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Plant-Microbe Interactions, 2008:169-197 ISBN: 978-81-308-0212-1 Editors: E. Ait Barka and C. Clément

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Infection and plant defense responses during plantbacterial interaction

Roberto Buonaurio Dipartimento di Scienze Agrarie e Ambientali, Università degli Studi di Perugia Via Borgo XX Giugno, 74, 06121 Perugia, Italy

Abstract

To exploit plant nutrients, phytopathogenic bacteria have evolved sophisticated infection strategies. A number of biotrophic Gram-negative bacteria are able to cause diseases in plants through a type III secretion system, composed of a protruding surface appendage, known as the hrp pilus, through which the bacterium injects effector proteins into the host cells to manipulate plant cells, in particular to suppress plant defenses. A unique infection strategy in plant-bacterial interactions is adopted by Agrobacterium tumefaciens, which genetically transforms its host by transferring T-DNA from its tumor-inducing plasmid to the chromosome of a plant cell. This transfer is mediated by the pilus T,

Correspondence/Reprint request: Dr. Roberto Buonaurio, Dipartimento di Scienze Agrarie e Ambientali, Università degli Studi di Perugia, Via Borgo XX Giugno, 74, 06121 Perugia, Italy. E-mail: [email protected]

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belonging to the type IV secretion system. Other important virulence factors of phytopathogenic bacteria are phytotoxins, extracellular polysaccharides, phytohormones and plant cell-wall-degrading enzymes. These latter factors are fundamental for the pathogenesis of necrotrophic bacteria. Plants defend themselves from bacterial attacks through a multilayered system of passive and active defense mechanisms, which can interfere with entry of bacteria into the plant tissue and restrict bacterial growth when the ingress has been gained. A number of hypotheses have been advanced to explain the restriction of the bacterial growth observed during the hypersensitive reaction and systemic acquired resistance development.

1. Introduction

Among the about 7100 classified bacterial species, roughly 150 species cause diseases to plants obtaining nutrients from these plants for their own growth by more or less specialized mechanisms. Although found in all parts of the world, bacterial diseases are most frequent and severe in tropical and subtropical countries, where warm and humid conditions are ideal for bacterial growth. Indeed, consistent annual crop yield losses are recorded in these countries. Bacterial diseases are essentially characterized by symptoms of leaf and fruit spots, cankers, blights, vascular wilts, rots and tumors. They are most often caused by Gram-negative bacteria belonging to the Proteobacteria phylum, including Xanthomonadaceae, Pseudomonadaceae and Enterobacteriaceae families. Except for a few rare cases, phytopathogenic bacteria provoke diseases in plants by penetrating into host tissues. Penetration occurs through natural openings, such as stomata, hydathodes, lenticels, nectarthodes, stigma etc., or through wounds. Bacteria colonize the apoplast, that is the intercellular spaces or xylem vessels, causing parenchymatous and vascular or parenchymatousvascular diseases, respectively. Besides the endophytic habitat, some bacterial species also have the capacity to survive as epiphytes on plant surfaces (phylloplane, rhizoplane, carpoplane, etc.). From an epidemiological point of view, this poses a particular danger because they are quick to infect plants in favourable conditions. Once inside plant tissues, bacteria may implement two main attack strategies to exploit the host plant nutrients: biotrophy, in which the plant cells are kept alive as long as possible and bacteria extract nutrients from live cells, and necrotrophy, in which bacteria kill plant cells and extract nutrients from dead cells. Interactions of bacteria with plants can be either incompatible or compatible. Incompatible interactions occur when the bacterium encounters a non-host plant (non-host resistance) or a resistant host plant (cultivar-specific resistance) and they are frequently associated with a hypersensitive response (HR), i.e. a rapid, programmed death of plant cells that

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occurs at the site of infection. Compatible interactions occur when the bacterium infects susceptible host plants causing disease symptoms. In this chapter, I examine the pathogenicity and virulence factors used by biotrophic and necrotrophic phytopathogenic bacteria (mainly Gram-negative) causing disease in plants and the ascertained and hypothetical defence mechanisms by which plants directly counteract these attacks.

2. Bacterial pathogenicity and virulence

To avoid any confusion in terminology, it is important to define the terms pathogenicity and virulence, which are often erroneously considered synonyms. According to Shurtleff and Averre [114], pathogenicity is, `the ability of a pathogen to cause disease', while, `virulence is the degree or measure of pathogenicity of a given pathogen'. Therefore, a bacterium could be pathogenic yet have varying degrees of virulence. Pathogenicity and/or virulence of Gram-negative plant pathogenic bacteria is strictly dependent on the presence of secretion apparatuses in their cells, through which they secrete proteins or nucleoproteins involved in their virulence in the apoplast or inject in the host cell. To date, five secretion systems, numbered from I to V have been described in both animal and plant Gram-negative pathogenic bacteria [46]. In addition, it is now emerging that the expression of virulence factors is under the control of quorum sensing, a communication mechanism by which bacteria regulate the expression of certain genes in response to their population density. I recommend the following excellent reviews for more detailed information on secretion systems [67, 106] and quorum sensing [42, 135] in relation to bacterial pathogenicity and virulence.

3. Pathogenicity and type III secretion system

The pathogenicity of a number of biotrophic Gram-negative bacteria in the genera Pseudomonas, Xanthomonas, Ralstonia, Erwinia and Pantoea is mainly due to their ability to produce a type III secretion system (T3SS), also called injectisome [46], by which the bacterium injects proteins involved in its virulence into plant cells (T3SS effectors). It is worth remembering that if the effector leads to the development of disease symptoms in the plant it is called a virulence protein, while if it triggers a defense reaction that leads to the HR, it is referred to as an avirulence protein. The T3SS is encoded by hrp (HR and pathogenicity) and hrc (HR and conserved) genes, whose mutations eliminate bacterial pathogenicity in susceptible host plants and the ability to elicit HR in non-host or cultivar-specific resistant plants. The hrc genes are so called as they encode proteins homologous to the T3SS described in Gram-negative bacterial

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pathogens of mammals in the genera Yersinia, Shigella and Salmonella, which are thought to be the core components of this secretion apparatus. The hrp/hrc genes, extensively characterized in Pseudomonas syringae, Erwinia amylovora, Ralstonia solanacearum and Xanthomonas campestris, are located in a large cluster (about 25 kb) in the chromosome, or in a megaplasmid in R. solanacearum, comprising more than 20 genes, and are organized in operons. Based on sequence similarity, operon structure and regulatory system, this gene cluster can be classified into two groups. P. syringae and E. amylovora are in the group I, while R. solanacearum and X. campestris in the group II [4]. A key difference in the regulation is that group I hrp/hrc operons are activated by HrpL, a member of the ECF (extracytoplasmic function) subfamily of sigma factors, while most group II hrp/hrc operons are activated by a member of the AraC family, which is designated HrpB in R. solanacearum and HrpX in X. campestris [4]. The injectisome is composed of two parts, an envelope-embedded multiring base and a long protruding surface appendage, called the hrp pilus, 2 µm or longer, with an outer diameter 6-10 nm and an inner one probably up to 2 nm [76]. Hrp pili, described for P. syringae [110], R. solanacearum [133], Erwinia amylovora [69] and X. campestris pv. vesicatoria [137], elongate distally with the addition of their major component, Hrp pilin subunits, likewise T3SS effectors are secreted from the pilus tip [68, 82]. This indicates that Hrp pili serve as conduits through which substrates are transported [68, 82]. Considering the dimensions of the pilus, one has to assume that the effector proteins, which are up to 200 kDa in size, move within the channel in an at least partially unfolded state [70]. Many of the T3SS effector proteins have been shown to be dependent on chaperones, which keep the effector in a partially unfolded form in the bacterial cytoplasm [123]. Although the pilus proteins, HrpA (P. syringae and E. amylovora), HrpY (R. solanacearum) and HprE (X. campestris pv. vesicatoria) do not share any significant sequence homology, they have a number of physicochemical features in common [136]. They are small (8.7-11.3 kDa), predicted to consist almost exclusively of helices, show very similar hydrophobicity profiles and resemble each other in their instability and aliphatic indices [76, 136, 137]. As growth occurs at the tip, it has been hypothesized that pilus assembly occurs inside the plant cell wall rather than the structure being driven into the wall by basal extension [82]. There is no conclusive evidence on the fate of the pilus when it reaches the plant cell plasma membrane. It is possible that either the emerging pilin monomers are dispersed within the lipid membrane or the pilus may puncture the membrane, as suggested in Yersinia [61]. In mammalian bacterial pathogens, the translocation of T3SS effectors into host cells requires T3SSsecreted accessory proteins called translocons, which forms pores in the host

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plasma membrane [30, 31, 40]. Although little is known about T3SS translocons in phytopathogenic bacteria, recent evidence suggests that HrpF in X. campestris pv. vesicatoria [32, 111] and HopB1 and HrpK in P. syringae pv. tomato have this function [101]. Specific genes of the hrp/hrc cluster also encode harpins, which are proteins delivered into the intercellular space and accumulated along the length of the growing pilus [69, 82]. HrpN and HrpW of E. amylovora, HrpZ and HrpW of P. syringae and PopA of R. solanacearum are harpins that have been extensively studied [9, 34, 59, 74, 138]. They are heat stable, glycine-rich and cysteine-lacking and, except for PopA, have a non-specific HR elicitor activity when infiltrated at relatively high concentrations into the leaf intercellular space of tobacco and several other plants [5]. PopA elicits the HR selectively on those plants in which R. solanacearum also elicits the HR [9]. Although little is known of the role of these proteins in the pathogenesis process, many of their properties point to an interaction with the plant cell wall and plasma membrane, which suggests that they are helpers in effector delivery. HrpW of E. amylovora and P. syringae and the harpin HopPmaHPto, recently revealed by the analysis of the complete genome sequence of P. syringae pv. tomato DC3000 [27], have an apparently bifunctional, two-domain structure [5]. The N-terminal domain is particularly glycine-rich, whereas the C-terminal one shows a similarity to pathogen pectate lyases [34, 74]. Both proteins show heat-stable HR elicitor activity when infiltrated into tobacco plants [5]. The similarities of HrpW and HopPmaHPto with pectic enzymes, and the observed ability of HrpW to bind specifically to pectate [34], suggest they play a role in assisting pilus penetration through the cell wall matrix [5]. The hypothesis that harpins are helpers in effector delivery is also suggested by their interaction with plasma membrane. Indeed, HrpZ is able to insert in lipid bilayers and to form ion-conducting pores [80]. Since this harpin forms multimers, up to octamers, in solution [35], it may function as a membrane-associated complex able to translocate effectors across the plasma membrane. A recent study of Li et al. [83] reported that HrpZ of Pseudomonas savastanoi pv. phaseolicola (HrpZPph) interacts with proteins, since it has a central domain that harbors a peptide binding site, which is distinct from the domain presumed to act as an HR elicitor [80]. The possible interaction of HrpZPph with a host plant protein suggests its involvement in bacterial pathogenesis. Hrp/hrc genes can be located within pathogenic islands (PAIs), which are defined as chromosomal loci harbouring more than one virulence gene and having an altered G+C content from the rest of the bacterial genome (an indicator of acquisition via horizontal gene transfer from a different host organism). They are flanked by specific DNA sequences, such as direct repeats, and carry genes coding for genetic mobility such as phage genes, insertion sequence elements, integrases, transposases and origins of replication

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[10]. The P. syringae Hrp PAI, the first characterized, has for example a tripartite mosaic structure, where the hrp/hrc gene cluster is flanked by a unique exchangeable effector locus (EEL), and a conserved effector locus (CEL) [3]. EEL is a distinct unit of varying size (2.5­7.3 kb) that contains completely different candidate effector genes in the different strains, and is located 3 nt after the hrpK stop codon. It is rich in transposable elements and plasmid-related sequences, and its open reading frames have a G+C content lower than those of the average whole genome of P. syringae pv. tomato, which suggests its acquiring by horizontal gene transfer [10]. CEL, which carries several candidate effector genes, showed a high level of gene synteny, with a normal G+C ratio and an absence of sequences related to mobile genetic elements. Deletion of the EEL from P. syringae pv. tomato DC3000 slightly reduce its virulence, while deletion of the CEL abolished its pathogenicity [10]. Therefore, it seems that CEL is likely to be an important and stable region, possibly conserved among many plant pathogenic pseudomonads, while EEL may represent a host-specific locus. Other well characterized Hrp PAIs are those of Xanthomonas axonopodis pv. glycines [75] and E. amylovora [100]. It is noteworthy that the hrp/hrc cluster of R. solanacearum does not seem to be a PAI and that its effector genes are distributed randomly on both the plasmid and chromosome [10]. The study of the molecular mechanisms underlying T3SS effector functions is attracting the attention of many researchers. However, this goal is difficult to reach as phytopathogenic bacteria possess a large arsenal of effectors, which presumably interfere in a collective manner with host cellular pathways, to the benefit of the pathogen, and mutations of individual effectors often does not significantly affect bacterial pathogenicity [31]. The emergent results on their role in pathogenesis have indicated that they act as molecular double agents betraying the pathogen to plant defenses in some interactions and suppressing host defenses in others. For some effectors, enzymatic functions such as cysteine protease or phosphatase activities were demonstrated. In addition, suppression of programmed cell death, of plant cellwall remodelling and of resistance proteins, activation of the jasmonate pathway and of plant transcription are functions described for some effector proteins [97]. Further information on this subject has been reported in several excellent recent reviews [5, 56, 70, 97].

4. Agrobacterium tumefaciens infection process

The particular infection modality of Agrobacterium tumefaciens, the causal agent of crown gall in many woody and herbaceous dicotyledonous plants, is worthy of separate discussion. This Gram-negative soil bacterium is able to genetically transform healthy host cells in tumoral cells by inserting a part of its DNA (transferred DNA; T-DNA), contained on the tumor-inducing

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(Ti) plasmid, into the plant genome [116]. T-DNA carries genes involved in the synthesis of plant growth hormones (auxins and cytokinins) and synthesis and secretion of amino compounds called opines, tumor-specific compounds exclusively assimilated by the pathogen as major carbon and nitrogen sources. The actively growing tumoral cells for the high plant growth hormone levels and the opine they produce render the tumor a favourable biological niche for A. tumefaciens growth. At least 3 genetic components are required for tumorigenesis: i) T-DNA; ii) the virulence (vir) region located on the Ti plasmid, which genes respond to specific plant-released signals, to generate a copy of the T-DNA and mediate its transfer into the host cell; iii) a suite of chromosomal virulence (chv) genes, involved in bacterial chemotaxis toward-and attachment to the wounded plant cell wall [116]. In natural infections, A. tumefaciens cells present in the soil, reach wounds (the main infection sites) of roots and the subterranean part of the stem by the means of flagella, attracted by the compounds (e.g., sugars) released from plant wounds. The importance of motility in the infection process is illustrated by the fact that mutations in genes encoding flagellin abolish motility and reduce tumorigenesis [36, 58]. Binding of agrobacteria to plant surfaces, an essential stage for establishing a long-term interaction with the host, is dependent on several plant factors and takes place in two steps [91]. The first, rather weak and reversible, may involve a variety of bacterial polysaccharides (e.g. cyclic glucans synthesized by chvA and chvB), which bind host polysaccharides [25]. Mutations in the chv genes reduced the binding of the agrobacteria to cultured plant cells and abolished tumorigenesis [25]. The second binding step requires the synthesis of bacterial cellulose, which causes a tight, irreversible binding and formation of bacterial aggregates on the host surface [90]. The expression of vir genes, another crucial event for tumorigenesis, is stimulated by plant-released signals, which include specific phenolic compounds and monosaccharides in combination with acidic pH (5.2 to 5.7) and temperatures below 30°C [25]. Acetosyringone and its derivatives are specific phenolics [93, 122], whose action is greatly enhanced by galacturonic and glucuronic acid and, to a lesser extent, by other specific monosaccharides [8]. All these vir-inducing conditions mainly occur during wounding, an event that is generally thought to be required for tumorigenesis [72], albeit they have been recorded in unwounded tobacco plants [48]. At wound sites, phenolics accumulate as precursors of lignin biosynthesis during the wound healing process, monosaccharides originate from mechanical and enzymatic degradation of plant cell wall polysaccharides, the pH level tends to be acidic given the presence of acidic compounds in the wound sap [25].

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Conditions inducing vir genes are perceived by the VirA-VirG twocomponent system and the ChvE sugar binding protein. After detecting plantreleased phenolics, monosaccharides, and acidity, VirA, a transmembrane histidine kinase, phosphorylates VirG, the DNA binding response regulator. Moreover, monosaccharides seem to be indirectly detected by VirA through ChvE, a periplasmic sugar binding protein required for chemotaxis toward and uptake of monosaccharides that directly interacts with the VirA periplasmic domain [25]. Phosphorylated VirG binds to the vir box, a conserved sequence in the promoter regions of vir genes, activating the transcription of these genes [116]. The successive cellular process involved in A. tumefaciens tumorigenesis is the cleavage of T-DNA from the Ti plasmid by the action of VirD1 and VirD2 [116]. These two proteins act together as site-specific nucleases, which cut the left and right borders of the bottom strand of the T-DNA (25 base pair direct repeats defining T-DNA), and release a single-stranded (ss) T-DNA molecule (T-strand). In addition, the VirD2 molecule covalently attaches to the 5' end of the T-strand, forming the immature T-complex, which, along with several other Vir proteins, is exported into the host cell by a VirB/D4 type IV secretion system, which is encoded by the virB operon and the virD4 gene [39, 84]. The virB gene products, termed the mating pair formation (Mpf) proteins, elaborate a cell envelope-spanning structure required for substrate transfer, as well as an extracellular appendage termed the T pilus that mediates attachment to recipient cells [39]. VirD4 is a coupling protein, which is not involved in TDNA processing or biogenesis of the T pilus but instead acts together with the Mpf structure to deliver substrates across the cell envelope [38, 78]. Once inside the host-cell cytoplasm, the T-DNA is thought to exist as a mature T-complex (T-complex), in which the entire length of the T-strand molecule is coated with numerous VirE2 molecules, which confer to the TDNA the structure and protection needed for its journey to the host-cell nucleus [129]. There is evidence that the T-complex, like many DNA viruses, uses the plant cytoskeleton as a track for its subcellular movement toward the nucleus [129]. Since the T-complex is large in size (about 15.7 nm outer diameter), an active mechanism for its nuclear import is most likely involved, probably mediated by the plant nuclear-import machinery. In fact, VirD2 and VirE2 were found to interact with host proteins for their nuclear import in host cells. VirD2 interacts with AtKAP, a member of the Arabidopsis karyopherin family, which mediates its nuclear import in permeabilized yeast cells, while VirE2 interacts with the plant VirE2-interacting protein 1 (VIP1) and the bacterial VirE3 protein, both of which act as molecular adaptors between VirE2 and the host-cell karyopherin [129].

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Once inside the nucleus, the T-complex needs to travel to its integration point and be uncovered from its escorting proteins before integration into the host genome. VIP1 interacts with the H2A histone, a plant chromatin protein essential for T-DNA integration, suggesting it is involved in targeting the Tcomplex to the site of integration [129]. Furthermore, there is evidence that the stripping of the T-complex is due to proteasomal degradation [129]. The molecular mechanism underlying T-DNA integration is still under debate. One hypothesis is that host DNA repair machinery, by converting the T-strand molecule to double-stranded (ds) T-DNA, may recognize these molecules as broken DNA fragments and incorporate them into the host genome [129].

5. Other bacterial virulence factors

The severity of disease symptoms caused by bacteria in plants is determined by the production of a number of virulence factors, including phytotoxins, plant cell-wall-degrading enzymes, extracellular polysaccharides and phytohormones. In general, phytopathogenic bacterial strains mutated in any virulence factor more or less reduce their virulence, while their pathogenicity remains unchanged.

5.1 Phytotoxins

Phytopathogenic bacteria of the Pseudomonas genus, especially Pseudomonas syringae, produce a wide spectrum of nonhost-specific phytotoxins, i.e. toxic compounds causing symptoms in many plants independently of the fact that they can or cannot be infected by the toxinproducing bacterium. On the basis of the symptoms they induce in plants, phytotoxins of Pseudomonas spp. have been grouped in necrosis-inducing and chlorosis-inducing phytotoxins. P. syringae pv. syringae, the causal agent of many diseases and types of symptoms in herbaceous and woody plants, produces necrosis-inducing phytotoxins, lipodepsipeptides, which based on their amino acid chain length are usually divided in two groups: mycins (e.g. syringomycins) and peptins (e.g. syringopeptins) [94]. Syringomycins and syringopeptins are synthesised by modular nonribosomal peptide synthases, whose chromosomal genes are present in the syr and syp clusters, respectively. These clusters are adjacent to one another inside the syr-syp genomic island [57]. Both phytotoxins induce necrosis in plant tissues and form pores in plant plasma membranes, thereby promoting transmembrane ion flux and cell death [17]. Since all strains of P. syringae pv. syringae analyzed produce both syringomycins and syringopeptins, interrelated roles for the toxins in the plant pathogen interaction have been suggested. The advantages of producing two phytotoxic cytotoxins during P. syringae pv. syringae pathogenesis are unclear. Studies

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carried out to determine their contribution to virulence, based on assays of mutants defective in the synthesis of one or both types of lipopeptide toxins, provided contrasting results in the function of the host used. Mutations in P. syringae pv. syringae of either the syrB1 (syringomycin synthetase) or the sypA (syringopeptin synthetase) genes provoked a reduction in virulence of the bacterium in immature cherry fruits, which was strongest in a syrB1-sypA double mutant [17]. By contrast, the virulence of a mutant for the syrB operon in P. syringae pv. syringae strain B728a did not change virulence on bean [17]. Chlorosis-inducing phytotoxins include coronatine, produced by P. syringae pvs. atropurpurea, glycinea, maculicola, morsprunorum and tomato, phaseolotoxin, produced by Pseudomonas savastanoi pv. phaseolicola and P. syringae pv. actinidiae, and tabtoxin produced by the pvs. tabaci, coronafaciens, and garcae of P. syringae [16]. Among these phytotoxins, my attention will be focused on coronatine (COR), while information on the other chlorosis-inducing phytotoxins can be found elsewhere in excellent reviews [16, 17]. COR structurally resembles a polyketide, and consists of two distinct moieties, coronafacic acid (CFA) and coronamic acid (CMA), which function as intermediates in the biosynthetic pathway to COR and are fused together by an amide bond [16]. The primary symptom observed in leaf tissue treated with COR is an intense spreading chlorosis that can be induced on a wide variety of plant species [139]. COR is also known to induce hypertrophy of storage tissue, compression of thylakoids, thickening of plant cell walls, accumulation of protease inhibitors, inhibition of root elongation, and stimulation of ethylene production in some but not all plant species [139]. Both CFA and CMA moieties of the COR molecule have been predicted to function as analogues of endogenous plant signalling molecules. The CFA moiety is structurally and functionally similar to several jasmonates, a family of endogenous plant growth regulators derived from the octadecanoid signalling pathway and involved in plant defense mechanisms [105]. Although the CMA moiety resembles aminocyclopropyl carboxylic acid (ACC), the immediate precursor to ethylene in plants [20], it does not function as an analogue of ACC [131]. Thus, the precise mechanism of COR function in altering host physiology and promoting pathogen virulence is unclear. COR biosynthesis genes are located in the COR gene cluster, which is generally harboured on a plasmid. This cluster contains two distinct regions that encode the structural genes for CMA and CFA biosynthesis, separated by a 3.4 kb regulatory region in the strain PG4180 of P. syringae pv. glycinea [2], and has several features of a genomic island [10]. It is noteworthy that COR production is thermoresponsive. Indeed, strain PG4180 of P. syringae pv. glycinea produces COR predominantly at 18°C, whilst at 28°C, the optimal growth temperature for the bacterium, production is undetectable [17]. Thermoregulation occurs at the level of transcription of the biosynthetic genes

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and is mediated by the products of three regulatory genes, corS, corR, and corP, which encode an unconventional two-component system consisting of a transmembrane histidine kinase, CorS, two response regulators, CorR and CorP [130], and an alternative sigma factor, RpoN (54) [1]. Since temperature markedly affects the fatty-acid composition of the membrane, the physical state of the membrane (fluidity) might trigger a conformational change in one or more transmembrane domains of CorS, causing the conserved H-box, a presumed site of phosphorylation to become sequestered by insertion into the cytoplasmic membrane [119]. COR production plays an important role in virulence of toxin-producing P. syringae strains. Studies with COR-defective mutants have shown that COR synthesis contributes significantly to lesion expansion, the development of chlorosis, and bacterial multiplication in infected leaves [18, 95, 126]. These findings were confirmed by Budde and Ullrich [26], who investigated the impact of COR production by P. syringae pv. glycinea PG4180 during infection of soybean plants. Interestingly, they observed a significant delay of the hypersensitive response (HR) on tobacco plants treated with a CFAoverproducing derivative of PG4180 indicating that COR/CFA plays also a role during incompatible plant-bacteria interactions. It has been recently reported that stomatal closure in Arabidopsis is part of a plant innate immune response, which prevents bacteria from entering the plant leaf, and that COR is able to suppress this defense mechanism by re-opening stomata [94].

5.2. Plant cell-wall degrading enzymes

Extracellular enzymes able to degrade plant cell walls are essential virulence factors for necrotrophic soft rot bacteria, such as the soft rot erwiniae, now belonging to the Pectobacterium genus (e.g. Pectobacterium carotovorum subsp. carotovorum, Pectobacterium atrosepticum, Pectobacterium chrysanthemi). A combination of extracellular enzymes: pectate lyases, pectin methylesterases, pectin lyases, polygalacturonases, cellulase, and proteases are involved in the depolymerization process of plant cell walls provoked by these bacteria [128]. Proteases are secreted by the type I secretion system (T1SS), whereas the rest of the above mentioned enzymes by the type II secretion system (T2SS) [67, 106]. Among these enzymes, pectate lyases (Pels) are mainly involved in the virulence of soft rot Pectobacterium species [128]. P. chrysanthemi has five major Pel isoenzymes, encoded by the pelA, pelB, pelC, pelD, and pelE genes, which are organized in two clusters, pelADE and pelBC [65]. Mutations in individual major pel genes does not bring about any significant changes in P. chrysanthemi virulence [14, 109]. In addition, a deletion of all major pel genes fails to eliminate tissue maceration activity, and shows a set of secondary Pel isoenzymes (e.g. pelL, pelZ, and

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pelI), whose activities are only expressed in plants and appear to have an important role in both infection and host specificity [14, 85, 103, 109, 117]. The expression of pectinase genes is induced by the breakdown products of pectin and pectate, particularly 2-keto-3-deoxygluconate (KDG), 5-keto-4deoxyuronate (DKI), and 2,5-diketo-3-deoxygluconate (DKII), and it is repressed by three independent repressors, KdgR, PecS and PecT [25, 128]. KdgR binds to a conserved binding site in the operators of a number of different genes involved in pectinolysis. As the disease process begins and more breakdown intermediates are formed, they interact with KdgR, causing it to dissociate from its binding site and leading to induction/de-repression of the pathogenicity determinants [128]. Bauer et al. [13] demonstrated that hrp/hrc cluster is also present in the genome of P. chrysanthemi and that mutations in this cluster provoke a slight reduction in virulence in susceptible hosts. Later, Yang et al. [144], using a lower bacterial inoculum and a set of African violet varieties, found that the virulence of P. chrysanthemi hrpG and hrcC mutants was greatly reduced when the mutants were inoculated in semitolerant varieties. It is worth noting that the multiple pel- mutant (pelABCE-), deficient in exoenzyme action, elicits HR on tobacco and that this reaction does not appear in plants, inoculated with the hrpN/pelABCE- double mutant [128].

5.3. Extracellular polysaccharides

Extracellular polysaccharides (EPSs) may be associated with the bacterial cell as a capsule, be released as fluidal slime, or be present in both forms [45]. EPSs are important pathogenicity or virulence factors, particularly for bacteria with a vascular habitat. For example, the EPSs amylovoran and levan are pathogenicity and virulence factors, respectively, of Erwinia amylovora, the causal agent of fire blight on some Rosaceous plants [100]. Amylovoran is an acidic heteropolysaccharide composed of a pentasaccharide repeating unit of four differently linked galactose molecules and a glucuronic acid residue, which are decorated with pyruvate and acetate groups, while levan is a neutral homopolysaccharide composed of 2,6-linked fructose [66]. Amylovoran affects plants primarily by plugging the vascular tissue, thus inducing wilt of shoots, and is considered a pathogenicity factor as amylovoran-deficient mutants are not pathogenic [15]. The biosynthesis of amylovoran requires the ams operon, consisting of 12 genes, whose expression is controlled by the regulatory proteins RcsA and RcsB, able to bind the promoter region of the ams operon [100]. Levan is synthesized by levansucrase, encoded by the lsc gene, which mutation results in a slow symptom formation on shoots of host plants [51]. Ralstonia solanacearum, which causes wilting of several hundred plant species (e.g. potato, tomato, tobacco, peanut, and banana), is another phytopathogenic bacterium whose virulence mainly depends on EPS

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production. Among the EPSs it produces, EPS1, an acidic high molecular mass heteropolysaccharide, is the single most important virulence factor of the bacterium, since eps mutants are severely reduced in systemic colonization of tomato plants when inoculated via unwounded roots and do not cause typical wilt symptoms even when introduced directly into stem wounds [45]. Besides their involvement in wilting, EPSs might play further roles such as shield bacteria from toxic plant compounds, reduce contact with plant cells to minimize host defense responses, promote multiplication by prolonging watersoaking of tissues, or otherwise aid invasion or systemic colonization [45]. Yun et al. [145] have demonstrated that xanthan, the major exopolysaccharide secreted by Xanthomonas spp., plays an important role in X. campestris pv. campestris pathogenesis. They observed that a xanthan minus mutant and a mutant producing truncated xanthan fail to cause disease in both Nicotiana benthamiana and Arabidopsis plants. They also demonstrated that xanthan suppresses callose deposition in plant cell wall, a basal form of resistance to bacterial colonization.

5.4. Phytohormones

Production of the phytohormones auxins (e.g. indole-3-acetic acid-IAA) and cytokinins are important virulence factors for the gall-forming phytopathogenic bacteria, Pantoea agglomerans pv. gypsophilae, the causal agent of crown and root gall disease of Gypsophila paniculata, and the pvs. savastanoi and nerii of Pseudomonas savastanoi, which incite olive and oleander knot diseases, respectively. Starting from L-tryptophan, these bacteria synthesize IAA by the indole-3acetamide (IAM) route, mediated by tryptophan-2-monooxygenase and indole3-acetamide hydrolase, encoded by iaaM and iaaH genes, respectively [33, 87]. These genes are exclusively located on a plasmid in P. agglomerans pv. gypsophilae, while on a plasmid or in the chromosome in P. savastanoi. It is worth noting that in pathogenic and non-pathogenic strains of P. agglomerans, IAA synthesis also follows the indole-3-pyruvate route (IPyA route), which enzymes are encoded by chromosomal genes [24]. Biosynthesis of cytokinins in gall-forming phytopathogenic bacteria is similar to those occurring in higher plants, with isopentenyl transferase as key biosynthesis enzyme. Mutations of the IAM route and/or cytokinin biosynthesis genes provoked reductions in the virulence of P. agglomerans pv. gypsophilae and P. savastanoi [86, 125], while mutations in hrp/hrc cluster genes annulled their pathogenicity [12, 118]. It is worth noting that pathogenicity and virulence genes of P. agglomerans pv. gypsophilae are harboured in a putative PAI, contained on the plasmid pPATHPag [12, 86]. It seems that Pantoea agglomerans, widespread in nature as epyphite, has recently evolved into a

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pathogen by the acquisition of this PAI-containing plasmid via horizontal gene transfer [12]. The gaseous phytohormone ethylene, also produced by various microorganisms including plant pathogenic bacteria [141], can be considered a virulence factor for some of them. P. syringae pv. glycinea and P. savastanoi pv. phaseolicola are very efficient ethylene producers, generating it by using 2-oxoglutarate as the substrate and the ethylene-forming enzyme (EFE) [142]. Weingart et al. [140] demonstrated that when bean and soybean plants were inoculated with the ethylene-negative (efe) mutants of these bacterial species, only P. syringae pv. glycinea significantly reduced its virulence. This virulence attenuation, particularly evident in the efe mutant unable to produce the virulence factor coronatine, was characterized by weak symptoms and reduced bacterial growth in planta.

6. Plant defense responses against bacterial attacks

During their lifetime, plants are continually exposed to a vast number of potential phytopathogenic bacteria, against which they try to defend themselves through a multilayered system of passive and active defense mechanisms. When defense responses are effective in contrasting them, plants are considered resistant. Most plant species are resistant to most species of potential bacterial invaders, a phenomenon termed non-host or species resistance [99]. It is likely that during evolution, non-host resistance has been overcome by individual phytopathogenic strains of a given bacterial species through the acquisition of virulence factors, which enabled them to either evade or suppress plant defense mechanisms [99]. In such cases, plants that became hosts to such bacteria were rendered susceptible to their colonization and disease ensued (compatible interaction). Furthermore, within a single host plant, resistance to bacterial diseases can also occur at the level of individual cultivars and it is termed host resistance and in particular cultivar-specific resistance. As a result of coevolution between host plant and the host bacterium, individual plant genotypes have evolved resistance genes that specifically recognize bacterial strain or racespecific factors and allow the plant to resist to the infection of this particular race (race-specific resistance or cultivar-specific resistance) [99]. In general, cultivarspecific resistance conforms to the gene-for-gene hypothesis and is genetically determined by complementary pairs of bacterium-encoded avirulence (Avr) genes [22, 97] and plant resistance (R) genes [88]. Most Avr proteins are considered virulence factors required for the colonization of host plants, which act as specific elicitors of plant defense in resistant host cultivars as they trigger the plant surveillance system [99]. Non-host resistance of the type II [98] and cultivar-specific resistances to phytopathogenic bacteria, are typically associated with HR, which is characterized

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by the localised rapid death of host cells at the infection site and contributes to limit the growth and spread of the invading bacterium. However, there are some plant-bacterium interactions characterized by non-host resistance not involving the HR (type I non-host resistance) [98], which mainly rely on the so-called basal resistance or innate immunity [43, 71]. Similarly to the innate immunity in mammals, basal resistance is elicited in plants by pathogenassociated molecular patterns (PAMPs) or, more precisely, by microbialassociated molecular patterns (MAMPs), such as in the case of bacteria, lipopolysaccharide [47], flagellin [54], and cold shock protein [49]. Basal resistance is also induced outside of plant cells by non-pathogenic bacteria, TTSS mutants and heat-killed bacteria and manifests in the formation of a callose-rich papilla beneath the plant cell wall, localized production of reactive oxygen species and increased expression of phenylpropanoid pathway genes and of other defense associated genes [5, 71, 121]. Further details on basal resistance are discussed more fully by Ott and Bozsó (see Chapter 8).

6.1. Preformed defenses

Preformed defenses, both structural and chemical, can discourage entry of bacteria into the plant tissue and restrict their growth when the ingress has been gained [7]. Particular morphological features of plant natural openings may contribute to plant resistance during the bacterium entry stage of the infection process. McLean [92] demonstrated that the fully developed ridge of the stomata of some resistant Citrus spp. is responsible for the resistance to the citrus canker agent, Xanthomonas axonopodis pv. citri. This structural stomatal conformation does not permit the entrance of the bacterium inside plant tissues. Ramos et al. [107] showed that there is a relationship between frequency of stomata, stomatal size, some morphological leaf characteristics of tomato plants and resistance to bacterial leaf spot disease caused by Xanthomonas campestris pv. vesicatoria. By using scanning electron microscopy, they also hypothesized that other morphological features, such as the raised stomatal complex in Lycopersicon hirsutum and persistent hydrophobic waxy coating of the epidermis in Lycopersicon peruvianum are associated with resistance. Zinsou et al. [146] postulated that the number of adaxial leaf stomata together with leaf surface wax contribute to the resistance of cassava to Xanthomonas axonopodis pv. manihotis. Horino [64] reported that the openings of the hydathode water pores of Leersia japonica, which is resistant to Xanthomonas oryzae pv. oryzae, are narrower than those of the susceptible rice leaves. When phytopathogenic bacteria are inside host tissues, pre-existing structural and chemical plant defenses can restrict their spread and growth in planta. The movement in the vascular tissue of the xylem-inhabiting bacterium

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Clavibacter michiganensis subsp. insidiosus, the agent of bacteria wilt of alfalfa, is reduced in resistant alfalfa cultivars, as they have fewer vascular bundles, shorter vessel elements and a thicker cortex than susceptible cultivars [37]. The resistance of pear plants to Erwinia amylovora seems to be associated with a high level of arbutin-hydroquinone, the antibacterial compound present in the exterior parts of the blossoms, which is the most susceptible part of the plant to the bacterium [113]. This compound is released from the glucoside arbutin through the action of -glucosidase, which activity is particularly elevated in the exterior parts of the blossoms.

6.3. Induced defenses

Structural and biochemical defenses induced in planta by bacterial infection can contribute to disease resistance. The formation of tylose and gum occlusions in the xylem vessels of grapevines seems to be associated with resistance to the Pierce's disease, caused by Xylella fastidiosa [50]. However, further research is necessary to verify this assumption as contrasting results have recently been reported [77]. The most studied induced biochemical defences are those associated with the HR, which are responsible for restricting the bacteria and for blocking bacterial multiplication in planta. It is worth pointing out that establishing which defense responses occur during HR is particularly difficult, since it most likely involves a complex combination of responses, which may act additively or synergistically. Several lines of evidence suggest that death of host cells during the HR is not caused directly by toxic substances produced by the bacterium but rather results from the activation of suicide processes encoded by the plant. Indeed, HR is considered a form of programmed cell death, recalling certain aspects of mammalian apoptotic cell death [52, 60], such as the chromatin condensation at the nuclear periphery, reported in the cultivar-specific resistance of pepper plants to Xanthomonas campestris pv. vesicatoria [104]. However, it has been suggested that cell death during the HR induced by bacteria in Arabidopsis is programmed, but is a variant of necrosis rather than apoptosis [121]. The overproduction of reactive oxygen species, the so-called oxidative burst, is an early event characterizing the HR induced by bacteria, which, at least in part, may generate unfavourable conditions for bacterial multiplication in the apoplast [11]. This adverse environment for bacterial life could be due to the antimicrobial activity of hydrogen peroxide, which is strongly increased around bacterial cells, and to the oxidative cross-linking of the cell wall, driven by the rapid accumulation of hydrogen peroxide at the plant cell walls adjacent to attached bacteria [19, 121]. Pharmacological studies performed by the same authors support the hypothesis that the oxidative burst associated with

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bacterially induced HR is generated by the plasma membrane NADPH oxidase and apoplastic peroxidases. Besides hydrogen peroxide, other plant antibacterial molecules, such as for example C6-volatiles, wall-bound phenols and chitinase, could be responsible for the restriction of bacterial growth observed during the HR. Early increases in antimicrobial C6-volatiles derived by the lipoxygenase pathway were reported in bean and pepper plants undergoing the HR induced by avirulent strains of Pseudomonas savastanoi pv. phaseolicola and Xanthomonas campestris pv. vesicatoria, respectively [29, 41]. Soylu [120] demonstrated that cell-wall bound phenolic compounds accumulate in Arabidopsis thaliana undergoing the HR caused by phytopathogenic Pseudomonads and suggested that they may be involved in resistance. Phenolics have been proposed to modify cell-wall polysaccharides to resist the action of lytic enzymes [89]. It is known that chitinases have a bifunctional activity of both chitinase and lysozyme and therefore may hydrolyse bacterial cell walls [55]. Transcripts of an extracellular pepper class II basic chitinase, designated CAChi2, are highly expressed in pepper plants undergoing the HR in response to X. campestris pv. vesicatoria [63]. Since the overexpression of CAChi2 in transgenic Arabidopsis plants enhanced bacterial disease resistance against P. syringae pv. tomato infection [62], it is possible that this enzyme plays a similar role in the resistance of pepper plants to X. campestris pv. vesicatoria. Lignin accumulation [81, 108] and changes in apoplastic water potential [143] are additional possible post-infection resistance mechanisms to bacterial infection. Apoplastic water potential is known to be a critical factor for the growth of phytopathogenic bacteria in plant tissue. Interestingly, Wright and Beattie [143], using a water stress-responsive transcriptional fusion, noted a marked reduction in apoplastic water potential during the HR induced by an avirulent strain of Pseudomonas syringae pv. tomato in Arabidopsis thaliana. Since water potential values were low enough to prevent bacterial division, this can account for the restriction of bacterial growth during HR. Of interest is a recent study on an induced biochemical plant defense mechanism relying on the sequestration of iron, a fundamental element for bacterial growth [44]. Iron is sequestered in plant by ferritins, which are multimeric iron storage proteins. AtFer1, one of the 4 genes encoding ferritin in Arabidopsis, is upregulated in plants inoculated with Pectobacterium chrysanthemi or treated with the siderophores (chrysobactin and desferrioxamine) produced by the bacterium. In addition, the upregulation was compromised after inoculation with a siderophore null mutant of the bacterium and AtFer1 knock-out Arabidopsis mutant was found to be more susceptible to bacterial infection. Together these results showed that ferritin accumulation observed during the infection of Arabidopsis with P. chrysanthemi is a basal defense mechanism.

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6.4. Induced resistance

Following HR or cell death caused by necrogenic pathogens, tissues distal to the infection sites can develop resistance to secondary infection by the same or by different pathogens. This phenomenon named systemic acquired resistance (SAR) is dependent upon the action of salicylic acid (SA), which is produced locally and systemically in the plant, and is effective against a fairly broad range of pathogens, bacteria included [23]. Besides being biologically induced, SAR can be induced chemically by functional analogues of SA, such as acibenzolar-S-methyl. This compound, registered in many countries, has no antibacterial activity in vitro, rapidly translocates in plants and is effective in protecting plants against several bacterial diseases [28, 112, 132]. Although SAR is typically coupled with a reduction in symptom severity and bacterial growth in planta, there is a case in which these two parameters are uncoupled. Block et al. [21] reported that reduction in symptom severity systemically induced in tomato plants by virulent and avirulent strains of Xanthomonas campestris pv. vesicatoria against a virulent strain of the same bacterium was not accompanied by a reduced bacterial growth. On the basis of their results, the authors coined the term systemic acquired tolerance (SAT) and suggest that SAT and SAR share common signals including those that repress symptom development, but additional or stronger signals may be responsible for repression of pathogen growth in SAR. Although many studies have been dedicated to the dissection of the signalling cascade leading to SAR especially in Arabidopsis [127], very little information is available on the resistance mechanisms, including those effective against bacterial pathogens. It is likely that plants adopt the same resistance mechanisms to contrast phytopathogenic bacteria during the HR and SAR. It is known that micro-HRs occur in the distal part of plants, where SAR induced by HR develops [6]. It is likely that an unfavourable environment for bacterial growth occurs in the apoplast during SAR development. The antimicrobial compounds likely responsible for SAR resistance are a number of pathogenesis-related proteins (PRs), which accumulate locally in plant tissues undergoing HR and systemically in tissues where SAR is detected [134]. PRs with chitinase and -1,3-glucanase activities may have a role in SAR to bacterial diseases. Besides SAR, another form of induced resistance is ISR (Induced Systemic Resistance), which is potentiated by plant growth-promoting rhizobacteria and is also effective against bacterial diseases [132]. Unlike SAR, ISR does not involve the accumulation of PRs or salicylic acid and relies on pathways regulated by jasmonate and ethylene [102]. For further details on this subject see Chapter 8 of this book.

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7. Concluding remarks

The risk of occurrence of bacterial plant disease epidemics is rising with the increased exchange of plant material worldwide, while the current means for controlling them are often unsatisfactory. Development of new control strategies is outmost urgency and basic research on plant-bacterium interactions, especially at a molecular level, can substantially contribute to attain this goal. As concerns the pathogen, the genome sequencing of an increasing number of phytopathogenic bacteria is providing new information useful for understanding the molecular basis of their pathogenicity and virulence [115]. By in silico analyses of bacterial genomes, such as homology searches, domain analyses and signal peptide predictions, it is possible firstly to survey the secretomes of these pathogens in order to identify key similarities and differences in their secretion systems and secreted protein, and then to systematically profile the expression of these proteins during plant-bacterial interactions [106]. The major challenge for the future is to establish the functions of these proteins, T3SS effectors included, and to identify plant virulence targets. Greater attention should be paid to study the molecular basis of the pathogenicity of Gram-positive phytopathogenic bacteria, especially those which genome has been completely or partially sequenced, such as the subspecies michiganensis and sepedonicus of Clavibacter michiganensis and Leifsonia xyli subsp. xyli. As concerns the plant, rapid progress has been recently achieved in the study of plant defense-signaling pathways in resistance to pathogens, especially during the hypersensitive response and induced resistance. The model plant Arabidopsis thaliana is proving to be an ideal system for studying host defense responses to pathogen attacks [53, 127] also in plant-bacterium interactions, in particular the interaction between Arabidopsis and P. syringae [73]. However, further efforts are necessary to understand the mechanisms responsible for the restriction of bacterial growth during local and systemic resistance, an aspect which has yet to be fully explored.

8. Acknowledgments

This chapter is dedicated to my wife Simona and our son Tommaso. I would like to thank Boris Vinatzer for critical reading of this manuscript. Research funded by the FISR SIMBIO-VEG Project (2005-08).

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