Distribution and the evolutionary history of G-protein components in plant and algal lineages

Heterotrimeric G-proteins show sporadic presence in algae, and specific components are frequently lost in land plants, suggesting distinct distribution and evolutionary histories of their constituents. Heterotrimeric G-protein complexes comprising G alpha-, G beta-, and G gamma-subunits and the regulator of G-protein signaling (RGS) are conserved across most eukaryotic lineages. Signaling pathways mediated by these proteins influence overall growth, development, and physiology. In plants, this protein complex has been characterized primarily from angiosperms with the exception of spreading-leaved earth moss (Physcomitrium patens) and Chara braunii (charophytic algae). Even within angiosperms, specific G-protein components are missing in certain species, whereas unique plant-specific variants-the extra-large G alpha (XLG alpha) and the cysteine-rich G gamma proteins-also exist. The distribution and evolutionary history of G-proteins and their function in nonangiosperm lineages remain mostly unknown. We explored this using the wealth of available sequence data spanning algae to angiosperms representing extant species that diverged approximately 1,500 million years ago, using BLAST, synteny analysis, and custom-built Hidden Markov Model profile searches. We show that a minimal set of components forming the XLG alpha beta gamma trimer exists in the entire land plant lineage, but their presence is sporadic in algae. Additionally, individual components have distinct evolutionary histories. The XLG alpha exhibits many lineage-specific gene duplications, whereas G alpha and RGS show several instances of gene loss. Similarly, G beta remained constant in both number and structure, but G gamma diverged before the emergence of land plants and underwent changes in protein domains, which led to three distinct subtypes. These results highlight the evolutionary oddities and summarize the phyletic patterns of this conserved signaling pathway in plants. They also provide a framework to formulate pertinent questions on plant G-protein signaling within an evolutionary context.