Research ArticleEVOLUTION

Saltational evolution of the heterotrimeric G protein signaling mechanisms in the plant kingdom

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Sci. Signal.  20 Sep 2016:
Vol. 9, Issue 446, pp. ra93
DOI: 10.1126/scisignal.aaf9558

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Diverge and conquer

Signaling through heterotrimeric G proteins mediates diverse developmental and adaptive processes in eukaryotes. Through gene duplication followed by gradual evolution, animals evolved multiple closely related Gα subunits that mediate distinct cellular responses. Plants have both canonical Gα and extra-large Gα (XLG) proteins. The C-terminal portions of XLGs are homologous to canonical Gα, but the N-terminal portions of these proteins lack characterized domains. Urano et al. found that plant canonical Gα proteins evolved slowly, like their animal counterparts, but that XLG proteins underwent rapid diversification early in the land plant lineage. Arabidopsis thaliana has a single canonical Gα and three XLGs. Phenotypic analyses of Arabidopsis Gα and XLG mutants revealed that canonical Gα signaling was primarily involved in developmental processes, whereas XLGs preferentially mediated stress responses. These results suggest that rapid diversification of XLGs may have enabled plants to adapt to the profound environmental changes that accompanied the invasion of land.

Abstract

Signaling proteins evolved diverse interactions to provide specificity for distinct stimuli. Signaling complexity in the G protein (heterotrimeric guanosine triphosphate–binding protein) network was achieved in animals through subunit duplication and incremental evolution. By combining comprehensive and quantitative phenotypic profiles of Arabidopsis thaliana with protein evolution informatics, we found that plant heterotrimeric G protein machinery evolved by a saltational (jumping) process. Sequence similarity scores mapped onto tertiary structures, and biochemical validation showed that the extra-large Gα (XLG) subunit evolved extensively in the charophycean algae (an aquatic green plant) by gene duplication and gene fusion. In terrestrial plants, further evolution uncoupled XLG from its negative regulator, regulator of G protein signaling, but preserved an α-helix region that enables interaction with its partner Gβγ. The ancestral gene evolved slowly due to the molecular constraints imposed by the need for the protein to maintain interactions with various partners, whereas the genes encoding XLG proteins evolved rapidly to produce three highly divergent members. Analysis of A. thaliana mutants indicated that these Gα and XLG proteins all function with Gβγ and evolved to operate both independently and cooperatively. The XLG-Gβγ machinery specialized in environmental stress responses, whereas the canonical Gα-Gβγ retained developmental roles. Some developmental processes, such as shoot development, involve both Gα and XLG acting cooperatively or antagonistically. These extensive and rapid evolutionary changes in XLG structure compared to those of the canonical Gα subunit contrast with the accepted notion of how pathway diversification occurs through gene duplication with subsequent incremental coevolution of residues among interacting proteins.

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