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

Urano, D., Maruta, N., Trusov, Y., Stoian, R., Wu, Q., Liang, Y., Jaiswal, D. K., Thung, L., Jackson, D., Botella, J. R., Jones, A. M. (September 2016) Saltational evolution of the heterotrimeric G protein signaling mechanisms in the plant kingdom. Sci Signal, 9 (446). ra93. ISSN 1937-9145 (Electronic)1945-0877 (Linking)

DOI: 10.1126/scisignal.aaf9558


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 Galpha (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 alpha-helix region that enables interaction with its partner Gbetagamma. 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 Galpha and XLG proteins all function with Gbetagamma and evolved to operate both independently and cooperatively. The XLG-Gbetagamma machinery specialized in environmental stress responses, whereas the canonical Galpha-Gbetagamma retained developmental roles. Some developmental processes, such as shoot development, involve both Galpha and XLG acting cooperatively or antagonistically. These extensive and rapid evolutionary changes in XLG structure compared to those of the canonical Galpha subunit contrast with the accepted notion of how pathway diversification occurs through gene duplication with subsequent incremental coevolution of residues among interacting proteins.

Item Type: Paper
Subjects: organs, tissues, organelles, cell types and functions > cell types and functions > cell functions > cell signaling
bioinformatics > genomics and proteomics > genetics & nucleic acid processing > protein structure, function, modification > protein types > G protein
organism description > plant
CSHL Authors:
Communities: CSHL labs > Jackson lab
Depositing User: Matt Covey
Date: 20 September 2016
Date Deposited: 23 Sep 2016 19:25
Last Modified: 23 Sep 2016 19:25
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