Plants being sessile integrate information from a variety of endogenous and external cues simultaneously to optimize growth and development. This necessitates the signaling networks in plants to be highly dynamic and flexible. One such network involves heterotrimeric G-proteins comprised of G alpha, G beta, and G gamma subunits, which influence many aspects of growth, development, and stress response pathways. In plants such as Arabidopsis, a relatively simple repertoire of G-proteins comprised of one canonical and three extra-large G alpha, one G beta and three G gamma subunits exists. Because the G beta and G gamma proteins form obligate dimers, the phenotypes of plants lacking the sole G beta or all G gamma genes are similar, as expected. However, G alpha proteins can exist either as monomers or in a complex with G beta gamma, and the details of combinatorial genetic and physiological interactions of different G alpha proteins with the sole G beta remain unexplored. To evaluate such flexible, signal-dependent interactions and their contribution toward eliciting a specific response, we have generated Arabidopsis mutants lacking specific combinations of G alpha and G beta genes, performed extensive phenotypic analysis, and evaluated the results in the context of subunit usage and interaction specificity. Our data show that multiple mechanistic modes, and in some cases complex epistatic relationships, exist depending on the signal-dependent interactions between the G alpha and G beta proteins. This suggests that, despite their limited numbers, the inherent flexibility of plant G-protein networks provides for the adaptability needed to survive under continuously changing environments.