Conservation and divergence in the AGAMOUS subfamily of MADS-box genes: evidence of independent sub- and neofunctionalization events

Authors

  • Laura M. Zahn,

    1. Department of Biology, The Huck Institutes of the Life Sciences, and the Institute for Molecular Genetics and Evolution, The Pennsylvania State University, University Park, PA 16802, USA
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  • James H. Leebens-Mack,

    1. Department of Biology, The Huck Institutes of the Life Sciences, and the Institute for Molecular Genetics and Evolution, The Pennsylvania State University, University Park, PA 16802, USA
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  • Jennifer M. Arrington,

    1. Department of Biology, The Huck Institutes of the Life Sciences, and the Institute for Molecular Genetics and Evolution, The Pennsylvania State University, University Park, PA 16802, USA
    2. Department of Biology, Duke University, Durham, NC 27708, USA
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  • Yi Hu,

    1. Department of Biology, The Huck Institutes of the Life Sciences, and the Institute for Molecular Genetics and Evolution, The Pennsylvania State University, University Park, PA 16802, USA
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  • Lena L. Landherr,

    1. Department of Biology, The Huck Institutes of the Life Sciences, and the Institute for Molecular Genetics and Evolution, The Pennsylvania State University, University Park, PA 16802, USA
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  • Claude W. DePamphilis,

    1. Department of Biology, The Huck Institutes of the Life Sciences, and the Institute for Molecular Genetics and Evolution, The Pennsylvania State University, University Park, PA 16802, USA
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  • Annette Becker,

    1. Lehrstuhl für Genetik, Friedrich-Schiller-Universität Jena, Philosophenweg 12, D-07743, Jena, Germany
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    • 1Present address: Evolutionary Developmental Genetics Group, University of Bremen, Leobener Str., UFT 28359 Bremen, Germany

  • Günter Theissen,

    1. Lehrstuhl für Genetik, Friedrich-Schiller-Universität Jena, Philosophenweg 12, D-07743, Jena, Germany
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  • Hong Ma

    Corresponding author
    1. Department of Biology, The Huck Institutes of the Life Sciences, and the Institute for Molecular Genetics and Evolution, The Pennsylvania State University, University Park, PA 16802, USA
      *Author for correspondence (email: hxm16@psu.edu)
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*Author for correspondence (email: hxm16@psu.edu)

SUMMARY

The MADS-box gene AGAMOUS (AG) plays a key role in determining floral meristem and organ identities. We identified three AG homologs, EScaAG1, EScaAG2, and EScaAGL11 from the basal eudicot Eschscholzia californica (California poppy). Phylogenetic analyses indicate that EScaAG1 and EScaAG2 are recent paralogs within the AG clade, independent of the duplication in ancestral core eudicots that gave rise to the euAG and PLENA (PLE) orthologs. EScaAGL11 is basal to core eudicot AGL11 orthologs in a clade representing an older duplication event after the divergence of the angiosperm and gymnosperm lineages. Detailed in situ hybridization experiments show that expression of EScaAG1 and EScaAG2 is similar to AG; however, both genes appear to be expressed earlier in floral development than described in the core eudicots. A thorough examination of available expression and functional data in a phylogenetic context for members of the AG and AGL11 clades reveals that gene expression has been quite variable throughout the evolutionary history of the AG subfamily and that ovule-specific expression might have evolved more than twice. Although sub- and neofunctionalization are inferred to have occurred following gene duplication, functional divergence among orthologs is evident, as is convergence, among paralogs sampled from different species. We propose that retention of multiple AG homologs in several paralogous lineages can be explained by the conservation of ancestral protein activity combined with evolutionarily labile regulation of expression in the AG and AGL11 clades such that the collective functions of the AG subfamily in stamen and carpel development are maintained following gene duplication.

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