Resurrected protein interaction networks reveal the innovation potential of ancient whole genome duplication

Abstract

The evolution of plants is characterized by several rounds of ancient whole genome duplication, sometimes closely associated with the origin of large groups of species. A good example is the γ triplication at the origin of core eudicots. Core eudicots comprise about 75% of flowering plants and are characterized by the canalization of reproductive development. To better understand the impact of this genomic event, we studied the protein interaction network of MADS-domain transcription factors, which are key regulators of reproductive development. We accurately inferred, resurrected and tested the interactions of ancestral proteins before and after the triplication and directly compared these ancestral networks to the networks of Arabidopsis and tomato. We find that the γ triplication generated a dramatically innovated network that strongly rewired through the addition of many new interactions. Many of these interactions were established between paralogous proteins and a new interaction partner, establishing new redundancy. Simulations show that both node and edge addition through the triplication were important to maintain modularity in the network. In addition to generating insights into the impact of whole genome duplication and elementary processes involved in network evolution, our data provide a resource for comparative developmental biology in flowering plants.

Protein interaction evolution from promiscuity to specificity with reduced flexibility in an increasingly complex network

“…In two previous studies, we inferred and resurrected ancestral sequences for plant MADS-domain proteins which made it possible to characterize these ancient proteins using current laboratory methods3747. We were able to reconstruct the networks of their protein interactions as dimers, using the yeast-two-hybrid method, at different time points in evolution.…”

“…We were able to reconstruct the networks of their protein interactions as dimers, using the yeast-two-hybrid method, at different time points in evolution. One striking observation was that the gamma whole genome triplication at the origin of core eudicots induced strong rewiring of this dimeric MADS-domain protein interaction network37. While this major event also added many new interactions, the density of the network, i.e.…”

“…A first network was reconstructed at 120 mya (million years ago), at the origin of eudicots before the gamma whole genome triplication named pre-PIN and a second at 109 mya at the split of the Asterids and Rosids, named post-gamma PIN or post-PIN. In addition, we applied the same methodology to investigate the extant protein networks of Arabidopsis thaliana (Ara-PIN) and Solanum lycopersicum (Sol-PIN)37. The interactions were quantitatively determined and the two-hybrid network was subtracted.…”

“…Alternatively, the two copies can partition functions. Such scenarios can explain the retention of the duplicated genes after each major duplication event followed by rewiring of the resulting protein networks293031323334353637.…”

“…Some MADS-domain proteins have come to function as hubs, interacting with many other MADS-domain proteins. Other proteins can be considered as islands, having very few protein-protein interactions26374243. Our understanding of the molecular mechanisms involved in positioning these proteins into their protein-protein interaction networks is far from complete.…”