Open access peer-reviewed chapter

Xanthomonas citri ssp. citri Pathogenicity, a Review

Written By

Juan Carlos Caicedo and Sonia Villamizar

Submitted: 29 January 2021 Reviewed: 19 April 2021 Published: 24 June 2021

DOI: 10.5772/intechopen.97776

From the Edited Volume

Citrus - Research, Development and Biotechnology

Edited by Muhammad Sarwar Khan and Iqrar Ahmad Khan

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Abstract

The infectious process of plant by bacteria is not a simple, isolated and fortuitous event. Instead, it requires a vast collection of molecular and cell singularities present in bacteria in order to reach target tissues and ensure successful cell thriving. The bacterium Xanthomonas citri ssp. citri is the etiological agent of citrus canker, this disease affects almost all types of commercial citrus crops. In this chapter we review the main structural and functional bacterial features at phenotypical and genotypical level that are responsible for the symptomatology and disease spread in a susceptible host. Biological features such as: bacterial attachment, antagonism, effector production, quorum sensing regulation and genetic plasticity are the main topics of this review.

Keywords

  • Biofilm
  • Secondary Metabolites
  • Antibiotic
  • Xanthomonadine
  • Quorum sensing

1. Introduction

The surface of the plants is one of the most hostile environments, prevailing factors at the phyllosphere such as: the low availability of nutrients, the high incidence of UV rays, the fluctuating periods of temperature and humidity, mechanical disruption by winds, antibacterial compounds produced by the host plant or by microorganisms member of leaf microbiome, among others, make the bacterial persistence and survival itself a pathogenicity strategy. Due the symptoms development ceases when one pathway involved in the bacterial epiphytic survival is seriously threatened [1]. In phytopathogenic bacteria whose infection route is the phyllosphere, it is important to understand how phenotypic traits upset to ensure survival and surface fitness, and how these traits interact with the phyllosphere microbiome in order to secure the onset of infection (Figure 1). Besides, over the time, on a large-scale, plant leaves will age and fall, thus, the phyllosphere bacteria must have to anticipate living outside of the leaf, for example in the air, soil or reach to young leaves [2].

Figure 1.

Phytopathogenic bacteria plant infection. A. Surface leaf survivor and biofilm formation. B. Bacterial movement to natural opening on leaf. C. Phytotoxins secretion to modulate stomatal closure. D. Effector secretion that affect the cell host behavior. E. Degrading cell wall plant protein secretion.

Bacterium Xanthomonas citri ssp. citri (Xcc) is the etiological agent of bacterial citrus canker. This bacterium is equipped with a huge arsenal of cellular structures that allow its survival in the phyllosphere before it reaches the target mesophyll tissue. Xcc secretes toxins that directly affect the survival of its competitors. Once in the mesophilic tissue Xcc produces effectors that are responsible by the appearance of spongy and corky pathognomonic lesion of citrus canker. In this chapter we will review the both bacterial life style outside and inside of the host.

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2. Xanthomonas citri ssp. citri taxonomy

The bacterium Xantomonas citri ssp. citri is a gram negative rod shape bacteria with a single polar flagellum. Xcc belongs to the Xanthomonas genus from the gamma proteobacteria group. This genus is constituted by 28 species and more than 150 pathovars [3]. In the early 1900s, due to pathogenicity experiments, the bacterium was classified as Pseudomonas citri [4]. Subsequently, the bacterium was classified into different genus such as: phytomonas bacterium and finally at late 1930 classified as Xanthomonas citri [5]. The bacterium continued in X. citri until 1978, when it was classified in X. campestris pv. citri in order to reserve citri at the specific level [6]. In 1989 Gabriel suggest the replaced of bacterium as X. citri [7]. Using DNA–DNA hybridization approach and based on renaturation rates, the bacterium was classified as X. axonopodis pv. citri by Vauterin [8]. Lately, It was suggested major changes to Xanthomond taxonomy, it which were based on multilocus sequence analysis (MLSA) and digital DNA–DNA hybridization of whole genome nucleotide, the author has been recommend the names Xanthomonas citri ssp citri for the etiological agent of citrus cancer type A [9].

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3. Microbe- host interaction

3.1 Microbe -host interaction outside the susceptible host “epiphytic life style”

Bacterial citrus canker disease cycle begins with the deposit of inoculum of XCC at the leaf surface by rain splash. Subsequently, the bacteria move toward the natural opening of leaves, the stomata, then, the bacteria reach the apoplastic space and start the infection process inside the host “endophytic lifestyle”. In this section we are going to focus on the structures, toxins, molecules and extracellular substances that favor and promote the epiphytic interaction between XCC and susceptible citrus host.

3.1.1 Type IV pili

Several bacterial genera are endowed with filamentous appendages called pili. These filamentous organelles include the chaperon- Usher pili, type IV pili (T4P) and gram-positive pili. All types of pili are homopolymers ensembled of thousands of units of pilin protein. The outstanding function of pili is the attachment to surfaces, besides, in Xcc pili type IV is also responsible for the twitching motility and biofilm formation [10]. Type 4 pili is unique in its dynamism, since, it polymerizes and depolymerizes in very fast cycles, which leads to instantaneous extension and retraction cycles producing considerable mechanical force [11], as a consequence, this organelle could attract several substrates like DNA or bacteriophages in order to internalize to periplasmic space, as well as to secrete protein across the membrane [12]. Twitching motility is a bacterial displacement that able to cell to move over humid on organic and inorganic surfaces on a fashion independent of flagella [13]. In the process of biofilm development, the T4P contributes in the initial steps exactly in the reversible attachment phase and subsequently, in the formation of mushroom microcolonies. Contribution of T4P in the pathogenicity in XCC is not completely demonstrated, however, the mutation of pilM gene responsible to encode a membrane protein that participate in the T4P pili ensemble reduce drastically the bacterial virulence [10].

3.1.2 Type V secretion system (non fimbrial adhesins)

Xanthomonads encode type V secretion system (T5SS), it which has a function as non fimbrial adhesins [14]. Compared with the other bacterial secretion systems, the secretion system 5 is one of the simplest complexities from the structural point of view; it is smaller and has only presence at the outer membrane of gram negative bacteria [15]. This T5SS do not have a direct energy source, there is no ATP accessible in the periplasm space neither proton gradient. Consequently, the name of autotransporter has been coined for the this T5SS [16]. The T5SS is comprised of two domains: the β barrel that is located at the out membrane and a secreted passenger. There are five subtypes of T5SS from Va-Ve and recently a new subtype the Vf has been discovered [17]. The bacterium Xcc is endowed with three subclasses of T5SS: Va, Vb and Vc. (Figure 2). Va is a classical auto-transporter, it which transport proteases, lipases and adhesins. The type Vb is a secretion system knowing as Two-Partner Secretion System (TPS), which is composed by a translocator protein and a cognate passenger protein. Translocation from the cytoplasm to the periplasm space occurs by Sec translocase pathway once the perception of amino terminal from signaling peptide is done. The passenger protein has effector function and is termed TpsA. It is transported by TpsB, which forms a pore in the outer membrane in order to enable the TpsA translocation. TpsB also comprise two periplasmic domains. TpsB typically contains a 16-stranded beta-barrel domain that forms the outer membrane pore and two periplasmic POTRA (Polypeptide transport associated). Its function is the recognition of the cognate partner via binding to a TPS domain in TpsA.

Figure 2.

Schematic representation of T5SS present in Xcc. β barrel domain and POTRA are characterized with blue, linker, passengers transported are represented in green and two partner secretion system domain are characterized with red.

The T5SS subclass Vc have a trimeric transporter adhesin conformation, this surface exposed adhesin assembles as homotrimeric structure at the outer membrane [18]. Proteomic and functional studies involving T5SS have revealed roles in pathogenicity to host primarily implicated in the adhesion, especially in the initial steps of pathogenicity process [19, 20].

3.1.3 Xanthomonadin pigment

Xanthomonads bacteria produce a yellow pigment membrane bound known as Xanthomonadins. Several studies have shown that Xanthomonadin has a pivotal role in a epiphytic survival and in plant-pathogen interaction [21, 22]. In the early years this yellow pigment was associated with the carotenoids. However, it was only until its full characterization was achieved that this pigment represents a unique group of aryl-polyene, water insoluble new type of pigment [23]. Genomic analysis shows that a region near to 25.4 kb contains seven transcriptional units (pigA, pigB, pigC, pigD, pigE, pigf and pigG). This gene cluster encodes necessary elements for Xanthomonadin biosynthesis [24]. Biological roles of xanthomonadin in a pathogenicity context are: (i). favor the bacterial epiphytic survival, since, Xanthomonadin avoid the photodamage produced by UV light irradiation that results in ROS production. Similar as structural related carotenoids, Xanthomonadin absorbs wavelengths between UV-C to red light. This pigment gives the bacteria additional advantages against the other phyllosphere colonizer bacteria as it is to deal with stress related factors such as UV irradiation and consequently the photo oxidative damage. Xanthomonadin also offers protection against visible light in the presence of exogenous photosensitizers. Cellular location of Xanthomadin (outer membrane) strongly suggests that this pigment stabilizes cell membrane in the epiphytic phase of this phytopathogenic bacterium. Previous studies in which Xcc deletion mutants of the pig genes were used and which were inoculated using the needleless syringe pressure technique did not show a significant reduction in virulence compared to the wild type phenotype inoculated using the same technique. Instead, when using the spray infection method, that resembles the natural infection method, it which involve the epiphytic fitness stage, the Xcc pig mutant strains display great reduction in the virulence compare with the wild type phenotypes [25]. (ii) Antioxidant activity, the oxidative stressors as ROS and H202 injury the membranes, DNA and proteins, the carotenoids pigments could efficiently quench the ROS.

3.1.4 EPS xanthan and LPS

The EPS in Xanthomonas is named as xanthan, this polysaccharide surrounds the outer membrane through non-covalent ligations [26]. Pathogenicity roles in Xanthomonas genus differ greatly depending on specie, e.g. in Xanthomonas campestris, xanthan suppresses induced innate immunity by calcium chelation [27]. In addition xanthan increases the plant susceptibility to X. campestris due to avoiding the callose deposition [28]. In Xac there is controversy regarding the direct participation of xanthan in the pathogenicity process, while some authors find just a discrete participation in the epiphytic survival [29], another study shows that xanthan deletion mutants reduce the surface leave colonization ability and consequently the severity of citrus canker disease was deeply reduced [30]. Xanthan is a key component in the biofilm formation. The gene cluster gum is responsible for the xanthan production and exportation. This gene cluster comprise 12 successive genes with one operon-like identical direction of transcription i.e. gumB to gumM. The first two genes of cluster gumB and gumC encode components of channel than spans the outmembrane and the periplasmic space and enable the xanthan secretion [31].

The LPS is the major component of the outer leaflet of the outer membrane. The LPS in Xcc have a classic conformation being a tripartite glycoconjugate forming by: lipid A that carries a core oligosaccharide and polysaccharide the O- antigen. LPS that lack the O-antigen are named as lipooligosaccharide (LOS) or rough-type LPS. LPS has an essential role in bacterial growth acting as a barrier for antibacterial compounds and delivering protection against stress as well contributing to the structural proprieties of outer membrane. Lipid A is fairly conserved in most gram-negative bacteria, however, in Xanthomonas genus there is variation in the core oligosaccharide and O antigen structures, there may even be variation between the different species of Xanthomonas [32]. Nowadays is has been established that LPS has a double role in plant-microbial interaction; (i) elicitor of immunity plant response and (ii) It has a role in the promotion of virulence, because it acts as a barrier against antimicrobial activity compounds produced by root hair. Xcc is able to overwhelming plant defense responses induced by LPS.

3.1.5 Quorum sensing and biofilm formation

One discovery in microbiology that completely changed the conception of microbial ecology in the last two decades was the establishment of cooperative behavior in bacterial populations. This social behavior allows members of the bacterial community to adapt to new ecological niches, colonize new habitats, gain a competitive advantage against potential competitors and resist or avoid the host defense [33]. This cooperative behavior is based on a cell to cell communication system known as Quorum Sensing. Quorum sensing (QS) is a system of bacterial cell–cell communication that enables the microorganism to sense a minimum number of cells (quorum) in order to respond to external stimuli in a concerted fashion [34]. The process of QS relies upon the production, release and detection of small signaling molecules called auto-inducers. Each bacterial cell produces a basal quantity of auto-inducers, which are exported to the extracellular environment and reflect bacterial population density. At high cell densities, the auto-inducers reach a critical concentration, at which point they are recognized by their cognate receptor, triggering a cascade of biological functions [35].

The autoinducer in Xcc is a short chain fatty acid molecule known as DSF (Diffusible Signal Factor). Once this DSF accumulates at the extracellular space up to a critical level, it is sensed by its cognate receptor and triggers a cascade of biological function via the internal second messenger cyclic di-GMP, which is involved in virulence, resistance and biofilm formation. The encoding genes for quorum sensing components in Xcc form a cluster termed as rpf (Regulation of Pathogenicity Factors). For detailed revision of DSF quorum sensing circuit in Xcc [36].

Once Xcc reaches a leaf surface, it begins the initial adhesion process that was mention above. This attachment is followed by the formation of biofilm-like structures. Biofilm classical definition is an aggregated composed by several bacterial communities, which are embedded in a self-produced matrix of EPS, these bacterial cells are attached to each other or/and to a surface [37]. Biofilm is composed by polysaccharides, nucleic acids (eDNA), proteins, and have a pivotal role in attachment and protection against biotic and abiotic factors. In Xcc the biofilm formation in leaf and fruit surfaces is a main virulence factor in the early stage of development of citrus canker disease. In Xcc biofilm formation and dispersion is modulated by the quorum sensing autoinducer molecule DSF. How it was mention before DSF autoinducer promotes the biofilm formation because it stimulates the EPS production and pilus ensemble. On the other hand, DSF negatively regulates the biofilm formation because; it upregulates β 1–4 mannanase, ManA, leading to EPS dispersion and disassembly of biofilm [38]. Our previous study shown that quorum sensing signaling plays an essential role in the epiphytic stage survival, which is crucial at the early phase of pathogenicity development. Since, quorum quenchers bacteria belonging to genus Pseudomonas and Bacillus, it which were isolated from leaves of susceptible citrus host, which displayed the ability to disrupt the DSF pathway in Xcc and reduce citrus canker severity in a high susceptible citrus host [34].

3.1.6 T4SS and T6SS potentiates the Xcc antagonism with bacteria inhabiting the phylloplane and the soil amoeba

Nutrient limitation in the phyllosphere additional to environmental changes conditions, make the surface of the leaves one of the most hostile, restrictive and competitive habitats [38]. The type IV protein secretion system is used by bacteria to inject proteins and/or DNA into the prokaryotes and eukaryotes targets. Xanthomonas are endowed with genes that encode components of T4SS, the encoding genes VirB7, VirB8 and VirB9 responsible for the outer membrane pore formation. Genes that encode for VirB3, VirB4, VirB6, VirB8, Vir11, VirD4 and VirB10, responsible for the pore formation at the inner membrane. Finally, the gene that encodes for the subunits VirB2 and VirB5 that form the extracellular pilus structure. Besides, the encoding gene for VirB1 subunit predicted as a periplasmic lytic transglycosylase that plays a role in peptidoglycan alteration throughout T4SS biogenesis [39].

A recent study shows that in Xcc there are near to 12 proteins that interact with inner membrane associated ATPase VirD4, that is responsible for the recognition of substrates to be secreted [40]. These proteins share a C terminal domain termed XVIPCDs (Xanthomonas VirD4-interacting proteins conserved domains). These proteins are translocated into the target bacteria cell resulting in the dead of the receptor cells [41]. This bactericidal T4SS is knowing as X-T4SS and the effectors secreted by this nanomachine are termed X-Tfes (Xanthomonadales likeceeae t4SS effectors). Finally, a recent study reported that T6SS protect Xcc against the predatory amoeba Dyctiostelium [42].

3.2 Microbe -host interaction inside the susceptible host

Once the bacterium Xcc reaches the mesophilic tissue, after of epiphytic fitness and survival events mention before, must have to face the host defense response and parallel to express the pathogenicity factors;

3.2.1 T3SS the main pathogenicity determinant

The type 3 Secretion systems T3SS is the main protein secretion system widely studied in relationship to the pathogenicity. This secretion system is shared with several pathogenic bacteria ranging from animal to plants. This system is known as the “needle” and it works by delivering effector proteins directly to the target cells and modifying their behavior. Effectors from Xcc strains determine the host range. i.e. avirulence factors limit the specificity at the pathogen race/cultivar level by triggering immunity reactions in hosts with a related specific resistance gene. [43]. The effector delivered by the T3SS in Xcc belongs to the AvrBs3/PthA family. Xcc contains four PthA genes that encode transcription activator-like effector (TALE); of these four genes, pthA4 is responsible for the formation of citrus canker lesions. In citrus host the gene known as CsLOB is targeted by the TALE encoded by the Xcc gene pthA4; this gene was assessed in two susceptible host to Xcc infection, i.e., grape fruit and sweet orange [44]. CsLOB1-specific function still remains unclear; some previous studies suggest that CsLOB1 is involved in the regulation of development of lateral organ and metabolism of nitrogen and anthocyanin. Some plant hormones such as auxin, gibberellin, and cytokines also have proven to exert an effect on CsLOB1 gene [45]. Therefore, TALE have been shown to promote host cell transcriptional reprogramming as a virulence strategy [46].

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4. Conclusions

The bacterium Xcc uses various adaptation and colonization strategies, it which are mainly aimed at guaranteeing its epiphytic survival, either by overcoming stress factors of biotic origin (predators, competitors, nutrient limitation) and abiotic origin (UV radiation, humidity and temperature variability). Because, this phase of epiphytic adaptation is crucial for the subsequent development of citric cancer symptoms in the susceptible host. Despite, these mechanism not having a direct effect on the health of the host, they become virulence factors, since its abolition avoid the subsequent development of the characteristic symptoms of citric cancer. Already inside the host, the bacterium uses as the main direct pathogenicity factor, the inoculation of effector proteins TALE, this effector is responsible for inducing cell hyperplasia, leading to rupture of the leaf epidermis and resulting in raised corky and spongy lesions surrounded by a water-soaked margin, the pathognomonic lesson of bacterial citrus canker.

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Conflict of interest

The authors declare no conflict of interest.

References

  1. 1. Pfeilmeier S, Caly DL, Malone JG. Bacterial pathogenesis of plants: future challenges from a microbial perspective: Challenges in Bacterial Molecular Plant Pathology. Mol Plant Pathol. 2016 Oct;17(8):1298-1313. doi: 10.1111/mpp.12427
  2. 2. Vorholt JA. Microbial life in the phyllosphere. Nat Rev Microbiol. 2012 Dec;10(12):828-840. doi: 10.1038/nrmicro2910. PMID: 23154261
  3. 3. Bull CT, De Boer SH, Denny TP et al (2012) List of new names of plant pathogenic bacteria (2008 2010). J Plant Pathol 94(1):21-27
  4. 4. Hasse, C.H. (1915) Pseudomonas citri, the cause of citrus canker – a preliminary report. J. Agric. Res. 4, 97-100
  5. 5. Dowson, W.J. (1939) On the systematic position and generic names of the gram negative bacterial plant pathogens. Zentr. Bakteriol. Parasitenk. Abt. II. 100, 177-193
  6. 6. Young, J.M., Dye, D.W., Bradbury, J.F., Panagopoulos, C.G. and Robbs, C.F. (1978) Proposed nomenclature and classification for plant pathogenic bacteria. N. Z. J. Agric. Res. 21, 153-177
  7. 7. Gabriel, D.W., Kingsley, M.T., Hunter, J.E. and Gottwald, T. (1989) Reinstate- ment of Xanthomonas citri (ex Hasse) and Xanthomonas phaseoli (ex Smith) to species and reclassification of all Xanthomonas campestris pv citri strains. Int. J. Syst. Bacteriol. 39, 14-22
  8. 8. Vauterin, L., Hoste, B., Kersters, K. and Swings, J. (1995) Reclassification of Xanthomonas. Int. J. Syst. Bacteriol. 45, 472-489
  9. 9. Constantin, E.C., Cleenwerck, I., Maes, M., Baeyen, S., Van Malderghem, C., De Vos, P. and Cottyn, B. (2016) Genetic characterization of strains named as Xanthomonas axonopodis pv. dieffenbachiae leads to a taxonomic revision of the X. axonopodis species complex. Plant Pathol. 65, 792-806
  10. 10. German Dunger, Cristiane R. Guzzo, Maxuel O. Andrade, Jeffrey B. Jones, and Chuck S. Farah (2014) Xanthomonas citri subsp. citri Type IV Pilus Is Required for Twitching Motility, Biofilm Development, and Adherence Molecular Plant-Microbe Interactions 27:10, 1132-1147
  11. 11. Ribbe, J., Baker, A. E., Euler, S., O’Toole, G. A. & Maier, (2017) B. Role of cyclic Di-GMP and exopolysaccharide in type IV pilus dynamics. J. Bacteriol. 199, e00859–e00816
  12. 12. Ellison, C. K. et al (2018). Retraction of DNA-bound type IV competence pili initiates DNA uptake during natural Sheetz, M. pili enables transformation in Vibrio cholerae. Nat. Microbiol. 3, 773-780
  13. 13. Henrichsen, J. 1983. Twitching motility. Annu. Rev. Microbiol. 37:81-93
  14. 14. Moreira LM, de Souza RF, Almeida Jr NF, Setubal JC, Oliveira JC, Furlan LR, Ferro JA, da Silva AC (2004) Comparative genomics analyses of citrus-associated bacteria. Annu Rev Phytopathol 42:163-184
  15. 15. Leo, J. C., Grin, I., and Linke, D. (2012). Type V secretion: mechanism(S) of autotransport through the bacterial outer membrane. Philos. Trans. R. Soc. B Biol. Sci. 367, 1088-1101. doi: 10.1098/rstb.2011.0208
  16. 16. Drobnak, I., Braselmann, E., Chaney, J. L., Leyton, D. L., Bernstein, H. D., Lithgow, T., et al. (2015). Of linkers and autochaperones: an unambiguous nomenclature to identify common and uncommon themes for autotransporter secretion. Mol. Microbiol. 95, 1-16. doi: 10.1111/mmi.12838
  17. 17. Grijpstra, J., Arenas, J., Rutten, L., and Tommassen, J. (2013). Autotransporter secretion: varying on a theme. Res. Microbiol. 164, 562-582. doi: 10.1016/j. resmic.2013.03.010
  18. 18. Fan E, Chauhan N, Udatha DBRKG, Leo JC, Linke D. Type V Secretion Systems in Bacteria. Microbiol Spectr 2016;4. https://doi.org/10.1128/microbiolspec. VMBF-0009-2015
  19. 19. Bogdanove AJ, Koebnik R, Lu H, Furutani A, Angiuoli SV, Patil PB, et al. Two new complete genome sequences offer insight into host and tissue specificity of plant pathogenic Xanthomonas spp. J Bacteriol 2011;193:5450-5464
  20. 20. Mhedbi-Hajri N, Darrasse A, Pigné S, Durand K, Fouteau S, Barbe V, et al. Sensing and adhesion are adaptive functions in the plant pathogenic xanthomonads. BMC Evol Biol 2011;11:67
  21. 21. Park, Y.J., Song, E.S., Noh, T.H., Kim, H., Yang, K.S., Hahn, J.H. et al. (2009) Virulence analysis and gene expression profiling of the pigment-deficient mutant of Xanthomonas oryzae pathovar oryzae. FEMS Microbiol Lett 301: 149-155
  22. 22. Rajagopal, L., Sundari, C.S., Balasubramanian, D., and Sonti, R.V. (1997) The bacterial pigment xanthomonadin offers protection against photodamage. FEBS Lett 415: 125-128
  23. 23. Andrewes, A.G., Jenkins, C.L., Starr, M.P., Shepherd, J., and Hope, H. (1976) Structure of xanthomonadin I, a novel di- brominated aryl-polyene pigment produced by the bacterium Xanthomonas juglandis. Tetrahedron Lett 17: 4023-4024
  24. 24. Poplawsky, A.R., and Chun, W. (1997) pigB determines a diffusible factor needed for extracellular polysaccharide slime and xanthomonadin production in Xanthomonas campestris pv. campestris. J Bacteriol 179: 439-444
  25. 25. Poplawsky, A. R., Urban, S. C., & Chun, W. (2000). Biological role of xanthomonadin pigments in Xanthomonas campestris pv. campestris. Applied and environmental microbiology, 66(12), 5123-5127.doi.org/10.1128/aem.66.12.5123-5127.2000
  26. 26. BeckerA, Vorholter F-J. Xanthan biosynthesis by Xanthomonas bacteria: an overview of the current biochemical and genomic data. In: Bernd H. A. Rehm (ed). Microbial Production of Biopolymers and ·polymer Precursors: Applications and Perspectives. UK: Caister Academic Press, 2009, 1-12
  27. 27. Aslam SN, Newman MA, Erbs G et al. Bacterial polysaccharides suppress induced innate immunity by calcium chelation. Curr Biol 2008;18:1078-1083
  28. 28. Yun MH. Xanthan induces plant susceptibility by suppressing callose deposition. PLANT Physiol 2006;141:178-187
  29. 29. Dunger G, Relling VM, Tondo ML et al. 2007. Xanthan is not essential for pathogenicity in citrus canker but contributes to Xanthomonas epiphytic survival. Arch Microbiol;188:127-135
  30. 30. Rigano LA, Siciliano F, Enrique R et al. 2007. Biofilm Formation, Epi- phytic Fitness, and Canker Development in Xanthomonas axonopodis pv. citri. Mol Plant-Microbe Interact;20:1222-30
  31. 31. Bianco MI, Jacobs M, Salinas SR et al. 2014. Biophysical characterizaion of the outer membrane polysaccharide export protein and the polysaccharide co-polymerase protein from Xanthomonas campestris. Protein Expr Purif;101:42-53
  32. 32. Molinaro A, Silipo A, Lanzetta R et al. 2003. Structural elucidation of the O-chain of the lipopolysaccharide from Xanthomonas campestris strain 8004. Carbohydr Res;338:277-281
  33. 33. Ng WL, Bassler BL, 2009. Bacterial quorum-sensing network architectures. Annual Review of Genetics 43, 197-222
  34. 34. Caicedo JC, Villamizar S, Ferro MIT, Kupper KC, Ferro JA. (2016). Bacteria from the citrus phylloplane can disrupt cell–cell signalling in Xanthomonas citri and reduce citrus canker disease severity. Plant Pathology.;65:782-791
  35. 35. Federle MJ, Bassler BL, 2003. Interspecies communication in bacteria. Journal of Clinical Investigations 112, 1291-1299
  36. 36. Juan Carlos Caicedo, Sonia Villamizar and Jesus Aparecido Ferro (2017). Quorum Sensing, Its Role in Virulence and Symptomatology in Bacterial Citrus Canker, Citrus Pathology, Harsimran Gill and Harsh Garg, IntechOpen, DOI: 10.5772/66721
  37. 37. Vert, M. et al. Terminology for biorelated polymers and applications (IUPAC Recommendations 2012). Pure Appl. Chem. 84, 377-410 (2012)
  38. 38. Lindow SE, Brandl MT, 2003. Microbiology of the phyllosphere. Applied and Environmental Microbiology 69, 1875-1883
  39. 39. Ilangovan A, Connery S, Waksman G. (2015). Structural biology of the Gram-negative bacterial conjugation systems. Trends Microbiol;23:301-310
  40. 40. Sgro GG, Oka GU, Souza DP, Cenens W, Bayer-Santos E, Matsuyama BY, et al. 2019. Bacteria-killing type IV secretion systems. Front Microbiol;10:1078
  41. 41. Alegria MC, Souza DP, Andrade MO, Docena C, Khater L, Ramos CHI, et al. 2005. Identification of new protein-protein interactions involving the products of the chromosome- and plasmid-encoded type IV secretion loci of the phytopathogen Xanthomonas axonopodis pv. citri. J Bacteriol;187:2315-25
  42. 42. Bayer-Santos E, Lima L dos P, Ceseti L de M et al. Xanthomonas citri T6SS mediates resistance to Dictyostelium predation and is regulated by an ECF σ factor and cognate Ser/Thr kinase. Environ Microbiol 2018;20:1562-1575
  43. 43. He YQ, Zhang L, Jiang BL et al. 2007. Comparative and functional genomics reveals genetic diversity and determinants of host specificity among reference strains and a large collection of Chinese isolates of the phytopathogen Xanthomonas campestris pv. campestris. Genome Biol;8:R218
  44. 44. Yang H, Junli Z, Hongge J, Davide S, Ting L, Wolf BF, et al (2014). Lateral organ boundaries 1 is a disease susceptibility gene for citrus bacterial canker disease. Proceedings of the National Academy of Sciences of the United States of America.;111:E521-E529
  45. 45. Majer C, Hochholdinger F. (2011). Defining the boundaries: Structure and function of LOB domain proteins. Trends in Plant Science.;16(1):47-52. DOI: 10.1016/j.tplants.2010.09.009
  46. 46. Peng Z, Hu Y, Zhang J, Huguet-Tapia JC, Block AK, Park S, et al. (2019 ). Xanthomonas translucens commandeers the host rate-limiting step in ABA biosynthesis for disease susceptibility. Proc Natl Acad Sci;116:20938-46. https://doi. org/10.1073/pnas.1911660116

Written By

Juan Carlos Caicedo and Sonia Villamizar

Submitted: 29 January 2021 Reviewed: 19 April 2021 Published: 24 June 2021