Evolutionary Dynamics of Floral Homeotic Transcription Factor Protein–Protein Interactions
Bartlett, Madelaine; Thompson, Beth; Brabazon, Holly; Del Gizzi, Robert; Zhang, Thompson; Whipple, Clinton
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 (PIL) and AP3-like (AP3L) proteins from a number of plants, including Arabidopsis thaliana (Arabidopsis) and the grass Zea mays (maize), bind DNA as obligate heterodimers. However, a PIL protein from the grass relative Joinvillea can bind DNA as a homodimer. To ascertain whether Joinvillea PIL homodimerization is an anomaly or indicative of broader trends, we characterized PIL dimerization across the Poales and uncovered unexpected evolutionary lability. Both obligate B-class heterodimerization and PIL homodimerization have evolved multiple times in the order, by distinct molecular mechanisms. For example, obligate B-class heterodimerization in maize evolved very recently from PIL homodimerization. A single amino acid change, fixed during domestication, is sufficient to toggle one maize PIL 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 PIL dimerization activity. Furthermore, ectopic expression of a Joinvillea PIL 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. Key words: PISTILLATA, Poales, APETALA3, convergent molecular evolution, B-class MADS box genes, evolution of flower development.
Bartlett, Madelaine, & Thompson, Beth, & Brabazon, Holly, & Del Gizzi, Robert, & Zhang, Thompson, & Whipple, Clinton. (February 2016). Evolutionary Dynamics of Floral Homeotic Transcription Factor Protein–Protein Interactions. Molecular Biology and Evolution, (33:6), p.1486-1501. Retrieved from http://hdl.handle.net/10342/8528
Bartlett, Madelaine, and Thompson, Beth, and Brabazon, Holly, and Del Gizzi, Robert, and Zhang, Thompson, and Whipple, Clinton. "Evolutionary Dynamics of Floral Homeotic Transcription Factor Protein–Protein Interactions". Molecular Biology and Evolution. 33:6. (1486-1501.), February 2016. June 21, 2021. http://hdl.handle.net/10342/8528.
Bartlett, Madelaine and Thompson, Beth and Brabazon, Holly and Del Gizzi, Robert and Zhang, Thompson and Whipple, Clinton, "Evolutionary Dynamics of Floral Homeotic Transcription Factor Protein–Protein Interactions," Molecular Biology and Evolution 33, no. 6 (February 2016), http://hdl.handle.net/10342/8528 (accessed June 21, 2021).
Bartlett, Madelaine, Thompson, Beth, Brabazon, Holly, Del Gizzi, Robert, Zhang, Thompson, Whipple, Clinton. Evolutionary Dynamics of Floral Homeotic Transcription Factor Protein–Protein Interactions. Molecular Biology and Evolution. February 2016; 33(6) 1486-1501. http://hdl.handle.net/10342/8528. Accessed June 21, 2021.