The Agrobacterium tumefaciens virulence gene chvE is part of a putative ABC-type sugar transport operon

Abstract

The Agrobacterium tumefaciens virulence determinant ChvE is a periplasmic binding protein which participates in chemotaxis and virulence gene induction in response to monosaccharides which occur in the plant wound environment. The region downstream of the A. tumefaciens chvE gene was cloned and sequenced for nucleotide and expression analysis. Three open reading frames transcribed in the same direction as chvE were revealed. The first two, together with chvE, encode putative proteins of a periplasmic binding protein-dependent sugar uptake system, or ABC-type (ATP binding cassette) transporter. The third open reading frame encodes a protein of unknown function. The deduced transporter gene products are related on the amino acid level to bacterial sugar transporters and probably function in glucose and galactose uptake. We have named these genes gguA, -B, and -C, for glucose galactose uptake. Mutations in gguA, gguB, or gguC do not affect virulence of A. tumefaciens on Kalanchöe diagremontiana; growth on 1 mM galactose, glucose, xylose, ribose, arabinose, fucose, or sucrose; or chemotaxis toward glucose, galactose, xylose, or arabinose.Agrobacterium tumefaciens is a gram-negative bacterial pathogen that forms crown gall tumors on dicotyledonous plants by transferring a piece of its DNA into the plant cell, where it becomes stably integrated into the host genome (for a review, see reference 44). The transferred DNA, termed the T-DNA, is processed and transported from the bacterial cell by components encoded by the vir regulon. The vir genes are induced in response to chemical signals of the plant wound site, which include low pH, phenolic compounds, and monosaccharide components of the plant cell wall (6,33,38,39). Monosaccharides are bound by the periplasmic sugar-binding protein ChvE, which then interacts with the periplasmic region of the membrane-bound VirA molecule of the VirA-VirG sensor-regulator pair to activate transcription of the vir regulon (24,34,45). ChvE also mediates chemotaxis toward various sugars, presumably by interacting in the sugar-bound form with an unidentified membrane-bound receptor (6). Thus, this sugar-binding protein plays at least two roles in the physiology and virulence of A. tumefaciens.ChvE may have an additional role as well. In gram-negative bacteria, periplasmic binding proteins like ChvE often constitute part of a high-affinity uptake system (22, 23). These transporters couple hydrolysis of ATP to transport and are capable of taking up solutes at low concentrations (micromolar range and less) and concentrating them across a large gradient. Structurally, they are composed of a minimum of three components: a periplasmic binding protein, a membrane-bound transport protein(s) which interacts with the periplasmic protein bound to its ligand, and an ATP-binding protein(s) which energizes transport at the cytoplasmic face of the membrane. These periplasmic binding protein-dependent transporters take up a wide assortment of solutes, and a large number of separate transport systems for...

Structure, Function, and Evolution of Bacterial ATP-Binding Cassette Systems

“…Pathogens are able to scavenge iron from these sources by secreting highaffinity iron-complexing molecules called siderophores and reabsorbing them as iron-siderophore complexes (see reference 516 for a review). Another example of involvement in virulence is the chvE-gguAB operon in Agrobacterium tumefaciens, which encodes a glucose and galactose importer (61,241). Sugar binding to ChvE triggers a signaling response that results in virulence gene expression.…”

Agrobacterium -Mediated Plant Transformation: the Biology behind the “Gene-Jockeying” Tool

“…Further research defined the roles of many of these genes. Included among these functions are exopolysaccharide production, modification, and secretion (pscA/exoC, chvA, and chvB [36,37,88,89,313]) and other roles in bacterial attachment to plant cells (att genes [212,213]), sugar transporters involved in coinduction of vir genes (chvE [86,172,289]), regulation of vir gene induction (chvD [204]), and T-DNA transport (acvB [168,248,360,361,362]). …”

Sinorhizobium meliloti pSymB carries genes necessary for arabinose transport and catabolism

“…The gene araA is a homologue of chvE in Agrobacterium tumefaciens, which has been shown to couple sugar binding with the induction of plant virulence genes (Huang et al, 1990;Cangelosi et al, 1990), and is thought to be the periplasmic sugar-binding protein of an ATP-binding cassette (ABC) transporter (Kemner et al, 1997). An InterProScan search showed that AraA is a member of the periplasmic binding protein family (InterPro accession number IPR001761).…”