A Golgi-localized Hexose Transporter Is Involved in Heterotrimeric G Protein-mediated Early Development inArabidopsis

Abstract

Signal transduction involving heterotrimeric G proteins is universal among fungi, animals, and plants. In plants and fungi, the best understood function for the G protein complex is its modulation of cell proliferation and one of several important signals that are known to modulate the rate at which these cells proliferate is D-glucose. Arabidopsis thaliana seedlings lacking the ␤ subunit (AGB1) of the G protein complex have altered cell division in the hypocotyl and are D-glucose hypersensitive. With the aim to discover new elements in G protein signaling, we screened for gain-of-function suppressors of altered cell proliferation during early development in the agb1-2 mutant background. One agb1-2-dependent suppressor, designated sgb1-1 D for suppressor of G protein beta1 (agb1-2), restored to wild type the altered cell division in the hypocotyl and sugar hypersensitivity of the agb1-2 mutant. Consistent with AGB1 localization, SGB1 is found at the highest steady-state level in tissues with active cell division, and this level increases in hypocotyls when grown on D-glucose and sucrose. SGB1 is shown here to be a Golgi-localized hexose transporter and acts genetically with AGB1 in early seedling development. INTRODUCTIONAn evolutionarily ancient mechanism for sensing extracellular signals involves the heterotrimeric G proteins, composed of ␣, ␤, and ␥ subunits. Heterotrimeric G protein complexes link ligand perception via seven-transmembrane (7TM), G protein-coupled receptors (GPCRs) to downstream effectors. Genes that encode G protein signaling elements have been identified in amoebae, fungi, plants, and animals, but among all multicellular eukaryotes, plants have the simplest repertoire of G protein elements to date. Specifically, the Arabidopsis genome encodes a single canonical G␣ and G␤ (AGB1) subunit and two G␥ subunits and a single regulator of G signaling (RGS1) protein (Jones and Assmann, 2004). There are as yet no plant GPCRs having confirmed ligands, although plants do have a limited set of predicted 7TM proteins (Moriyama and Jones, unpublished data). Similarly, there are few known downstream effectors that physically interact with either the plant G␣ subunit or the G␤␥ dimer. One example is a pirin protein (Lapik and Kaufman, 2003), known to serve as a transcriptional cofactor in humans, but with unknown function in Arabidopsis. Based on either genetic or biochemical tests, G␣ effectors in plants also include phospholipase D (Mishra et al., 2006) and ion channels (Aharon et al., 1998;Wang et al., 2001). Recently, we reported that a plant interactor and putative effector to G␣ is an outer membrane plastid protein designated THF1, and this protein together with G␣ comprises part of a dglucose signaling network (Huang et al., 2006).In animals and yeast, heterotrimeric G proteins couple a diverse set of signals such as photons, ions, small molecules, sugars, peptides, and protein ligands (Jones and Assmann, 2004) to control a broad range of physiology (Csaszar and Abel, 2001;Rosenkilde et al., 2001;Roc...

Monosaccharide Absorption Activity of Arabidopsis Roots Depends on Expression Profiles of Transporter Genes under High Salinity Conditions

“…The ERD6-like family is a facilitated diffusion transporter for monosaccharides including glucose (13). Although the transport system of the pGlcT family has not yet been defined, SGB1, which is a member of the pGlcT family, has been shown to transport glucose (17). Other families of monosaccharide transporters have been reported to be secondary active transporters.…”

Dissecting Arabidopsis Gβ Signal Transduction on the Protein Surface

“…Other cell proliferation defects were characterized in G-protein mutants. For example, in the presence of 1% sucrose (Suc) or glucose (Glu), 50-h-old etiolated agb1 seedlings display shorter hypocotyls and more open apical hooks, which is the consequence of reduced epidermal cell numbers in the hypocotyl (Ullah et al, 2003;Wang et al, 2006). agb1 mutants also display an increased stomatal index and altered leaf, silique, and rosette morphologies (Ullah et al, 2003;Zhang et al, 2008;Booker et al, 2012).…”

Acireductone Dioxygenase 1 (ARD1) Is an Effector of the Heterotrimeric G Protein β Subunit in Arabidopsis

“…Screen for Suppressors of agb1-2 and Plasmid Rescue-sgb3-1 D was identified in the activation tagging suppressor screen that was described previously by Wang et al (9).…”

“…Eight genetic loci suppressed this phenotype to varying degrees, and these loci were named Suppressor of G Beta 1-8. The suppressor screen and one of the resulting genetic suppressors, SGB1, was described previously (9). This study focuses on SGB3, which fully rescued the hypocotyl length phenotype and partially rescued the apical hook opening phenotype.…”

“…Although we previously identified proteins that interact genetically (SGB1 (9)) and physically (NDL1 (10)) with AGB1, to date no AGB1 effectors (i.e. proteins whose activities are regulated by AGB1) have been identified in plants.…”