Type B Heterotrimeric G Protein γ-Subunit Regulates Auxin and ABA Signaling in Tomato

Abstract

Heterotrimeric G proteins composed of a, b, and g subunits are central signal transducers mediating the cellular response to multiple stimuli in most eukaryotes. Gg subunits provide proper cellular localization and functional specificity to the heterotrimer complex. Plant Gg subunits, divided into three structurally distinct types, are more diverse than their animal counterparts. Type B Gg subunits, lacking a carboxyl-terminal isoprenylation motif, are found only in flowering plants. We present the functional characterization of type B Gg subunit (SlGGB1) in tomato (Solanum lycopersicum). We show that SlGGB1 is the most abundant Gg subunit in tomato and strongly interacts with the Gb subunit. Importantly, the green fluorescent proteinSlGGB1 fusion protein as well as the carboxyl-terminal yellow fluorescent protein-SlGGB1/amino-terminal yellow fluorescent protein-Gb heterodimer were localized in the plasma membrane, nucleus, and cytoplasm. RNA interference-mediated silencing of SlGGB1 resulted in smaller seeds, higher number of lateral roots, and pointy fruits. The silenced lines were hypersensitive to exogenous auxin, while levels of endogenous auxins were lower or similar to those of the wild type. SlGGB1-silenced plants also showed strong hyposensitivity to abscisic acid (ABA) during seed germination but not in other related assays. Transcriptome analysis of the transgenic seeds revealed abnormal expression of genes involved in ABA sensing, signaling, and response. We conclude that the type B Gg subunit SlGGB1 mediates auxin and ABA signaling in tomato.

Mutation of RGG2, which encodes a type B heterotrimeric G protein γ subunit, increases grain size and yield production in rice

“…Structurally, the RGG2 subunit is similar to the truncated AGG3 protein, because RGG2 lacks both the transmembrane domain and the C‐terminus. The type B G γ subunit in tomato, SlGGB1, also localizes to the nucleus, plasma membrane and cytoplasm (Subramaniam et al ., ), thus sharing a common localization pattern with RGG2. These results indicate that both the transmembrane domain and CaaX motif might be sufficient but not essential for plasma membrane localization of G γ protein in plants.…”

“…Both RGG1 and RGG2 were constitutively expressed (Figure ). However, the expression levels of RGG2 were significantly higher than those of RGG1 , GS3 , qPE9‐1 / DEP1 and GGC2 in all tissues examined, and this finding was similar to the expression patterns of G γ genes in tomato (Subramaniam et al ., ). These results suggest that RGG2 may play an important role in rice development.…”

“…Structurally, the RGG2 subunit is similar to the truncated AGG3 protein, because RGG2 lacks both the transmembrane domain and the C-terminus. The type B G c subunit in tomato, SlGGB1, also localizes to the nucleus, plasma membrane and cytoplasm (Subramaniam et al, 2016), thus sharing a common localization pattern with RGG2.…”

The Role of Gβ Protein in Controlling Cell Expansion via Potential Interaction with Lipid Metabolic Pathways

“…Analysis of G-protein regulated pathways in Arabidopsis (Arabidopsis thaliana), rice (Oryza sativa), maize (Zea mays), soybean (Glycine max), tomato (Solanum lycopersicum), and pea (Pisum sativum) has confirmed their roles in controlling multiple aspects of plant development, signaling, and stress responses (Misra et al, 2007;Sun et al, 2014Sun et al, , 2018Urano and Jones, 2014;Roy Choudhury and Pandey, 2015;Subramaniam et al, 2016;Bi et al, 2018;Liang et al, 2018;Wu et al, 2018). The most elaborate data are available from Arabidopsis where G-protein mutants exhibit altered phenotypes in response to almost all plant hormones at the physiological and molecular (large-scale omics) level (Pandey and Assmann, 2004;Pandey et al, 2006Pandey et al, , 2008Pandey et al, , 2009Pandey et al, , 2010Fan et al, 2008;Zhao et al, 2010;Alvarez et al, 2011;Chakravorty et al, 2011;Jin et al, 2013;Tsugama et al, 2013;Wang et al, 2017;Peng et al, 2018;Zhang et al, 2018b).…”

“…The most elaborate data are available from Arabidopsis where G-protein mutants exhibit altered phenotypes in response to almost all plant hormones at the physiological and molecular (large-scale omics) level (Pandey and Assmann, 2004;Pandey et al, 2006Pandey et al, , 2008Pandey et al, , 2009Pandey et al, , 2010Fan et al, 2008;Zhao et al, 2010;Alvarez et al, 2011;Chakravorty et al, 2011;Jin et al, 2013;Tsugama et al, 2013;Wang et al, 2017;Peng et al, 2018;Zhang et al, 2018b). Similarly, G-protein mutants in Arabidopsis (and other plants) show altered sensitivity to multiple abiotic stresses such as drought, temperature, salt, redox, ultraviolet, and high light (Zhang et al, 2011;He et al, 2013;Torres et al, 2013;Subramaniam et al, 2016;Lee et al, 2017;Kaur et al, 2018;Yu and Assmann, 2018). G-proteins also mediate regulation of defense responses against host and nonhost bacterial pathogens, a variety of biotrophic and necrotrophic fungi and viruses (Liu et al, 2013;Lorek et al, 2013;Aranda-Sicilia et al, 2015;Cheng et al, 2015;Maruta et al, 2015;Meng et al, 2015;Liang et al, 2016Liang et al, , 2018Yuan et al, 2017;Bi et al, 2018;Wang et al, 2018).…”