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

Urano, Daisuke, Maruta, Natsumi, Trusov, Yuri, Stoian, Richard, Wu, Qingyu, Liang, Ying, Jaiswal, Dinesh Kumar, Thung, Leena, Jackson, David, Botella, José Ramón and Jones, Alan M. (2016) Saltational evolution of the heterotrimeric G protein signaling mechanisms in the plant kingdom. Science Signaling, 9 446: . doi:10.1126/scisignal.aaf9558


Author Urano, Daisuke
Maruta, Natsumi
Trusov, Yuri
Stoian, Richard
Wu, Qingyu
Liang, Ying
Jaiswal, Dinesh Kumar
Thung, Leena
Jackson, David
Botella, José Ramón
Jones, Alan M.
Title Saltational evolution of the heterotrimeric G protein signaling mechanisms in the plant kingdom
Journal name Science Signaling   Check publisher's open access policy
ISSN 1937-9145
Publication date 2016-09-20
Year available 2016
Sub-type Article (original research)
DOI 10.1126/scisignal.aaf9558
Open Access Status Not yet assessed
Volume 9
Issue 446
Total pages 10
Place of publication Washington, DC, United States
Publisher American Association for the Advancement of Science
Language eng
Subject 1303 Biochemistry
1312 Molecular Biology
1307 Cell Biology
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 G alpha (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 a-helix region that enables interaction with its partner G beta gamma. The ancestral gene evolved slowly due to themolecular constraints imposed by the need for the protein tomaintain 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 G alpha and XLG proteins all function with G beta gamma and evolved to operate both independently and cooperatively. The XLG-G beta gamma machinery specialized in environmental stress responses, whereas the canonical G alpha-G beta gamma retained developmental roles. Some developmental processes, such as shoot development, involve both Ga and XLG acting cooperatively or antagonistically. These extensive and rapid evolutionary changes in XLG structure compared to those of the canonical G alpha subunit contrast with the accepted notion of how pathway diversification occurs through gene duplication with subsequent incremental coevolution of residues among interacting proteins.
Formatted 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.
Keyword Biochemistry & Molecular Biology
Cell Biology
Biochemistry & Molecular Biology
Cell Biology
Q-Index Code C1
Q-Index Status Provisional Code
Grant ID R01GM065989
MCB-0718202
DE-FG02-05er15671
Institutional Status UQ

Document type: Journal Article
Sub-type: Article (original research)
Collections: HERDC Pre-Audit
School of Agriculture and Food Sciences
 
Versions
Version Filter Type
Citation counts: TR Web of Science Citation Count  Cited 10 times in Thomson Reuters Web of Science Article | Citations
Scopus Citation Count Cited 9 times in Scopus Article | Citations
Google Scholar Search Google Scholar
Created: Tue, 11 Oct 2016, 11:01:26 EST by System User on behalf of Learning and Research Services (UQ Library)