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Mol Biol Evol. 2016 Jun;33(6):1486-501. doi: 10.1093/molbev/msw031. Epub 2016 Feb 22.

Evolutionary Dynamics of Floral Homeotic Transcription Factor Protein-Protein Interactions.

Author information

1
Department of Biology, University of Massachusetts Amherst Department of Biology, Brigham Young University mbartlett@bio.umass.edu whipple@byu.edu.
2
Department of Biology, East Carolina University.
3
Department of Biology, Brigham Young University.
4
Department of Biology, University of Massachusetts Amherst.
5
Department of Biology, Brigham Young University mbartlett@bio.umass.edu whipple@byu.edu.

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.

KEYWORDS:

APETALA3; B-class MADS box genes; PISTILLATA; Poales; convergent molecular evolution; evolution of flower development.

PMID:
26908583
PMCID:
PMC4868119
DOI:
10.1093/molbev/msw031
[Indexed for MEDLINE]
Free PMC Article

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