Abstract
Heterotrimeric G proteins comprising Gα, Gβ, and Gγ subunits regulate many fundamental growth and development processes in all eukaryotes. Plants possess a relatively limited number of G-protein components compared with mammalian systems, and their detailed functional characterization has been performed mostly in Arabidopsis (Arabidopsis thaliana) and rice (Oryza sativa). However, the presence of single Gα and Gβ proteins in both these species has significantly undermined the complexity and specificity of response regulation in plant G-protein signaling. There is ample pharmacological evidence for the role of G proteins in regulation of legume-specific processes such as nodulation, but the lack of genetic data from a leguminous species has restricted its direct assessment. Our recent identification and characterization of an elaborate G-protein family in soybean (Glycine max) and the availability of appropriate molecular-genetic resources have allowed us to directly evaluate the role of G-protein subunits during nodulation. We demonstrate that all G-protein genes are expressed in nodules and exhibit significant changes in their expression in response to Bradyrhizobium japonicum infection and in representative supernodulating and nonnodulating soybean mutants. RNA interference suppression and overexpression of specific G-protein components results in lower and higher nodule numbers, respectively, validating their roles as positive regulators of nodule formation. Our data further show preferential usage of distinct G-protein subunits in the presence of an additional signal during nodulation. Interestingly, the Gα proteins directly interact with the soybean nodulation factor receptors NFR1α and NFR1β, suggesting that the plant G proteins may couple with receptors other than the canonical heptahelical receptors common in metazoans to modulate signaling.
Highlights
Heterotrimeric G proteins comprising Ga, Gb, and Gg subunits regulate many fundamental growth and development processes in all eukaryotes
The structure/function information on G proteins is mostly limited to Arabidopsis (Arabidopsis thaliana) and rice (Oryza sativa), where their roles have been established in regulation of a multitude of signaling pathways, such as those regulated by multiple phytohormones, sugar, light, and pathogens (Fujisawa et al, 1999; Ueguchi-Tanaka et al, 2000; Ullah et al, 2001; Wang et al, 2001; Pandey and Assmann, 2004; Oki et al, 2005; Pandey et al, 2006; Trusov et al, 2006; Temple and Jones, 2007; Warpeha et al, 2007; Nilson and Assmann, 2010; Chakravorty et al, 2011; Utsunomiya et al, 2011)
Given the general position of G proteins as integrators of receptor and effector proteins during signaling, we evaluated whether G proteins interact with known Nod factor receptors (NFRs)
Summary
Heterotrimeric G proteins comprising Ga, Gb, and Gg subunits regulate many fundamental growth and development processes in all eukaryotes. The importance of G proteins in regulating fundamental signaling pathways involved in sensory perception, neurotransmission, hormone perception, and immunity-related cues has prompted their in-depth characterization (Cabrera-Vera et al, 2003; Offermanns, 2003) Such studies have revealed an elegant mechanism where a signal-dependent exchange of GTP for GDP on Ga protein leads to the dissociation of inactive GDP$Gabg heterotrimer into active GTP$Ga and Gbg dimer. We have recently identified an elaborate G-protein family in soybean (Glycine max), consisting of 4 Ga, 4 Gb, and 10 Gg proteins (Bisht et al, 2010; Choudhury et al, 2011), which has greatly expanded the plant G-protein networks Detailed analysis of these proteins has started to reveal properties reminiscent of mammalian G proteins such as subunit-specific expression patterns, interaction specificity between different protein subunits, and distinct biochemical activities of individual Ga proteins (Choudhury et al, 2012); the functional significance of such differences remains unclear
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