title: Molecular Evidence for Functional Divergence and Decay of a Transcription Factor Derived from Whole-Genome Duplication in Arabidopsis thaliana.
abstract: Functional divergence between duplicate transcription factors (TFs) has been linked to critical events in the evolution of land plants and can result from changes in patterns of expression, binding site divergence, and/or interactions with other proteins. Although plant TFs tend to be retained post polyploidization, many are lost within tens to hundreds of million years. Thus, it can be hypothesized that some TFs in plant genomes are in the process of becoming pseudogenes. Here, we use a pair of salt tolerance-conferring transcription factors, DWARF AND DELAYED FLOWERING1 (DDF1) and DDF2, that duplicated through paleopolyploidy 50 to 65 million years ago, as examples to illustrate potential mechanisms leading to duplicate retention and loss. We found that the expression patterns of Arabidopsis thaliana (At)DDF1 and AtDDF2 have diverged in a highly asymmetric manner, and AtDDF2 has lost most inferred ancestral stress responses. Consistent with promoter disablement, the AtDDF2 promoter has fewer predicted cis-elements and a methylated repetitive element. Through comparisons of AtDDF1, AtDDF2, and their Arabidopsis lyrata orthologs, we identified significant differences in binding affinities and binding site preference. In particular, an AtDDF2-specific substitution within the DNA-binding domain significantly reduces binding affinity. Cross-species analyses indicate that both AtDDF1 and AtDDF2 are under selective constraint, but among A. thaliana accessions, AtDDF2 has a higher level of nonsynonymous nucleotide diversity compared with AtDDF1. This may be the result of selection in different environments or may point toward the possibility of ongoing functional decay despite retention for millions of years after gene duplication.
authors.affiliation: Department of Plant Biology (M.D.L.-S., D.E.H., S.-H.S.), Genetics Program (S.U., N.P., S.-H.S.), Department of Energy Plant Research Laboratory (S.U.), Department of Biochemistry and Molecular Biology (G.D.M., L.F., M.F.), and Department of Chemistry (M.F.), Michigan State University, East Lansing, Michigan 48824; andLaPorte High School, LaPorte, Indiana 46350 (H.L.J.) lehtishi@msu.edu shius@msu.edu.
authors.forename: Melissa D
authors.identifier: http://orcid.org/0000-0003-1985-2687
authors.initials: MD
authors.lastname: Lehti-Shiu
authors.affiliation: Department of Plant Biology (M.D.L.-S., D.E.H., S.-H.S.), Genetics Program (S.U., N.P., S.-H.S.), Department of Energy Plant Research Laboratory (S.U.), Department of Biochemistry and Molecular Biology (G.D.M., L.F., M.F.), and Department of Chemistry (M.F.), Michigan State University, East Lansing, Michigan 48824; andLaPorte High School, LaPorte, Indiana 46350 (H.L.J.).
authors.forename: Sahra
authors.identifier: http://orcid.org/0000-0003-0863-0384
authors.initials: S
authors.lastname: Uygun
authors.affiliation: Department of Plant Biology (M.D.L.-S., D.E.H., S.-H.S.), Genetics Program (S.U., N.P., S.-H.S.), Department of Energy Plant Research Laboratory (S.U.), Department of Biochemistry and Molecular Biology (G.D.M., L.F., M.F.), and Department of Chemistry (M.F.), Michigan State University, East Lansing, Michigan 48824; andLaPorte High School, LaPorte, Indiana 46350 (H.L.J.).
authors.forename: Gaurav D
authors.identifier: http://orcid.org/0000-0002-8761-064X
authors.initials: GD
authors.lastname: Moghe
authors.affiliation: Department of Plant Biology (M.D.L.-S., D.E.H., S.-H.S.), Genetics Program (S.U., N.P., S.-H.S.), Department of Energy Plant Research Laboratory (S.U.), Department of Biochemistry and Molecular Biology (G.D.M., L.F., M.F.), and Department of Chemistry (M.F.), Michigan State University, East Lansing, Michigan 48824; andLaPorte High School, LaPorte, Indiana 46350 (H.L.J.).
authors.forename: Nicholas
authors.initials: N
authors.lastname: Panchy
authors.affiliation: Department of Plant Biology (M.D.L.-S., D.E.H., S.-H.S.), Genetics Program (S.U., N.P., S.-H.S.), Department of Energy Plant Research Laboratory (S.U.), Department of Biochemistry and Molecular Biology (G.D.M., L.F., M.F.), and Department of Chemistry (M.F.), Michigan State University, East Lansing, Michigan 48824; andLaPorte High School, LaPorte, Indiana 46350 (H.L.J.).
authors.forename: Liang
authors.initials: L
authors.lastname: Fang
authors.affiliation: Department of Plant Biology (M.D.L.-S., D.E.H., S.-H.S.), Genetics Program (S.U., N.P., S.-H.S.), Department of Energy Plant Research Laboratory (S.U.), Department of Biochemistry and Molecular Biology (G.D.M., L.F., M.F.), and Department of Chemistry (M.F.), Michigan State University, East Lansing, Michigan 48824; andLaPorte High School, LaPorte, Indiana 46350 (H.L.J.).
authors.forename: David E
authors.initials: DE
authors.lastname: Hufnagel
authors.affiliation: Department of Plant Biology (M.D.L.-S., D.E.H., S.-H.S.), Genetics Program (S.U., N.P., S.-H.S.), Department of Energy Plant Research Laboratory (S.U.), Department of Biochemistry and Molecular Biology (G.D.M., L.F., M.F.), and Department of Chemistry (M.F.), Michigan State University, East Lansing, Michigan 48824; andLaPorte High School, LaPorte, Indiana 46350 (H.L.J.).
authors.forename: Hannah L
authors.identifier: http://orcid.org/0000-0001-7062-0318
authors.initials: HL
authors.lastname: Jasicki
authors.affiliation: Department of Plant Biology (M.D.L.-S., D.E.H., S.-H.S.), Genetics Program (S.U., N.P., S.-H.S.), Department of Energy Plant Research Laboratory (S.U.), Department of Biochemistry and Molecular Biology (G.D.M., L.F., M.F.), and Department of Chemistry (M.F.), Michigan State University, East Lansing, Michigan 48824; andLaPorte High School, LaPorte, Indiana 46350 (H.L.J.).
authors.forename: Michael
authors.initials: M
authors.lastname: Feig
authors.affiliation: Department of Plant Biology (M.D.L.-S., D.E.H., S.-H.S.), Genetics Program (S.U., N.P., S.-H.S.), Department of Energy Plant Research Laboratory (S.U.), Department of Biochemistry and Molecular Biology (G.D.M., L.F., M.F.), and Department of Chemistry (M.F.), Michigan State University, East Lansing, Michigan 48824; andLaPorte High School, LaPorte, Indiana 46350 (H.L.J.) lehtishi@msu.edu shius@msu.edu.
authors.forename: Shin-Han
authors.identifier: http://orcid.org/0000-0001-6470-235X
authors.initials: SH
authors.lastname: Shiu
mesh_terms: D000595:Amino Acid Sequence; D017360:Arabidopsis / Q000235:genetics*; D029681:Arabidopsis Proteins / Q000737:chemistry / Q000235:genetics* / Q000378:metabolism; D001665:Binding Sites / Q000235:genetics; D003080:Cold Temperature; D019143:Evolution, Molecular; D020440:Gene Duplication; D018506:Gene Expression Regulation, Plant / Q000187:drug effects; D014644:Genetic Variation; D018745:Genome, Plant / Q000235:genetics; D008958:Models, Molecular; D008969:Molecular Sequence Data; D010802:Phylogeny; D018517:Plant Roots / Q000235:genetics; D018520:Plant Shoots / Q000235:genetics; D011485:Protein Binding; D017434:Protein Structure, Tertiary; D017386:Sequence Homology, Amino Acid; D012965:Sodium Chloride / Q000494:pharmacology; D014157:Transcription Factors / Q000145:classification / Q000235:genetics* / Q000378:metabolism
chemical_list: D029681:Arabidopsis Proteins; C487098:DDF1 protein, Arabidopsis; C487099:DDF2 protein, Arabidopsis; D014157:Transcription Factors; D012965:Sodium Chloride