The evolution of plant genomes is characterized by several rounds of polyploidization or ancient whole genome duplication. While the consequences of these major events for genome structure and transcriptome expression have been investigated, the effects at the protein level remain unknown and yet will be functionally important. To understand how a plant protein-protein interaction network organizes itself after whole genome duplication, we studied the evolution of MADS-domain transcription factors. We accurately inferred, resurrected and tested the interactions of their ancestral proteins before and after the gamma triplication at the origin of core eudicots and directly compare these ancestral networks to the ... More
The evolution of plant genomes is characterized by several rounds of polyploidization or ancient whole genome duplication. While the consequences of these major events for genome structure and transcriptome expression have been investigated, the effects at the protein level remain unknown and yet will be functionally important. To understand how a plant protein-protein interaction network organizes itself after whole genome duplication, we studied the evolution of MADS-domain transcription factors. We accurately inferred, resurrected and tested the interactions of their ancestral proteins before and after the gamma triplication at the origin of core eudicots and directly compare these ancestral networks to the networks of Arabidopsis and tomato. We find that the gamma triplication generated a network constrained in size and saturated in possible number of interactions, which strongly rewired by the addition of many new interactions. The new interactions are surprisingly often established with related proteins, something we call neo-redundancy. The evolved networks are organized around hubs and into modules. The direct observation of preferential attachment of existing interactions to hubs through gene duplication explains the scale-free organization. The evolutionary optimal modular organization is favored by the addition of new interactions to the network and by the avoidance of mis-interactions, as shown by simulations. The resurrection of ancestral networks and the direct observation of ancestral rewiring events allowed us to elucidate the role of whole genome triplication, elementary processes and evolutionary mechanisms in the origin of a biological network.
