
authors.lastname: Brabazon
authors.affiliation: Department of Biology, University of Massachusetts Amherst.
authors.forename: Robert
authors.initials: R
authors.lastname: Del Gizzi
authors.affiliation: Department of Biology, University of Massachusetts Amherst.
authors.forename: Thompson
authors.initials: T
authors.lastname: Zhang
authors.affiliation: Department of Biology, Brigham Young University mbartlett@bio.umass.edu whipple@byu.edu.
authors.forename: Clinton
authors.initials: C
authors.lastname: Whipple
mesh_terms: D000595:Amino Acid Sequence; D019143:Evolution, Molecular; D035264:Flowers / Q000235:genetics / Q000254:growth & development; D018506:Gene Expression Regulation, Plant; D005801:Genes, Homeobox; D017343:Genes, Plant; D026161:MADS Domain Proteins / Q000235:genetics* / Q000378:metabolism; D010802:Phylogeny; D006109:Poaceae / Q000235:genetics* / Q000254:growth & development / Q000378:metabolism; D054730:Protein Interaction Domains and Motifs; D017386:Sequence Homology, Amino Acid; D014157:Transcription Factors / Q000235:genetics* / Q000378:metabolism
chemical_list: D026161:MADS Domain Proteins; D014157:Transcription Factors
keywords: APETALA3; B-class MADS box genes; PISTILLATA; Poales; convergent molecular evolution; evolution of flower development.