Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Xanthomonas diversity, virulence and plant–pathogen interactions

Abstract

Xanthomonas spp. encompass a wide range of plant pathogens that use numerous virulence factors for pathogenicity and fitness in plant hosts. In this Review, we examine recent insights into host–pathogen co-evolution, diversity in Xanthomonas populations and host specificity of Xanthomonas spp. that have substantially improved our fundamental understanding of pathogen biology. We emphasize the virulence factors in xanthomonads, such as type III secreted effectors including transcription activator-like effectors, type II secretion systems, diversity resulting in host specificity, evolution of emerging strains, activation of susceptibility genes and strategies of host evasion. We summarize the genomic diversity in several Xanthomonas spp. and implications for disease outbreaks, management strategies and breeding for disease resistance.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Fig. 1: Xanthomonas spp. in different plant hosts.
Fig. 2: Diversity of Xanthomonas spp. and lineages and their virulence genes.
Fig. 3: Xanthomonas spp. effectors and their modes of action to trigger or suppress host defence responses.
Fig. 4: Role of Xanthomonas TALEs in plant susceptibility and resistance.

References

  1. Ryan, R. P. et al. Pathogenomics of Xanthomonas: understanding bacterium–plant interactions. Nat. Rev. Microbiol. 9, 344–355 (2011).

    CAS  PubMed  Google Scholar 

  2. Jacques, M.-A. et al. Using ecology, physiology, and genomics to understand host specificity in Xanthomonas. Ann. Rev. Phytopathol. 54, 163–187 (2016).

    CAS  Google Scholar 

  3. Quezado-Duval, A. M., Leite Jr, R. P., Truffi, D. & Camargo, L. E. Outbreaks of bacterial spot caused by Xanthomonas gardneri on processing tomato in central-west Brazil. Plant Dis. 88, 157–161 (2004).

    CAS  PubMed  Google Scholar 

  4. Babadoost, M. & Ravanlou, A. Outbreak of bacterial spot (Xanthomonas cucurbitae) in pumpkin fields in Illinois. Plant Dis. 96, 1222–1222 (2012).

    CAS  PubMed  Google Scholar 

  5. Nakato, V., Mahuku, G. & Coutinho, T. Xanthomonas campestris pv. musacearum: a major constraint to banana, plantain and enset production in central and east Africa over the past decade. Mol. Plant Pathol. 19, 525–536 (2018).

    CAS  PubMed  Google Scholar 

  6. Tripathi, L. et al. Xanthomonas wilt: a threat to banana production in east and central Africa. Plant Dis. 93, 440–451 (2009).

    PubMed  Google Scholar 

  7. Shimwela, M. M. et al. Banana Xanthomonas wilt continues to spread in Tanzania despite an intensive symptomatic plant removal campaign: an impending socio-economic and ecological disaster. Food Sec. 8, 939–951 (2016).

    Google Scholar 

  8. Constantin, E. C. et al. 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 (2016).

    CAS  Google Scholar 

  9. Timilsina, S. et al. Reclassification of Xanthomonas gardneri (ex Šutič 1957) Jones et al. 2006 as a later heterotypic synonym of Xanthomonas cynarae Trébaol et al. 2000 and description of X. cynarae pv. cynarae and X. cynarae pv. gardneri based on whole genome analyses. Int. J. Syst. Evol. Micr. 69, 343–349 (2019).

    CAS  Google Scholar 

  10. Rademaker, J. L. W. et al. A comprehensive species to strain taxonomic framework for Xanthomonas. Phytopathology 95, 1098–1111 (2005).

    CAS  PubMed  Google Scholar 

  11. Leibniz Institute DSMZ–German Collection of Microorganisms and Cell Cultures GmbH. Prokaryotic Nomenclature Up-to-date. https://www.dsmz.de/services/online-tools/prokaryotic-nomenclature-up-to-date/prokaryotic-nomenclature-up-to-date/genus/516930 (2019).

  12. Poplawsky, A. R. A xanthomonadin-encoding gene cluster for the identification of pathovars of Xanthomonas campestris. Mol. Plant Microbe Interact. 6, 545 (1993).

    CAS  Google Scholar 

  13. Midha, S. & Patil, P. B. Genomic insights into the evolutionary origin of Xanthomonas axonopodis pv. citri and its ecological relatives. Appl. Environ. Microbiol. 80, 6266–6279 (2014).

    PubMed  PubMed Central  Google Scholar 

  14. Ferreira, M. A. S. V. et al. Xanthomonas citri pv. viticola affecting grapevine in Brazil: emergence of a successful monomorphic pathogen. Front. Plant Sci. 10, 489 (2019).

    PubMed  PubMed Central  Google Scholar 

  15. Pruvost, O., Couteau, A., Perrier, X. & Luisetti, J. Phenotypic diversity of Xanthomonas sp. mangiferaeindicae. J. Appl. Microbiol. 84, 115–124 (1998).

    CAS  PubMed  Google Scholar 

  16. An, S.-Q. et al. Mechanistic insights into host adaptation, virulence and epidemiology of the phytopathogen Xanthomonas. FEMS Microbiol. Rev. 44, 1–32 (2019).

    PubMed Central  Google Scholar 

  17. Zhang, H. & Wang, S. Rice versus Xanthomonas oryzae pv. oryzae: a unique pathosystem. Curr. Opin. Plant Biol. 16, 188–195 (2013).

    PubMed  Google Scholar 

  18. Cesbron, S. et al. Comparative genomics of pathogenic and nonpathogenic strains of Xanthomonas arboricola unveil molecular and evolutionary events linked to pathoadaptation. Front. Plant Sci. 6, 1126 (2015).

    PubMed  PubMed Central  Google Scholar 

  19. Timilsina, S. et al. Multiple recombination events drive the current genetic structure of Xanthomonas perforans in Florida. Front. Microbiol. 10, 448 (2019).

    PubMed  PubMed Central  Google Scholar 

  20. Huang, C.-L. et al. Ecological genomics in Xanthomonas: the nature of genetic adaptation with homologous recombination and host shifts. BMC Genomics 16, 188 (2015).

    PubMed  PubMed Central  Google Scholar 

  21. Merda, D. et al. Recombination-prone bacterial strains form a reservoir from which epidemic clones emerge in agroecosystems. Environ. Microbiol. Rep. 8, 572–581 (2016).

    PubMed  Google Scholar 

  22. Newberry, E. A. et al. Independent evolution with the gene flux originating from multiple Xanthomonas species explains genomic heterogeneity in Xanthomonas perforans. Appl. Environ. Microbiol. 85, e00885-19 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Hsiao, Y.-M., Liao, H.-Y., Lee, M.-C., Yang, T.-C. & Tseng, Y.-H. Clp upregulates transcription of engA gene encoding a virulence factor in Xanthomonas campestris by direct binding to the upstream tandem Clp sites. FEBS Lett. 579, 3525–3533 (2005).

    CAS  PubMed  Google Scholar 

  24. Constantin, E. C. et al. Pathogenicity and virulence gene content of Xanthomonas strains infecting Araceae, formerly known as Xanthomonas axonopodis pv. dieffenbachiae. Plant Pathol. 66, 1539–1554 (2017).

    CAS  Google Scholar 

  25. Rossier, O., Wengelnik, K., Hahn, K. & Bonas, U. The Xanthomonas Hrp type III system secretes proteins from plant and mammalian bacterial pathogens. Proc. Natl Acad. Sci. USA 96, 9368–9373 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. White, F. F., Potnis, N., Jones, J. B. & Koebnik, R. The type III effectors of Xanthomonas. Mol. Plant Pathol. 10, 749–766 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Teper, D. et al. Identification of novel Xanthomonas euvesicatoria type III effector proteins by a machine-learning approach. Mol. Plant Pathol. 17, 398–411 (2016).

    CAS  PubMed  Google Scholar 

  28. Grau, J. et al. AnnoTALE: bioinformatics tools for identification, annotation, and nomenclature of TALEs from Xanthomonas genomic sequences. Sci. Rep. 6, 21077 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Sgro, G. G. et al. Bacteria-killing type IV secretion systems. Front. Microbiol. 10, 1078 (2019).

    PubMed  PubMed Central  Google Scholar 

  30. Szczesny, R. et al. Functional characterization of the Xcs and Xps type II secretion systems from the plant pathogenic bacterium Xanthomonas campestris pv vesicatoria. N. Phytol. 187, 983–1002 (2010).

    CAS  Google Scholar 

  31. Potnis, N. et al. Comparative genomics reveals diversity among xanthomonads infecting tomato and pepper. BMC Genomics 12, 146 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Weiberg, A. & Jin, H. Small RNAs—the secret agents in the plant–pathogen interactions. Curr. Opin. Plant Biol. 26, 87–94 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Schmidtke, C. et al. Genome-wide transcriptome analysis of the plant pathogen Xanthomonas identifies sRNAs with putative virulence functions. Nucleic Acids Res. 40, 2020–2031 (2012).

    CAS  PubMed  Google Scholar 

  34. Büttner, D. & Bonas, U. Regulation and secretion of Xanthomonas virulence factors. FEMS Microbiol. Rev. 34, 107–133 (2010).

    PubMed  Google Scholar 

  35. Russell, A. B., Peterson, S. B. & Mougous, J. D. Type VI secretion system effectors: poisons with a purpose. Nat. Rev. Microbiol. 12, 137–148 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Silva, A. C. R. da et al. Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nature 417, 459–463 (2002).

    PubMed  Google Scholar 

  37. Bogdanove, A. J. et al. Two new complete genome sequences offer insight into host and tissue specificity of plant pathogenic Xanthomonas spp. J. Bacteriol. 193, 5450–5464 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Richard, D. et al. Complete genome sequences of six copper-resistant Xanthomonas citri pv. citri strains causing asiatic citrus canker, obtained using long-read technology. Genome Announc. 5, e00010-17 (2017).

    PubMed  PubMed Central  Google Scholar 

  39. Pieretti, I. et al. The complete genome sequence of Xanthomonas albilineans provides new insights into the reductive genome evolution of the xylem-limited Xanthomonadaceae. BMC Genomics 10, 616 (2009).

    PubMed  PubMed Central  Google Scholar 

  40. Pieretti, I. et al. Genomic insights into strategies used by Xanthomonas albilineans with its reduced artillery to spread within sugarcane xylem vessels. BMC Genomics 13, 658 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Pieretti, I. et al. What makes Xanthomonas albilineans unique amongst xanthomonads? Front. Plant. Sci. 6, 289 (2015).

    PubMed  PubMed Central  Google Scholar 

  42. Mhedbi-Hajri, N. et al. Evolutionary history of the plant pathogenic bacterium Xanthomonas axonopodis. PLOS ONE 8, e58474 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Schwartz, A. R. et al. Phylogenomics of Xanthomonas field strains infecting pepper and tomato reveals diversity in effector repertoires and identifies determinants of host specificity. Front. Microbiol. 6, 535 (2015).

    PubMed  PubMed Central  Google Scholar 

  44. Kałużna, M., Pulawska, J., Waleron, M. & Sobiczewski, P. The genetic characterization of Xanthomonas arboricola pv. juglandis, the causal agent of walnut blight in Poland. Plant Pathol. 63, 1404–1416 (2014).

    Google Scholar 

  45. Garita-Cambronero, J., Palacio-Bielsa, A., López, M. M. & Cubero, J. Pan-genomic analysis permits differentiation of virulent and non-virulent strains of Xanthomonas arboricola that cohabit Prunus spp. and elucidate bacterial virulence factors. Front. Microbiol. 8, 573 (2017).

    PubMed  PubMed Central  Google Scholar 

  46. Jacobs, J. M., Pesce, C., Lefeuvre, P. & Koebnik, R. Comparative genomics of a cannabis pathogen reveals insight into the evolution of pathogenicity in Xanthomonas. Front. Plant Sci. 6, 431 (2015).

    PubMed  PubMed Central  Google Scholar 

  47. Timilsina, S. et al. Multilocus sequence analysis of xanthomonads causing bacterial spot of tomato and pepper plants reveals strains generated by recombination among species and recent global spread of Xanthomonas gardneri. Appl. Environ. Microbiol. 81, 1520–1529 (2015).

    PubMed  PubMed Central  Google Scholar 

  48. Jibrin, M. O. et al. Genomic inference of recombination-mediated evolution in Xanthomonas euvesicatoria and X. perforans. Appl. Environ. Microbiol. 84, e00136-18 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Quibod, I. L. et al. The green revolution shaped the population structure of the rice pathogen Xanthomonas oryzae pv. oryzae. ISME J. 14, 492–505 (2019).

    PubMed  PubMed Central  Google Scholar 

  50. Ochiai, H., Inoue, Y., Takeya, M., Sasaki, A. & Kaku, H. Genome sequence of Xanthomonas oryzae pv. oryzae suggests contribution of large numbers of effector genes and insertion sequences to its race diversity. Jpn. Agric. Res. Q. 39, 275–287 (2005).

    CAS  Google Scholar 

  51. Rajeshwari, R. & Sonti, R. V. Stationary-phase variation due to transposition of novel insertion elements in Xanthomonas oryzae pv. oryzae. J. Bacteriol. 182, 4797–4802 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Boch, J. & Bonas, U. Xanthomonas AvrBs3 family-type III effectors: discovery and function. Ann. Rev. Phytopathol. 48, 419–436 (2010).

    CAS  Google Scholar 

  53. Gochez, A. M. et al. Pacbio sequencing of copper-tolerant Xanthomonas citri reveals presence of a chimeric plasmid structure and provides insights into reassortment and shuffling of transcription activator-like effectors among X. citri strains. BMC Genomics 19, 16 (2018).

    PubMed  PubMed Central  Google Scholar 

  54. Escalon, A. et al. Variations in type III effector repertoires, pathological phenotypes and host range of Xanthomonas citri pv. citri pathotypes. Mol. Plant Pathol. 14, 483–496 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Gordon, J. L. et al. Comparative genomics of 43 strains of Xanthomonas citri pv. citri reveals the evolutionary events giving rise to pathotypes with different host ranges. BMC Genomics 16, 1098 (2015).

    PubMed  PubMed Central  Google Scholar 

  56. Rybak, M., Minsavage, G. V., Stall, R. E. & Jones, J. B. Identification of Xanthomonas citri ssp. citri host specificity genes in a heterologous expression host. Mol. Plant Pathol. 10, 249–262 (2009).

    CAS  PubMed  Google Scholar 

  57. Patané, J. S. L. et al. Origin and diversification of Xanthomonas citri subsp. citri pathotypes revealed by inclusive phylogenomic, dating, and biogeographic analyses. BMC Genomics 20, 700 (2019).

    PubMed  PubMed Central  Google Scholar 

  58. Roman-Reyna, V. et al. The rice leaf microbiome has a conserved community structure controlled by complex host–microbe interactions. Preprint at bioRxiv. https://doi.org/10.1101/615278 (2019).

  59. Zhang, J. et al. Insights into endophytic bacterial community structures of seeds among various Oryza sativa L. rice genotypes. J. Plant Growth Regul. 38, 93–102 (2019).

    CAS  Google Scholar 

  60. Merda, D. et al. Ancestral acquisitions, gene flow and multiple evolutionary trajectories of the type three secretion system and effectors in Xanthomonas plant pathogens. Mol. Ecol. 26, 5939–5952 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Baptista, J. C. et al. Mutation in the xpsD gene of Xanthomonas axonopodis pv. citri affects cellulose degradation and virulence. Genet. Mol. Biol. 33, 146–153 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Bayer-Santos, E. 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. 20, 1562–1575 (2018).

    CAS  PubMed  Google Scholar 

  63. Bayer-Santos, E., Ceseti, L. de M., Farah, C. S. & Alvarez-Martinez, C. E. Distribution, function and regulation of type 6 secretion systems of Xanthomonadales. Front. Microbiol. 10, 1635 (2019).

    PubMed  PubMed Central  Google Scholar 

  64. Shrivastava, S. & Mande, S. S. Identification and functional characterization of gene components of type VI secretion system in bacterial genomes. PLOS ONE 3, e2955 (2008).

    PubMed  PubMed Central  Google Scholar 

  65. Records, A. R. The type VI secretion system: a multipurpose delivery system with a phage-like machinery. Mol. Plant Microbe Interact. 24, 751–757 (2011).

    CAS  PubMed  Google Scholar 

  66. Boyer, F., Fichant, G., Berthod, J., Vandenbrouck, Y. & Attree, I. Dissecting the bacterial type VI secretion system by a genome wide in silico analysis: what can be learned from available microbial genomic resources? BMC Genomics 10, 104 (2009).

    PubMed  PubMed Central  Google Scholar 

  67. Kay, S. & Bonas, U. How Xanthomonas type III effectors manipulate the host plant. Curr. Opin. Microbiol. 12, 37–43 (2009).

    CAS  PubMed  Google Scholar 

  68. Mudgett, M. B. et al. Molecular signals required for type III secretion and translocation of the Xanthomonas campestris AvrBs2 protein to pepper plants. Proc. Natl Acad. Sci. USA 97, 13324–13329 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Roden, J., Eardley, L., Hotson, A., Cao, Y. & Mudgett, M. B. Characterization of the Xanthomonas AvrXv4 effector, a SUMO protease translocated into plant cells. Mol. Plant. Microbe Interact. 17, 633–643 (2004).

    CAS  PubMed  Google Scholar 

  70. Xia, J., Hu, X., Shi, F., Niu, X. & Zhang, C. Support vector machine method on predicting resistance gene against Xanthomonas oryzae pv. oryzae in rice. Expert. Syst. Appl. 37, 5946–5950 (2010).

    Google Scholar 

  71. Midha, S. et al. Population genomic insights into variation and evolution of Xanthomonas oryzae pv. oryzae. Sci. Rep. 7, 1–13 (2017).

    Google Scholar 

  72. Sinha, D., Gupta, M. K., Patel, H. K., Ranjan, A. & Sonti, R. V. Cell wall degrading enzyme induced rice innate immune responses are suppressed by the type 3 secretion system effectors XopN, XopQ, XopX and XopZ of Xanthomonas oryzae pv. oryzae. PLOS ONE 8, e75867 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Teper, D. et al. The Xanthomonas euvesicatoria type III effector XopAU is an active protein kinase that manipulates plant MAP kinase signaling. PLOS Pathog. 14, e1006880 (2018).

    PubMed  PubMed Central  Google Scholar 

  74. Mondal, K. K. et al. Pathotyping and genetic screening of type III effectors in Indian strains of Xanthomonas oryzae pv. oryzae causing bacterial leaf blight of rice. Physiol. Mol. Plant Pathol. 86, 98–106 (2014).

    CAS  Google Scholar 

  75. Roux, B. et al. Genomics and transcriptomics of Xanthomonas campestris species challenge the concept of core type III effectome. BMC Genomics 16, 975 (2015).

    PubMed  PubMed Central  Google Scholar 

  76. Üstün, S. & Börnke, F. Interactions of Xanthomonas type-III effector proteins with the plant ubiquitin and ubiquitin-like pathways. Front. Plant Sci. 5, 736 (2014).

    PubMed  PubMed Central  Google Scholar 

  77. Sonnewald, S. et al. Regulation of cell wall-bound invertase in pepper leaves by Xanthomonas campestris pv. vesicatoria type three effectors. PLOS ONE 7, e51763 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Feng, F. & Zhou, J.-M. Plant–bacterial pathogen interactions mediated by type III effectors. Curr. Opin. Plant Biol. 15, 469–476 (2012).

    PubMed  Google Scholar 

  79. Stall, R. E., Jones, J. B. & Minsavage, G. V. Durability of resistance in tomato and pepper to xanthomonads causing bacterial spot. Annu. Rev. Phytopathol. 47, 265–284 (2009).

    CAS  PubMed  Google Scholar 

  80. Han, S. W. & Hwang, B. K. Molecular functions of Xanthomonas type III effector AvrBsT and its plant interactors in cell death and defense signaling. Planta 245, 237–253 (2017).

    CAS  PubMed  Google Scholar 

  81. Teper, D. et al. Xanthomonas euvesicatoria type III effector XopQ interacts with tomato and pepper 14–3–3 isoforms to suppress effector-triggered immunity. Plant J. 77, 297–309 (2014).

    CAS  PubMed  Google Scholar 

  82. Szurek, B., Marois, E., Bonas, U. & Ackerveken, G. V. den. Eukaryotic features of the Xanthomonas type III effector AvrBs3: protein domains involved in transcriptional activation and the interaction with nuclear import receptors from pepper. Plant J. 26, 523–534 (2001).

    CAS  PubMed  Google Scholar 

  83. Song, C. & Yang, B. Mutagenesis of 18 type III effectors reveals virulence function of XopZ(PXO99) in Xanthomonas oryzae pv. oryzae. Mol. Plant Microbe Interact. 23, 893–902 (2010).

    CAS  PubMed  Google Scholar 

  84. Schulze, S. et al. Analysis of new type III effectors from Xanthomonas uncovers XopB and XopS as suppressors of plant immunity. N. Phytol. 195, 894–911 (2012).

    CAS  Google Scholar 

  85. Popov, G., Fraiture, M., Brunner, F. & Sessa, G. Multiple Xanthomonas euvesicatoria type III effectors inhibit flg22-triggered immunity. Mol. Plant Microbe Interact. 29, 651–660 (2016).

    CAS  PubMed  Google Scholar 

  86. Salomon, D., Dar, D., Sreeramulu, S. & Sessa, G. Expression of Xanthomonas campestris pv. vesicatoria type III effectors in yeast affects cell growth and viability. Mol. Plant Microbe Interact. 24, 305–314 (2011).

    CAS  PubMed  Google Scholar 

  87. Mutka, A. M. et al. Quantitative, image-based phenotyping methods provide insight into spatial and temporal dimensions of plant disease. Plant Physiol. 172, 650–660 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  88. Boch, J. et al. Breaking the code of DNA binding specificity of TAL-type III effectors. Science 326, 1509–1512 (2009).

    CAS  PubMed  Google Scholar 

  89. Yang, B., Sugio, A. & White, F. F. Os8N3 is a host disease-susceptibility gene for bacterial blight of rice. Proc. Natl Acad. Sci. USA 103, 10503–10508 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  90. Moscou, M. J. & Bogdanove, A. J. A simple cipher governs DNA recognition by TAL effectors. Science 326, 1501 (2009).

    CAS  PubMed  Google Scholar 

  91. Thieme, F. et al. Insights into genome plasticity and pathogenicity of the plant pathogenic bacterium Xanthomonas campestris pv. vesicatoria revealed by the complete genome sequence. J. Bacteriol. 187, 7254–7266 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Hutin, M., Pérez-Quintero, A. L., Lopez, C. & Szurek, B. MorTAL Kombat: the story of defense against TAL effectors through loss-of-susceptibility. Front. Plant. Sci. 6, 535 (2015).

    PubMed  PubMed Central  Google Scholar 

  93. Oliva, R. et al. Broad-spectrum resistance to bacterial blight in rice using genome editing. Nat. Biotechnol. 37, 1344–1350 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  94. Streubel, J. et al. Five phylogenetically close rice SWEET genes confer TAL effector-mediated susceptibility to Xanthomonas oryzae pv. oryzae. N. Phytol. 200, 808–819 (2013).

    CAS  Google Scholar 

  95. Ma, L. et al. Essential role of sugar transporter OsSWEET11 during the early stage of rice grain filling. Plant Cell Physiol. 58, 863–873 (2017).

    CAS  PubMed  Google Scholar 

  96. Römer, P. et al. Promoter elements of rice susceptibility genes are bound and activated by specific TAL effectors from the bacterial blight pathogen, Xanthomonas oryzae pv. oryzae. N. Phytol. 187, 1048–1057 (2010).

    Google Scholar 

  97. Antony, G. et al. Rice xa13 recessive resistance to bacterial blight is defeated by induction of the disease susceptibility gene Os-11N3. Plant. Cell 22, 3864–3876 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  98. Zhou, J. et al. Gene targeting by the TAL effector PthXo2 reveals cryptic resistance gene for bacterial blight of rice. Plant. J. 82, 632–643 (2015).

    CAS  PubMed  Google Scholar 

  99. Yu, Y. et al. Colonization of rice leaf blades by an African strain of Xanthomonas oryzae pv. oryzae depends on a new TAL effector that induces the rice nodulin-3 Os11N3 gene. Mol. Plant. Microbe Interact. 24, 1102–1113 (2011).

    CAS  PubMed  Google Scholar 

  100. Chen, L.-Q. et al. Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468, 527–532 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  101. Peng, Z. et al. Xanthomonas translucens commandeers the host rate-limiting step in ABA biosynthesis for disease susceptibility. Proc. Natl Acad. Sci. USA 116, 20938–20946 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  102. Falahi Charkhabi, N. et al. Complete genome sequencing and targeted mutagenesis reveal virulence contributions of Tal2 and Tal4b of Xanthomonas translucens pv. undulosa ICMP11055 in bacterial leaf streak of wheat. Front. Microbiol. 8, 1488 (2017).

    PubMed  PubMed Central  Google Scholar 

  103. Hu, Y. et al. Lateral organ boundaries 1 is a disease susceptibility gene for citrus bacterial canker disease. Proc. Natl Acad. Sci. USA 111, E521–E529 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  104. Li, Z. et al. A potential disease susceptibility gene CsLOB of citrus is targeted by a major virulence effector PthA of Xanthomonas citri subsp. citri. Mol. Plant. 7, 912–915 (2014).

    CAS  PubMed  Google Scholar 

  105. Jia, H. et al. Genome editing of the disease susceptibility gene CsLOB1 in citrus confers resistance to citrus canker. Plant Biotechnol. J. 15, 817–823 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  106. Peng, A. et al. Engineering canker-resistant plants through CRISPR/Cas9-targeted editing of the susceptibility gene CsLOB1 promoter in citrus. Plant Biotechnol. J. 15, 1509–1519 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  107. Schornack, S. et al. The tomato resistance protein Bs4 is a predicted non-nuclear TIR-NB-LRR protein that mediates defense responses to severely truncated derivatives of AvrBs4 and overexpressed AvrBs3. Plant. J. 37, 46–60 (2004).

    CAS  PubMed  Google Scholar 

  108. Triplett, L. R. et al. A resistance locus in the American heirloom rice variety Carolina Gold Select is triggered by TAL effectors with diverse predicted targets and is effective against African strains of Xanthomonas oryzae pv. oryzicola. Plant. J. 87, 472–483 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  109. Ji, Z. et al. Interfering TAL effectors of Xanthomonas oryzae neutralize R-gene-mediated plant disease resistance. Nat. Commun. 7, 13435 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  110. Yoshimura, S. et al. Expression of Xa1, a bacterial blight-resistance gene in rice, is induced by bacterial inoculation. Proc. Natl Acad. Sci. USA 95, 1663–1668 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  111. Zhang, J., Yin, Z. & White, F. TAL effectors and the executor R genes. Front. Plant Sci. 6, 641 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  112. Abendroth, U., Schmidtke, C. & Bonas, U. Small non-coding RNAs in plant-pathogenic Xanthomonas spp. RNA Biol. 11, 457–463 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  113. Solé, M. et al. Xanthomonas campestris pv. vesicatoria secretes proteases and xylanases via the Xps type II secretion system and outer membrane vesicles. J. Bacteriol. 197, 2879–2893 (2015).

    PubMed  PubMed Central  Google Scholar 

  114. Guerrero-Mandujano, A., Hernández-Cortez, C., Ibarra, J. A. & Castro-Escarpulli, G. The outer membrane vesicles: secretion system type zero. Traffic 18, 425–432 (2017).

    PubMed  Google Scholar 

  115. Sidhu, V. K., Vorhölter, F.-J., Niehaus, K. & Watt, S. A. Analysis of outer membrane vesicle associated proteins isolated from the plant pathogenic bacterium Xanthomonas campestris pv. campestris. BMC Microbiol. 8, 87 (2008).

    PubMed  PubMed Central  Google Scholar 

  116. Zhou, X. et al. A phosphorylation switch on lon protease regulates bacterial type III secretion system in host. mBio 9, e02146-17 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  117. Teper, D., Zhang, Y. & Wang, N. TfmR, a novel TetR-family transcriptional regulator, modulates the virulence of Xanthomonas citri in response to fatty acids. Mol. Plant. Pathol. 20, 701–715 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  118. Cheng, S.-T., Wang, F.-F. & Qian, W. Cyclic-di-GMP binds to histidine kinase RavS to control RavS-RavR phosphotransfer and regulates the bacterial lifestyle transition between virulence and swimming. PLOS Pathog. 15, e1007952 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  119. Deng, C.-Y. et al. Proteolysis of histidine kinase VgrS inhibits its autophosphorylation and promotes osmostress resistance in Xanthomonas campestris. Nat. Commun. 9, 1–15 (2018).

    Google Scholar 

  120. Wang, F.-F., Cheng, S.-T., Wu, Y., Ren, B.-Z. & Qian, W. A bacterial receptor PcrK senses the plant hormone cytokinin to promote adaptation to oxidative stress. Cell Rep. 21, 2940–2951 (2017).

    CAS  PubMed  Google Scholar 

  121. Zheng, D. et al. Two overlapping two-component systems in Xanthomonas oryzae pv. oryzae contribute to full fitness in rice by regulating virulence factors expression. Sci. Rep. 6, 1–13 (2016).

    Google Scholar 

  122. Kim, H. et al. A genome-scale co-functional network of Xanthomonas genes can accurately reconstruct regulatory circuits controlled by two-component signaling systems. Mol. Cell 42, 166–174 (2019).

    CAS  Google Scholar 

  123. Souza, D. P. et al. Bacterial killing via a type IV secretion system. Nat. Commun. 6, 1–9 (2015).

    CAS  Google Scholar 

  124. Jackson, R. W., Vinatzer, B., Arnold, D. L., Dorus, S. & Murillo, J. The influence of the accessory genome on bacterial pathogen evolution. Mob. Genet. Elem. 1, 55–65 (2011).

    Google Scholar 

  125. Bartoli, C., Roux, F. & Lamichhane, J. R. Molecular mechanisms underlying the emergence of bacterial pathogens: an ecological perspective. Mol. Plant. Pathol. 17, 303–310 (2015).

    PubMed  PubMed Central  Google Scholar 

  126. Lima, W. C., Sluys, M.-A. V. & Menck, C. F. M. Non-γ-proteobacteria gene islands contribute to the Xanthomonas genome. OMICS 9, 160–172 (2005).

    CAS  PubMed  Google Scholar 

  127. Lima, W. C., Paquola, A. C. M., Varani, A. M., Van Sluys, M.-A. & Menck, C. F. M. Laterally transferred genomic islands in Xanthomonadales related to pathogenicity and primary metabolism. FEMS Microbiol. Lett. 281, 87–97 (2008).

    CAS  PubMed  Google Scholar 

  128. Lang, J. M. et al. A pathovar of Xanthomonas oryzae infecting wild grasses provides insight into the evolution of pathogenicity in rice agroecosystems. Front. Plant. Sci. 10, 507 (2019).

    PubMed  PubMed Central  Google Scholar 

  129. Hert, A. P. et al. Relative importance of bacteriocin-like genes in antagonism of Xanthomonas perforans tomato race 3 to Xanthomonas euvesicatoria tomato race 1 strains. Appl. Environ. Microbiol. 71, 3581–3588 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  130. Timilsina, S. et al. Analysis of sequenced genomes of Xanthomonas perforans identifies candidate targets for resistance breeding in tomato. Phytopathology 106, 1097–1104 (2016).

    CAS  PubMed  Google Scholar 

  131. Abrahamian, P. et al. The type III effector AvrBsT enhances Xanthomonas perforans fitness in field-grown tomato. Phytopathology 108, 1355–1362 (2018).

    CAS  PubMed  Google Scholar 

  132. Quibod, I. L. et al. Effector diversification contributes to Xanthomonas oryzae pv. oryzae phenotypic adaptation in a semi-isolated environment. Sci. Rep. 6, 1–11 (2016).

    Google Scholar 

  133. Zipfel, C. et al. Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428, 764–767 (2004).

    CAS  PubMed  Google Scholar 

  134. Zipfel, C. et al. Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125, 749–760 (2006).

    CAS  PubMed  Google Scholar 

  135. Willmann, R. et al. Arabidopsis lysin-motif proteins LYM1 LYM3 CERK1 mediate bacterial peptidoglycan sensing and immunity to bacterial infection. Proc. Natl Acad. Sci. USA 108, 19824–19829 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  136. Kutschera, A. et al. Bacterial medium-chain 3-hydroxy fatty acid metabolites trigger immunity in Arabidopsis plants. Science 364, 178–181 (2019).

    CAS  PubMed  Google Scholar 

  137. Buscaill, P. et al. Glycosidase and glycan polymorphism control hydrolytic release of immunogenic flagellin peptides. Science 364, eaav0748 (2019).

    CAS  PubMed  Google Scholar 

  138. Sun, W., Dunning, F. M., Pfund, C., Weingarten, R. & Bent, A. F. Within-species flagellin polymorphism in Xanthomonas campestris pv campestris and its impact on elicitation of Arabidopsis FLAGELLIN SENSING2-dependent defenses. Plant. Cell 18, 764–779 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  139. Wang, S. et al. Rice OsFLS2-mediated perception of bacterial flagellins is evaded by Xanthomonas oryzae pvs. oryzae and oryzicola. Mol. Plant. 8, 1024–1037 (2015).

    CAS  PubMed  Google Scholar 

  140. Newman, M.-A., von Roepenack-Lahaye, E., Parr, A., Daniels, M. J. & Dow, J. M. Prior exposure to lipopolysaccharide potentiates expression of plant defenses in response to bacteria. Plant. J. 29, 487–495 (2002).

    CAS  PubMed  Google Scholar 

  141. Erbs, G. et al. Peptidoglycan and muropeptides from pathogens Agrobacterium and Xanthomonas elicit plant innate immunity: structure and activity. Chem. Biol. 15, 438–448 (2008).

    CAS  PubMed  Google Scholar 

  142. Lacombe, S. et al. Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance. Nat. Biotechnol. 28, 365–369 (2010).

    CAS  PubMed  Google Scholar 

  143. Proietti, S. et al. Xanthomonas campestris lipooligosaccharides trigger innate immunity and oxidative burst in Arabidopsis. Plant. Physiol. Biochem. 85, 51–62 (2014).

    CAS  PubMed  Google Scholar 

  144. Kakkar, A., Nizampatnam, N. R., Kondreddy, A., Pradhan, B. B. & Chatterjee, S. Xanthomonas campestris cell–cell signalling molecule DSF (diffusible signal factor) elicits innate immunity in plants and is suppressed by the exopolysaccharide xanthan. J. Exp. Bot. 66, 6697–6714 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  145. Keshavarzi, M. et al. Basal defenses induced in pepper by lipopolysaccharides are suppressed by Xanthomonas campestris pv. vesicatoria. Mol. Plant. Microbe Interact. 17, 805–815 (2004).

    CAS  PubMed  Google Scholar 

  146. Li, S. et al. The type III effector AvrBs2 in Xanthomonas oryzae pv. oryzicola suppresses rice immunity and promotes disease development. Mol. Plant. Microbe Interact. 28, 869–880 (2015).

    CAS  PubMed  Google Scholar 

  147. Priller, J. P. R., Reid, S., Konein, P., Dietrich, P. & Sonnewald, S. The Xanthomonas campestris pv. vesicatoria type-3 effector XopB inhibits plant defence responses by interfering with ROS production. PLOS ONE 11, e0159107 (2016).

    PubMed  PubMed Central  Google Scholar 

  148. Long, J. et al. Non-TAL effectors from Xanthomonas oryzae pv. oryzae suppress peptidoglycan-triggered MAPK activation in rice. Front. Plant. Sci. 9, 1857 (2018).

    PubMed  PubMed Central  Google Scholar 

  149. Medina, C. A. et al. The role of type III effectors from Xanthomonas axonopodis pv. manihotis in virulence and suppression of plant immunity. Mol. Plant. Pathol. 19, 593–606 (2018).

    CAS  PubMed  Google Scholar 

  150. Song, W. Y. et al. A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270, 1804–1806 (1995).

    CAS  PubMed  Google Scholar 

  151. Pruitt, R. N. et al. A microbially derived tyrosine-sulfated peptide mimics a plant peptide hormone. N. Phytol. 215, 725–736 (2017).

    CAS  Google Scholar 

  152. Liu, F. et al. Variation and inheritance of the Xanthomonas raxX–raxSTAB gene cluster required for activation of XA21-mediated immunity. Mol. Plant. Pathol. 20, 656–672 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  153. Tai, T. H. et al. Expression of the Bs2 pepper gene confers resistance to bacterial spot disease in tomato. Proc. Natl Acad. Sci. USA 96, 14153–14158 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  154. Wang, G. et al. The decoy substrate of a pathogen effector and a pseudokinase specify pathogen-induced modified-self recognition and immunity in plants. Cell Host Microbe 18, 285–295 (2015).

    CAS  PubMed  Google Scholar 

  155. Kearney, B. & Staskawicz, B. J. Characterization of IS476 and its role in bacterial spot disease of tomato and pepper. J. Bacteriol. 172, 143–148 (1990).

    CAS  PubMed  PubMed Central  Google Scholar 

  156. Kousik, C. & Ritchie, D. F. Race shift in Xanthomonas campestris pv. vesicatoria within a season in field-grown pepper. Phytopathology 86, 952 (1996).

    Google Scholar 

  157. Vera Cruz, C. M. et al. Predicting durability of a disease resistance gene based on an assessment of the fitness loss and epidemiological consequences of avirulence gene mutation. Proc. Natl Acad. Sci. USA 97, 13500–13505 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  158. Gassmann, W. et al. Molecular evolution of virulence in natural field strains of Xanthomonas campestris pv. vesicatoria. J. Bacteriol. 182, 7053–7059 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  159. Swords, K. M., Dahlbeck, D., Kearney, B., Roy, M. & Staskawicz, B. J. Spontaneous and induced mutations in a single open reading frame alter both virulence and avirulence in Xanthomonas campestris pv. vesicatoria avrBs2. J. Bacteriol. 178, 4661–4669 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  160. Read, A. C. et al. Suppression of Xo1-mediated disease resistance in rice by a truncated, non-DNA-binding TAL effector of Xanthomonas oryzae. Front. Plant Sci. 7, 1516 (2016).

    PubMed  PubMed Central  Google Scholar 

  161. Jones, J. B. et al. A non-hypersensitive resistance in pepper to the bacterial spot pathogen is associated with two recessive genes. Phytopathology 92, 273–277 (2002).

    CAS  PubMed  Google Scholar 

  162. Schornack, S., Minsavage, G. V., Stall, R. E., Jones, J. B. & Lahaye, T. Characterization of AvrHah1, a novel AvrBs3-like effector from Xanthomonas gardneri with virulence and avirulence activity. N. Phytol. 179, 546–556 (2008).

    CAS  Google Scholar 

  163. Narvel, J. M. et al. Molecular mapping of Rxp conditioning reaction to bacterial pustule in soybean. J. Hered. 92, 267–270 (2001).

    CAS  PubMed  Google Scholar 

  164. Chu, Z. et al. Promoter mutations of an essential gene for pollen development result in disease resistance in rice. Genes. Dev. 20, 1250–1255 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  165. Huang, S. et al. The broadly effective recessive resistance gene xa5 of rice is a virulence effector-dependent quantitative trait for bacterial blight. Plant. J. 86, 186–194 (2016).

    CAS  PubMed  Google Scholar 

  166. Kunwar, S. et al. Transgenic expression of EFR and Bs2 genes for field management of bacterial wilt and bacterial spot of tomato. Phytopathology 108, 1402–1411 (2018).

    CAS  PubMed  Google Scholar 

  167. Sun, L. et al. Citrus genetic engineering for disease resistance: past, present and future. Int. J. Mol. Sci. 20, 5256 (2019).

    CAS  PubMed Central  Google Scholar 

  168. Blanvillain-Baufumé, S. et al. Targeted promoter editing for rice resistance to Xanthomonas oryzae pv. oryzae reveals differential activities for SWEET14-inducing TAL effectors. Plant. Biotechnol. J. 15, 306–317 (2017).

    PubMed  Google Scholar 

  169. Li, T., Liu, B., Spalding, M. H., Weeks, D. P. & Yang, B. High-efficiency TALEN-based gene editing produces disease-resistant rice. Nat. Biotechnol. 30, 390–392 (2012).

    CAS  PubMed  Google Scholar 

  170. Shantharaj, D. et al. An engineered promoter driving expression of a microbial avirulence gene confers recognition of TAL effectors and reduces growth of diverse Xanthomonas strains in citrus. Mol. Plant. Pathol. 18, 976–989 (2017).

    CAS  PubMed  Google Scholar 

  171. Page, A. J. et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 31, 3691–3693 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  172. Boch, J., Bonas, U. & Lahaye, T. TAL effectors — pathogen strategies and plant resistance engineering. N. Phytol. 204, 823–832 (2014).

    CAS  Google Scholar 

  173. Richter, A. et al. A TAL effector repeat architecture for frameshift binding. Nat. Commun. 5, 1–10 (2014).

    Google Scholar 

  174. Pérez-Quintero, A. L. et al. An improved method for TAL effectors DNA-binding sites prediction reveals functional convergence in TAL repertoires of Xanthomonas oryzae strains. PLOS ONE 8, e68464 (2013).

    PubMed  PubMed Central  Google Scholar 

  175. Wernham, C. C. The species value of pathogenicity in the genus Xanthomonas. Phytopathology 38, 283–291 (1948).

    Google Scholar 

  176. Hajri, A. et al. A ‘repertoire for repertoire’ hypothesis: repertoires of type three effectors are candidate determinants of host specificity in Xanthomonas. PLOS ONE 4, e6632 (2009).

    PubMed  PubMed Central  Google Scholar 

  177. Figueiredo, J. F. L., Minsavage, G. V., Graham, J. H., White, F. F. & Jones, J. B. Mutational analysis of type III effector genes from Xanthomonas citri subsp. citri. Eur. J. Plant. Pathol. 130, 339–347 (2011).

    CAS  Google Scholar 

  178. Lu, H. et al. Acquisition and evolution of plant pathogenesis-associated gene clusters and candidate determinants of tissue-specificity in Xanthomonas. PLOS ONE 3, e3828 (2008).

    PubMed  PubMed Central  Google Scholar 

  179. Jacobs, J. M. et al. Evolutionary and biological basis of Xanthomonas systemic pathogenesis of plants [abstract 347-P]. Phytopathology 107, S5.1. (2017).

  180. Karasov, T. L. et al. Arabidopsis thaliana and Pseudomonas pathogens exhibit stable associations over evolutionary timescales. Cell Host Microbe 24, 168–179.e4 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  181. Salanoubat, M. et al. Genome sequence of the plant pathogen Ralstonia solanacearum. Nature 415, 497–502 (2002).

    CAS  PubMed  Google Scholar 

  182. Wu, D. et al. A plant pathogen type III effector protein subverts translational regulation to boost host polyamine levels. Cell Host Microbe 26, 638–649 (2019).

    CAS  PubMed  Google Scholar 

  183. Pérez-Quintero, A. L. et al. daTALbase: a database for genomic and transcriptomic data related to TAL effectors. Mol. Plant. Microbe Interact. 31, 471–480 (2018).

    PubMed  Google Scholar 

  184. Erkes, A., Mücke, S., Reschke, M., Boch, J. & Grau, J. PrediTALE: a novel model learned from quantitative data allows for new perspectives on TALE targeting. PLOS Comput. Biol. 15, e1007206 (2019).

    PubMed  PubMed Central  Google Scholar 

  185. Mücke, S. et al. Transcriptional reprogramming of rice cells by Xanthomonas oryzae TALEs. Front. Plant. Sci. 10, 162 (2019).

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors acknowledge A. M. Gochez and M. M. Shimwela for the images of Xanthomonas disease symptoms in citrus and banana, respectively.

Author information

Authors and Affiliations

Authors

Contributions

The authors contributed equally to all aspects of the article.

Corresponding authors

Correspondence to Erica M. Goss or Jeffrey B. Jones.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information

Nature Reviews Microbiology thanks Jian-Min Zhou and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Related links

Overview of T3SEs in Xanthomonas Resource: http://xanthomonas.org/t3e.html

Supplementary information

Glossary

Vascular tissue

Tissue involved in transporting nutrients and fluids in plants. The primary components include xylem and phloem.

Mesophyll tissue

Leaf tissue between the epidermis layers that carries out photosynthesis.

Recombination

Genetic exchange between bacteria resulting in the incorporation of homologous and non-homologous sequences.

Type III secretion system

(T3SS). A secretion system composed of ~20 proteins that forms a syringe-like structure to deliver bacterial proteins to eukaryotic cells. Also referred to as the injectisome.

Effector-triggered immunity

(ETI). Innate immune response triggered by recognition of the type III translocated effector proteins by host resistance gene products.

Type II secretion system

(T2SS). A secretion system formed by secretin proteins, which form characteristic β-barrels for passage of secreted proteins.

Type VI secretion system

(T6SS). A secretion system that delivers bacterial proteins across a cellular envelope to adjacent target cells. Primarily known for interbacterial antagonism.

Hypersensitive response

A response mechanism found in plant hosts, characterized typically by a rapid cell death to prevent the spread of the pathogen.

Accessions

Groups of related plant material from the same species collected from a specific location. The accessions are collections to capture the diversity in a given plant species.

Pathogen or damage-associated molecular pattern (P/DAMP)-triggered immunity

(PTI/DTI). PTI refers to the immune response in hosts triggered by recognizing patterns associated with pathogen, for example, flagellin or lipopolysaccharide. DTI refers to the host immune response triggered as a result of recognition of cell wall-degradation products that are generated by the action of pathogen-secreted cell wall-degrading enzymes during pathogen invasion. PTI and DTI pathways have a significant overlap in their signalling components.

Receptor-like cytoplasmic kinases

Kinase-mediated signalling proteins that regulate plant cellular activities in response to biotic or abiotic stresses and endogenous extracellular signalling molecules.

Receptor-like kinase superfamily

Transmembrane proteins with versatile amino-terminal extracellular domains and carboxy-terminal intracellular kinases. They control a wide range of physiological responses in plants and belong to one of the largest gene families in the Arabidopsis thaliana genome, with more than 600 members.

MAPK

Protein kinases involved in regulating cellular responses to an extensive array of stimuli, including mitogens, heat shock and stress. Specific to serine and threonine amino acids.

Protoplast

The entire cell excluding the cell wall.

SWEET genes

Sugar will eventually be exported transporter (SWEET) genes encode membrane proteins with diverse function, typically facilitating sucrose and glucose efflux.

Recessive resistance

Resistance conferred by recessive allele of a gene in a plant host. The term is also used to refer to resistance conferred by mutation in disease-susceptibility genes.

Abscisic acid

A plant hormone with numerous functions in the plant developmental process, including dormancy and stress response.

Nucleotide binding, leucine-rich repeat (NLR) resistance genes

Resistance genes named after their characteristic nucleotide binding and leucine-rich repeat domains.

Two-component system

(TCS). Mediators of signal transduction in bacteria to detect the surrounding changes and relay the signal for modulating gene expression.

Pathogenic races

Groups of strains that belong to the same or closely related bacterial species, characterized by differential responses (compatible or incompatible reaction) on an array of hosts.

Dominant resistance

Resistance conferred by a single dominant resistance gene in plant hosts.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Timilsina, S., Potnis, N., Newberry, E.A. et al. Xanthomonas diversity, virulence and plant–pathogen interactions. Nat Rev Microbiol 18, 415–427 (2020). https://doi.org/10.1038/s41579-020-0361-8

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41579-020-0361-8

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing