Growth attenuation under saline stress is mediated by the heterotrimeric G protein complex

Abstract

BackgroundPlant growth is plastic, able to rapidly adjust to fluctuation in environmental conditions such as drought and salinity. Due to long-term irrigation use in agricultural systems, soil salinity is increasing; consequently crop yield is adversely affected. It is known that salt tolerance is a quantitative trait supported by genes affecting ion homeostasis, ion transport, ion compartmentalization and ion selectivity. Less is known about pathways connecting NaCl and cell proliferation and cell death. Plant growth and cell proliferation is, in part, controlled by the concerted activity of the heterotrimeric G-protein complex with glucose. Prompted by the abundance of stress-related, functional annotations of genes encoding proteins that interact with core components of the Arabidopsis heterotrimeric G protein complex (AtRGS1, AtGPA1, AGB1, and AGG), we tested the hypothesis that G proteins modulate plant growth under salt stress.ResultsNa+ activates G signaling as quantitated by internalization of Arabidopsis Regulator of G Signaling protein 1 (AtRGS1). Despite being components of a singular signaling complex loss of the Gβ subunit (agb1-2 mutant) conferred accelerated senescence and aborted development in the presence of Na+, whereas loss of AtRGS1 (rgs1-2 mutant) conferred Na+ tolerance evident as less attenuated shoot growth and senescence. Site-directed changes in the Gα and Gβγ protein-protein interface were made to disrupt the interaction between the Gα and Gβγ subunits in order to elevate free activated Gα subunit and free Gβγ dimer at the plasma membrane. These mutations conferred sodium tolerance. Glucose in the growth media improved the survival under salt stress in Col but not in agb1-2 or rgs1-2 mutants.ConclusionsThese results demonstrate a direct role for G-protein signaling in the plant growth response to salt stress. The contrasting phenotypes of agb1-2 and rgs1-2 mutants suggest that G-proteins balance growth and death under salt stress. The phenotypes of the loss-of-function mutations prompted the model that during salt stress, G activation promotes growth and attenuates senescence probably by releasing ER stress.

Extra-Large G Proteins Expand the Repertoire of Subunits in Arabidopsis Heterotrimeric G Protein Signaling

“…Indeed, Maruta et al (2015) demonstrated that disruption of either XLG2 or AGB1 was able to suppress the cell death phenotype of bir1 and resulted in impaired pathogen defense responses, including ROS production. These results illustrate that G proteins modulate multiple cell death pathways, either suppressing (Warpeha et al, 2008;Wei et al, 2008;Chen and Brandizzi, 2012;Colaneri et al, 2014;Yu and Assmann, 2015) or stimulating (Liu et al, 2013;Maruta et al, 2015) cell death in a stimulispecific manner. XLGs also function in developmental pathways.…”

“…Colaneri et al (2014) found that agg1 and agg2 single mutants were not hypersensitive to NaCl; however, the agg1-1c agg2-1 agg3-1 triple mutant appeared hypersensitive to NaCl.…”

“…The four phenotypes we selected were NaCl, tunicamycin, and D-Glc hypersensitivity and increased stomatal density. Colaneri et al (2014) showed that Arabidopsis agb1 mutants are hypersensitive to NaCl, while gpa1 is hyposensitive to NaCl. Urano et al (2014) examined Ga mutants available in rice and maize (Zea mays) and found that the Ga mutants were, much like gpa1 mutants in Arabidopsis, hyposensitive to salt treatment.…”

“…However, Arabidopsis heterotrimeric G proteins have been implicated in a surprisingly large number of phenotypes, which is seemingly contradictory given the relative scarcity of subunits. Arabidopsis G proteins have been implicated in cell division Chen et al, 2006) and morphological development in various tissues, including hypocotyls (Ullah et al, , 2003, roots (Ullah et al, 2003;Chen et al, 2006;Li et al, 2012), leaves (Lease et al, 2001;Ullah et al, 2001), inflorescences (Ullah et al, 2003), and flowers and siliques (Lease et al, 2001), as well as in pathogen responses (Llorente et al, 2005;Trusov et al, 2006;Cheng et al, 2015), regulation of stomatal movement (Wang et al, 2001;Coursol et al, 2003;Fan et al, 2008) and development Nilson and Assmann, 2010), cell wall composition (Delgado-Cerezo et al, 2012), responses to various light stimuli (Warpeha et al, 2007;Botto et al, 2009), responses to multiple abiotic stimuli (Huang et al, 2006;Pandey et al, 2006;Trusov et al, 2007;Zhang et al, 2008;Colaneri et al, 2014), responses to various hormones during germination (Ullah et al, 2002), and postgermination development (Ullah et al, 2002;Pandey et al, 2006;Trusov et al, 2007). Since the Gg subunit appeared to be the only subunit that provides diversity in heterotrimer composition in Arabidopsis, it was proposed that all functional specificity in heterotrimeric G protein signaling was provided by the Gg subunit (Trusov et al, 2007;Chakravorty et al, 2011;Thung et al, 2012Thung et al, , 2013.…”

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

“…S10 and S11). The agb1 single, xlg123 triple, and the agg123 triple null mutants displayed hypersensitivity to multiple stresses (2,28,30,31), whereas the gpa1 mutant had wild-type stress responses. Sodium chloride treatment severely arrested leaf growth in the xlg123 triple, gpa1 xlg123 quadruple, agb1 single, and agg123 triple mutants but not in the gpa1 mutant or Col-0 control (Fig.…”