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Evolutionary Dynamics of Floral Homeotic Transcription Factor Protein–Protein Interactions
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 o...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Oxford University Press
2016
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4868119/ https://www.ncbi.nlm.nih.gov/pubmed/26908583 http://dx.doi.org/10.1093/molbev/msw031 |
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author | Bartlett, Madelaine Thompson, Beth Brabazon, Holly Del Gizzi, Robert Zhang, Thompson Whipple, Clinton |
author_facet | Bartlett, Madelaine Thompson, Beth Brabazon, Holly Del Gizzi, Robert Zhang, Thompson Whipple, Clinton |
author_sort | Bartlett, Madelaine |
collection | PubMed |
description | 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. |
format | Online Article Text |
id | pubmed-4868119 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2016 |
publisher | Oxford University Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-48681192016-05-17 Evolutionary Dynamics of Floral Homeotic Transcription Factor Protein–Protein Interactions Bartlett, Madelaine Thompson, Beth Brabazon, Holly Del Gizzi, Robert Zhang, Thompson Whipple, Clinton Mol Biol Evol Discoveries 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. Oxford University Press 2016-06 2016-02-22 /pmc/articles/PMC4868119/ /pubmed/26908583 http://dx.doi.org/10.1093/molbev/msw031 Text en © The Author 2016. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com |
spellingShingle | Discoveries Bartlett, Madelaine Thompson, Beth Brabazon, Holly Del Gizzi, Robert Zhang, Thompson Whipple, Clinton Evolutionary Dynamics of Floral Homeotic Transcription Factor Protein–Protein Interactions |
title | Evolutionary Dynamics of Floral Homeotic Transcription Factor Protein–Protein Interactions |
title_full | Evolutionary Dynamics of Floral Homeotic Transcription Factor Protein–Protein Interactions |
title_fullStr | Evolutionary Dynamics of Floral Homeotic Transcription Factor Protein–Protein Interactions |
title_full_unstemmed | Evolutionary Dynamics of Floral Homeotic Transcription Factor Protein–Protein Interactions |
title_short | Evolutionary Dynamics of Floral Homeotic Transcription Factor Protein–Protein Interactions |
title_sort | evolutionary dynamics of floral homeotic transcription factor protein–protein interactions |
topic | Discoveries |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4868119/ https://www.ncbi.nlm.nih.gov/pubmed/26908583 http://dx.doi.org/10.1093/molbev/msw031 |
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