Agrobacterium is a genus of Gram-negative bacteria that uses horizontal gene transfer to cause tumors in many plant species with agricultural and economic importance including woody ornamental shrubs (rose), vines (grape), shade trees, fruit trees (cherry, berry, walnut), and herbaceous perennials. Agrobacterium tumefaciens is the most commonly studied species in this genus. A. tumefaciens causes typical crown-gall diseases. The disease manifests as a tumor-like growth or gall usually at the junction of the root and shoot. Infection by the species Agrobacterium vitis results in cane gall on grapevines while A. rhizogenes causes excessive formation of hairy roots or root tumors. Agrobacterium–plant interaction is an excellent paradigm for studying both plant and bacterial responses, as well as the role of chemical signaling in these processes. A. tumefaciens–plant interaction is now relatively well-understood as a result of significant findings made over the past four decades (for reviews refer to Gelvin, 2003; Brencic and Winans, 2005; McCullen and Binns, 2006; Yuan and Williams, 2012; Pitzschke, 2013). The virulence proficiency of A. tumefaciens is dependent on the presence of the Tumor-inducing (Ti) plasmid, which harbors a Transferred DNA (T-DNA) defined by two direct repeat sequences of approximately 25 base pairs, termed the left and right borders. Most studies have made use of nopaline metabolizing strains C58 and T37 (carrying plasmids pTiC58 and pTiT37, respectively) or the octopine utilizing strain A6 (carrying pTiA6). As a ubiquitous soil bacterium, Agrobacterium is capable of two lifestyles: independent free-living or acting as a pathogen in association with a plant host. When living independently, Agrobacterium virulence is essentially silent. Upon detection of plant-derived signals in the rhizosphere, Agrobacterium activates its chromosomal virulence genes (chv genes) and Ti plasmid encoded virulence genes (vir genes). Vir genes are directly involved in T-DNA cleavage from the Ti plasmid, T-DNA processing, transferring and integration into plant nuclei, conversely, Chv genes are not directly involved in the T-DNA transfer process. Instead, chv genes play important roles in signal transduction necessary for Agrobacterium pathogenicity. Since T-DNA carries genes for the synthesis of indole-3-acetic acid (IAA) and cytokinin (CK; also called oncogenic genes), their expression in plants leads to the production of a large amount of plant hormones that promote uncontrolled cell division and undifferentiated growth of plant tissues, resulting in the formation of a plant tumor and permanent plant genetic transformation.

In addition to genes responsible for IAA and CK production, T-DNA also contains genes for the synthesis of opines (unusual amino acid and sugar condensates). Opines produced by transformed plant cells can be metabolized by Agrobacterium as a source of nutrients. In addition, opines act as signals that activate Agrobacterium quorum sensing (QS). QS is a special form of cell-to-cell communication by which microorganisms synthesize, release, and perceive diffusible signals such as N-(3-oxooctanoyl)-DL-homoserine lactone (3OC8-HSL). QS enables a single cell to sense the number of surrounding cells (cell density) and coordinates their collective behavior. In Agrobacterium, QS plays important roles in interaction with plant hosts, which will be discussed in later sections.

Interestingly, T-DNA encoded oncogenic genes are neither physiologically nor biologically required for the T-DNA transfer process. Therefore, T-DNA encoded genes can be deleted and replaced with genes of interest, and such genetically modified “T-DNA” can still be transferred, integrated and expressed in the plant cell. This unique ability of inter-kingdom DNA transfer makes Agrobacterium an important tool for genetically modifying plants, allowing for incorporation of useful traits like resistance to insects and herbicides, production of recombinant vaccines, proteins, etc. In addition, T-DNA is distally located from vir genes required for T-DNA transfer process. Thus, T-DNA and vir genes can be separated onto two plasmids without affecting T-DNA transfer into plant hosts. This feature prompted the design and construction of binary vectors that greatly facilitate DNA manipulation and plant transformation, especially considering the large size of the Ti plasmid (over 200 kb).

Agrobacterium is capable of infecting/transforming a wide variety of plant species including long-lived woody plants and cultivated plants. However, plants vary greatly in their ability to be infected/transformed by Agrobacterium, even among ecotypes within species, and the underlying molecular mechanisms are poorly understood (Nam et al., 1997). To mount a successful infection in nature, it is important for Agrobacterium to precisely and specifically recognize and respond to a combination of plant-derived signals in the rhizosphere including acidity, plant released sugars and plant-derived phenolic compounds (Stachel et al., 1985; Brencic and Winans, 2005; McCullen and Binns, 2006; Gelvin, 2012; Yuan and Williams, 2012; Pitzschke, 2013). Agrobacterium virulence programing and associations with plant hosts are stringently and synergistically regulated by a combination of plant-derived chemicals.

The rhizosphere is the narrow region (within millimeter range of roots) of soil that is directly influenced by root exudates and is densely populated by soil microorganisms. Rhizosphere is rich in not only plant-derived but microbe-derived signals as well (Winans, 1992; Phillips et al., 2004; Bais et al., 2005). Plants routinely secrete organic acids such as lactic, citric, oxalic, and malic acids as well as other secondary metabolites, resulting in acidic rhizosphere conditions (Rivoal and Hanson, 1994; Xia and Roberts, 1994; Walker et al., 2003; Phillips et al., 2004; Bais et al., 2005; Wang et al., 2006; Huckelhoven, 2007; Badri and Vivanco, 2009). Upon wounding, plants release phenolic compounds as well as neutral and acidic sugars necessary to repair damaged tissue acidifying the rhizosphere (Winans, 1992). Therefore the rhizosphere, where Agrobacterium primarily infects plant hosts, is typically an acidic niche driven by various plant-released chemicals.

Upon close proximity to a suitable plant host in the rhizosphere, acidic conditions and plant-derived chemicals play important roles in initiating the Agrobacterium virulence program, which involves various Agrobacterium regulatory factors and signaling pathways (Winans, 1992). A chromosomally encoded che cluster (chemotaxis) allows A. tumefaciens to be attracted to plant-derived chemicals in the rhizosphere (Wright et al., 1998). In addition, three Agrobacterium chromosomally encoded genes chvA, chvB, and exoC are involved in synthesis of extracellular oligosaccharides, such as cyclic 1,2-b-D-glucan, that allows Agrobacterium to attach to plant hosts (Cangelosi et al., 1989). Upon perception of acidity characteristic of the rhizosphere, Agrobacterium mounts both a conserved response as well as a signaling specific response to infect plant hosts. This conserved response allows Agrobacterium to adapt to the rhizosphere niche by modulating metabolism and cellular adaptation, such as the induction of genes coding for cell envelope synthesis, stress response, transporters of sugars and peptides (Yuan et al., 2008b).

The signaling specific response to acidity is mediated by the chromosomally encoded ChvG/ChvI two-component system, as well as other genes that allow Agrobacterium to initiate its early virulence program (Yuan et al., 2008a). ChvG acts as the sensor kinase while ChvI functions as the response regulator (Winans, 1990, 1992; Chen and Winans, 1991; Charles and Nester, 1993; Mantis and Winans, 1993; Li et al., 2002). The ChvG/I system is believed to recognize acidity in the rhizosphere and activates the expression of several virulence factors including chvI, aopB encoding an outer membrane protein, katA encoding a catalase, pckA encoding phosphoenol carboxykinase, and the imp gene cluster encoding a type VI secretion system (T6SS; Yuan et al., 2008a). A more recent study confirmed that Agrobacterium T6SS is indeed induced by acidity in a ChvG/ChvI dependent manner (Wu et al., 2012). Perhaps most interestingly, it was found that upon perception of acidic signals, several vir genes were also induced including virG, virE0, and virH (Yuan et al., 2008a), consistent with the observation that the ChvG/ChvI system activates the proximal promoter (P2) of virG (Li et al., 2002). However, to be functional, VirG requires phosphorylation signaling from another plant-derived signal, e.g., plant-derived phenolic compounds, which will be discussed in the following section. It is noteworthy that in addition to ChvG/I, another chromosomally encoded virulence gene, chvE, is also involved in Agrobacterium response to acidity and plant-derived sugars in the rhizosphere, which will also be discussed later.

Originally it was believed that plant wounding was necessary for Agrobacterium infection and pathogenicity. However, recent advances have found that plant wounding is in fact not essential for Agrobacterium pathogenicity since unwounded plants can also infected by Agrobacterium pathogens (Brencic and Winans, 2005). Besides acidic signals, plant-derived phenolic compounds are essential for the induction of Agrobacterium virulence (Stachel et al., 1986). Moreover, phenolics serve as chemoattractants for Agrobacterium (Parke et al., 1987; Melchers et al., 1989). Structural specificities of virulence inducing phenolics include the presence of a benzene ring with a hydroxyl group at position 4 and a methoxy group at position 3 (Dixon and Paiva, 1995). 3,5-dimethoxyacetophenone (acetosyringone) and hydroxyacetosyringone were the first identified inducers of Agrobacterium virulence (Stachel et al., 1985; Hess et al., 1991). The Agrobacterium VirA/VirG two-component system located on the Ti plasmid has been suggested to recognize acetosyringone as a host specific signal and activate vir gene expression (Winans et al., 1986; Leroux et al., 1987; Shaw et al., 1988; Winans, 1990). The membrane receptor VirA functions as a dimer with four domains; the periplasmic, cytoplasmic linker, kinase, and receiver domains. Upon phenolic signal perception, the linker domain of one VirA subunit activates the kinase domain of the opposite dimerized subunit by intermolecular phosphorylation (Chang and Winans, 1992; Turk et al., 1994; Toyoda-Yamamoto et al., 2000). However, a previous study has shown the binding of radiolabelled phenolic compounds to two small proteins other than VirA and controversy remains regarding the exact mechanism involved in phenolic detection by VirA (Lee et al., 1992). Nevertheless, the auto-phosphorylated sensor kinase VirA phosphorylates the cytosolic response regulator VirG at the conserved Asp52 (Morel et al., 1990; Lee et al., 1995). Phosphorylated VirG binds to a 12-bp vir box located upstream of transcription start sites of vir genes, thereby activating their transcription (Stachel et al., 1985; Stachel and Nester, 1986; Jin et al., 1990a,b,c; Pazour and Das, 1990; Roitsch et al., 1990). In fact, phosphorylated VirG also activates its own expression by activating virG transcription at the distal promoter (p1; Chang and Winans, 1992; Liu et al., 1992, 2005; Jia et al., 2002; Li et al., 2002; Yuan et al., 2008a; Wise et al., 2010).

Vir genes of Agrobacterium are organized in several vir operons. There are eight vir operons on the octopine-type Ti plasmid and relatively fewer vir genes on the nopaline-type Ti plasmid (Stachel and Nester, 1986; Rogowsky et al., 1987; Kalogeraki and Winans, 1998; Kalogeraki et al., 2000; Brencic and Winans, 2005). The vir operons are typically organized as virH, virA, virB, virG, virC, virD, virE, and virF transcriptional units (Brencic and Winans, 2005). Vir genes code for a set of proteins with different functions such as T-DNA excision and processing (virC and virD), coating and protecting T-DNA during transfer (virE), formation of the type IV secretion system (T4SS) responsible for the delivery of T-DNA to plant cells (virB operon), and T-DNA integration into plant nucleus (virE2 and virD4). A study by Cho and Winans (2005) revealed that each gene on the Ti plasmid was modestly induced by plant-derived phenolic signals, while the repABC operon, responsible for Ti plasmid replication/partitioning, was significantly induced by phenolic signals. This suggests that the copy number of the Ti plasmid is induced by plant-derived phenolics, which is confirmed by direct binding of phosphorylated VirG to a 12-bp vir box upstream of the repABC operon (Zhu et al., 2000; Pappas and Winans, 2003; Cho and Winans, 2005). Apparently an increase in Ti plasmid copy number enhances the dosage of vir genes responsible for T-DNA transfer. A proteomic study corroborated VirA/VirG dependent induction of vir genes by identifying 11 proteins that were significantly induced in response to acetosyringone, including proteins constituting the T4SS, the single strand binding protein VirE2 that is exported to the plant nucleus, and the trans-zeatin synthesizing protein Tzs (Lai et al., 2006). Moreover, responses to phenolic inducers may be modulated by detoxification of these compounds by VirH2. VirH2 was shown to play a role in the metabolism of several phenolic compounds including ferulic acid, another inducer of vir genes (Brencic et al., 2004).

Agrobacterium detects and responds to plant-derived sugars through a distinct signaling pathway involving VirA and a chromosomally encoded periplasmic protein, ChvE (Cangelosi et al., 1990). Expression of chvE is regulated by the LysR transcriptional regulator (TraR) galactose-binding protein regulator (GbpR) in the presence of sugars (Doty et al., 1993; Peng et al., 1998). ChvE mediates Agrobacterium chemotaxis in response to aldose monosaccharides such as galactose, glucose, arabinose, fucose, xylose, and sugar acids. Importantly, ChvE binds plant-derived sugars and subsequently interacts with the periplasmic domain of VirA to stimulate vir gene expression (Cangelosi et al., 1990; He et al., 2009; Hu et al., 2013). Mutations in the periplasmic domain of VirA present the same phenotype as a ChvE mutant with both mutants unable to infect specific plant hosts (Cangelosi et al., 1990; Chang and Winans, 1992; Banta et al., 1994; Peng et al., 1998; Gao and Lynn, 2005). Recent studies also suggest that the ability of ChvE to recognize and bind different plant-derived sugars is vital in determining the host range of Agrobacterium (Hu et al., 2013). Interestingly, the sugar response in Agrobacterium has been found to be linked with the acidity responses since the absence of sugars or mutations in chvE disrupted acidic signaling. In addition, the affinity of ChvE for sugar acids increases with a decrease in pH (Hu et al., 2013), which reinforces an important role for acidity in modulating Agrobacterium virulence. It has been proposed that acidic conditions, together with the presence of sugars and a functional ChvE, promotes VirA–ChvE interactions required for efficient vir gene induction (Shimoda et al., 1993; Toyoda-Yamamoto et al., 2000; Gao and Lynn, 2005; Nair et al., 2011). However, mutations in chvE that abolish sugar sensing do not abolish vir gene induction by acetosyringone, although ChvE is known to interact with the periplasmic domain of VirA. This suggests ChvE and associated sugar perception play additive roles that further promote vir gene expression in response to sugars and phenolic compounds, while phenolics are essential vir gene inducing signals (Cangelosi et al., 1990; He et al., 2009; Hu et al., 2013). Apart from its signaling role, ChvE also has a role in sugar utilization as it delivers sugars to the ABC transporter MmsAB (Hu et al., 2013).

T-DNA transfer and integration into the plant nucleus is mediated by a complex set of Agrobacterium and host proteins. As discussed in previous sections, Agrobacterium recognizes three main plant-derived signals (acidity, phenolics, and sugars) and activates vir genes. VirD1, a helicase, and VirD2, a site specific endonuclease, are essential for nicking the Ti plasmid and the release of T-DNA as a single stranded DNA (referred to as T-strand; Yanofsky et al., 1986; Wang et al., 1990). VirD4, the coupling protein, and VirB1–VirB11, the mating-pore-formation components, together constitute the trans-envelope channel and pilus of Agrobacterium T4SS apparatus. In depth studies have assigned functional roles to each protein of the T4SS complex; VirD4, VirB3, VirB4, and VirB11 constitute the ATP-dependent translocation machinery, VirB6–VirB10 form the channel and VirB1, VirB2, VirB5, and VirB7 form the pilus (Cascales and Christie, 2003). The T-strand is covalently attached by VirD2, which is subsequently bound by VirD4 and VirB11 forming the T-complex. Current findings suggest that such DNA binding by associated virulence proteins (VirD4 and VirB11) stimulates ATP hydrolysis to produce a structural transition in the membrane channel protein VirB10. This allows passage of the T-complex to the cell surface where it can be directed to the T4SS pili, followed by delivery into the plant cell by the T4SS apparatus (Cascales and Christie, 2003; Cascales et al., 2013). Notably, many Gram-negative plant and animal pathogenic bacteria employ a type III secretion system (T3SS) to inject effector proteins directly into the cytosol of eukaryotic cells and thus allow the manipulation of host cellular activities to the benefit of the pathogen (Buttner and He, 2009). However, no T4SS organelles in Agrobacterium reminiscent of the basal body of flagella or needle complexes of the T3SS were evident (Christie, 2004). The exact process is still unknown regarding how the T-DNA complex is delivered by T4SS into plant cells, especially how the T-DNA complex passes through cell wall and plasma membrane, subsequently moving through the cytoplasm to the plant cell nucleus (Cascales and Christie, 2003; Gelvin, 2003).

T-DNA integration into plant nuclei is thought to occur by hijacking various host systems including defense signaling, cytoskeletal networking, molecular motors, nuclear import, proteolytic degradation, chromatin targeting, and DNA repair to ensure successful plant transformation (for review see Citovsky et al., 2007). In the plant cytoplasm, the T-strand/VirD2 complex is coated along its entire length by the VirE2 ssDNA-binding protein that is transported into the plant cell independently of the T-strand complex (Vergunst et al., 2000; Citovsky et al., 2007). Both VirD2 and VirE2 carry plant nuclear localization signals and together with host protein VIP1 (VirE2 interacting protein 1), facilitate T-complex import into the plant cell for host chromatin targeting (Citovsky et al., 1992; Tzfira et al., 2001; Li et al., 2005; Djamei et al., 2007; Lacroix et al., 2008). T-DNA is thought to attach to chromatin by interacting with nucleosomal proteins and is released from the T-complex by proteolytic removal of associated proteins (Magori and Citovsky, 2011). VirF, a bacterial F-box protein, also targets both VIP1 and VirE2 for proteasome dependent degradation. The mechanism of T-DNA integration into the plant genome is thought to occur by illegitimate recombination; however, the details of many of the molecular events within the plant cell and nucleus are still unclear.

Besides IAA and CK, infected plant cells produce over 20 different kinds of opines that can be classified into four families: octopine, nopaline, mannopine, and agrocinopine families (Beck von Bodman et al., 1992; Fuqua and Winans, 1996b; Piper et al., 1999). In fact, the most intensively studied Ti plasmids are the octopine and nopaline types, named after the predominant opines synthesized by transformed plant cells. Octopine is synthesized by the T-DNA-encoded enzyme octopine synthase (Ocs), which condenses pyruvate with different amino acids to produce octopine, lysopine, histopine, or octopinic acid (Dessaux et al., 1998). Nopaline is generated by nopaline synthase (Nos) in a similar condensation reaction involving αα-ketoglutaric acid and either arginine or ornithine. Opines of the mannopine and agrocinopine families are structurally more heterogeneous, which contain sugar and phosphate groups in the case of agrocinopine. Since plants cannot metabolize opines, transformed plant cells accumulate and release opines into the rhizosphere. The precise mechanism by which opines are exuded from plant cells is unknown, although the exudation of octopine and nopaline appears to depend upon the product of T-DNA gene 6a. Nevertheless, opines are present on the plant (or tumor) surface and are part of the soluble plant exudates released into the phylloplane and rhizoplane (Savka and Farrand, 1992).

Agrobacterium Ti plasmids also contain genes for opine uptake and catabolism that are located in the non-transferrable region, e.g., occ and noc regions for octopine- and nopaline-type Ti plasmids. In addition, Ti plasmids contain chemotaxic genes for their corresponding opines (Beck von Bodman et al., 1992; Kim and Farrand, 1997). Agrobacterium LysR-type transcriptional activator OccR (octopine catabolic regulator) and NocR (nopaline catabolic regulator) recognize and bind to opines, subsequently activating the expression of opine catabolic genes (Beck von Bodman et al., 1992; Wang et al., 1992). Agrobacterium metabolism of agrocinopine is much more complicated. When agrocinopines are present, the repressor agrocinopine catabolic regulator (AccR) dissociates from the promoter, allowing for expression of the acc operon responsible for agrocinopine metabolism. In addition, the acc operon is activated in response to phosphate limitation (Kim et al., 2008). Some of opine catabolic genes are also under regulation of other factors, for example the presence of certain substrates such as succinate (Hong et al., 1993). Although the rhizosphere contains species other than Agrobacterium that are capable of utilizing opines, they comprise of a very small minority of the bacterial population (Nautiyal and Dion, 1990). Therefore, the ability to use opines as a carbon, nitrogen, and energy source provides distinct advantages to Agrobacterium in the rhizosphere niche.

In addition to serving as a nutrition source for Agrobacterium, opines produced by transformed plant cells also activate Agrobacterium QS. In fact, the original study of Agrobacterium QS was relevant to Ti plasmid conjugation. In soil or cultivation at temperatures greater than 30^∘C, the Ti plasmid is rapidly lost from Agrobacterium populations. Once infected by Agrobacterium, plant cells produce opines. In addition to activating genes for opine metabolism, the NocR- or OccR-opine complex also activates a LuxR-type TraR located on the Ti plasmid (Li and Farrand, 2000). When the diffusible QS signal N-(3-oxooctanoyl)- DL-homoserine lactone (3OC8-HSL) reaches a threshold level with high population density, TraR binds to 3OC8-HSL. The TraR–3OC8-HSL complex activates traI, a LuxI-type 3OC8-HSL synthase, and tra/trb genes coding for a second T4SS responsible for conjugal transfer of Ti plasmids (Piper et al., 1993; Zhang et al., 1993; Fuqua and Winans, 1994; Hwang et al., 1994). Since the Ti plasmid carries genes responsible for plant infection and opine metabolism, avirulent Agrobacterium lacking the Ti plasmid becomes infectious and capable of opine metabolism by acquiring the Ti plasmid through conjugation. Additionally, the TraR–3OC8-HSL complex activates the repABC operon thereby enhancing the replication and copy number of the Ti plasmid (Fuqua and Winans, 1996a; White and Winans, 2007). TraR–3OC8-HSL complex also activates the transcription of TraM, a TraR antiactivator in both octopine- and nopaline-type strains of Agrobacterium. TraM further modulates QS and Ti plasmid conjugation in the rhizosphere (Hwang et al., 1999). Therefore, the initial infection and T-DNA transfer leads to the synthesis of opines in plant cells. Opines activate the Agrobacterium TraR/TraI QS system, which activates Ti plasmid conjugation and enhances Ti plasmid copy number (up to eightfold). This typical positive feedback regulation is advantageous for maximal infection of plant hosts and opine metabolism (Zhu and Winans, 1999, 2001; Pappas and Winans, 2003; Cho and Winans, 2005; Pinto et al., 2012).

Agrobacterium QS is well regulated not only for QS signal production, but also for QS signal degradation, also known as quorum quenching. γ-amino butyric acid (GABA) significantly increases in wounded plant tissues and acidic conditions. GABA also accumulates in plants infected by Agrobacterium (Chevrot et al., 2006). In addition, proline significantly accumulates in plant tumors but neither in wounded nor healthy tissues (Deeken et al., 2006). The Agrobacterium proline/GABA receptor atu2422 and ABC-transporter braE (atu2427) are required for GABA and proline uptake. GABA activates transcription of the attKLM operon located on the second plasmid of Agrobacterium. AttK is a NAD dependent dehydrogenase. AttL is a alcohol dehydrogenase and AttM, a γ-butyrolactonase, breaks down the Agrobacterium QS signal 3OC8-HSL. Proline is a competitive antagonist of GABA and is also taken up through the Atu2422-Bra ABC transporter system (Wachter et al., 2003; Haudecoeur et al., 2009). It was found that plants with relatively higher proline levels present bigger tumors and severe disease symptoms, whereas those with relatively high GABA attenuated Agrobacterium pathogenesis. This is likely a result of the pathogen’s enhanced virulence through QS that is negatively regulated by GABA (Brugiere et al., 1999). Furthermore, it was found that a short interfering RNA, AbcR1, targets the ribosome binding site of atu2422 and negatively affects its translation (Wilms et al., 2011, 2012).

Recent studies revealed that the plant defense signal salicylic acid (SA) also activates the attKLM operon thereby down-regulating Agrobacterium QS (Yuan et al., 2007, 2008a). It was suggested that down-regulation of QS during the initial stages of infection benefits Agrobacterium pathogenicity, since high levels of QS signals are known to trigger a defense response in eukaryotic hosts (Ritchie et al., 2005; Wagner et al., 2007). Therefore, Agrobacterium QS is under tight and complex modulation by plant-derived opine, SA, and GABA to ensure optimum infection of plant hosts and to avoid the elicitation of plant defense responses by high levels of QS signals, reflecting an evolutionary advantage. In addition, quorum quenching induced by SA and GABA might function to prevent unnecessary energy expenditure after T-DNA transfer. Moreover, since the AttM lactonase has a broad substrate range, the activation of Agrobacterium quorum quenching by GABA and SA likely confers Agrobacterium a competitive advantage by degrading QS signals from unrelated competitive bacteria occupying the rhizosphere niche (Mathesius et al., 2003; Carlier et al., 2004; Chevrot et al., 2006; Yuan et al., 2007). Furthermore, induction of attKLM genes allows Agrobacterium to metabolize other plant-released compounds such as gamma-butyrolactone to produce succinic acid for the central metabolism (tricarboxylic acid cycle; Carlier et al., 2004; Chevrot et al., 2006; Chai et al., 2007).

Plant hormones play important roles in plant defense and stress resistance. IAA and ethylene (ET) levels in plant tissues are elevated at the initial stages of infection by Agrobacterium. Following T-DNA integration, SA, IAA, and ET levels are elevated (Lee et al., 2009), while jasmonic acid (JA) levels were unchanged. However, in tumors, IAA and ET signaling pathways were activated, while JA and SA signaling pathways remained inactivated. Synthesis of IAA in crown gall occurs as a two-step process from tryptophan via indoleacetamide, mediated by-products of the T-DNA encoded iaaM and iaaH genes (Thomashow et al., 1986). T-DNA also carries an ipt gene responsible for CK synthesis. The ipt product condenses isopentenyl pyrophosphate and AMP to produce isopentenyl-AMP, which is later converted to CK by host enzymes. The elevated level of IAA and CK promote plant cell growth and tumor formation. It is now becoming evident that key phytohormones significantly influence Agrobacterium pathogenicity and tumor formation through both plant signaling pathways as well as direct modulation of bacterial processes (Veselov et al., 2003; Yuan et al., 2007; Zottini et al., 2007; Anand et al., 2008). The following sections are focussed on the effects of plant hormones on Agrobacterium pathogenicity, in particular, how Agrobacterium responds to these plant hormones.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.