1932

Abstract

Among plant-associated bacteria, agrobacteria occupy a special place. These bacteria are feared in the field as agricultural pathogens. They cause abnormal growth deformations and significant economic damage to a broad range of plant species. However, these bacteria are revered in the laboratory as models and tools. They are studied to discover and understand basic biological phenomena and used in fundamental plant research and biotechnology. Agrobacterial pathogenicity and capability for transformation are one and the same and rely on functions encoded largely on their oncogenic plasmids. Here, we synthesize a substantial body of elegant work that elucidated agrobacterial virulence mechanisms and described their ecology. We review findings in the context of the natural diversity that has been recently unveiled for agrobacteria and emphasize their genomics and plasmids. We also identify areas of research that can capitalize on recent findings to further transform our understanding of agrobacterial virulence and ecology.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-phyto-021622-125009
2023-09-05
2024-12-04
Loading full text...

Full text loading...

/deliver/fulltext/phyto/61/1/annurev-phyto-021622-125009.html?itemId=/content/journals/10.1146/annurev-phyto-021622-125009&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Aktas M, Danne L, Möller P, Narberhaus F. 2014. Membrane lipids in Agrobacterium tumefaciens: biosynthetic pathways and importance for pathogenesis. Front. Plant Sci. 5:109
    [Google Scholar]
  2. 2.
    Amro J, Black C, Jemouai Z, Rooney N, Daneault C et al. 2022. Cryo-EM structure of the Agrobacterium tumefaciens T-pilus reveals the importance of positive charges in the lumen. Structure 314P375–84.E4
    [Google Scholar]
  3. 3.
    Anderson AR. 1979. Host specificity in the genus Agrobacterium. Phytopathology 69:4320–23
    [Google Scholar]
  4. 4.
    Atmakuri K, Cascales E, Burton OT, Banta LM, Christie PJ. 2007. Agrobacterium ParA/MinD-like VirC1 spatially coordinates early conjugative DNA transfer reactions. EMBO J. 26:102540–51
    [Google Scholar]
  5. 5.
    Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y et al. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2:2006.0008
    [Google Scholar]
  6. 6.
    Bhattacharjee S, Lee L-Y, Oltmanns H, Cao H, Veena et al. 2008. IMPa-4, an Arabidopsis importin α isoform, is preferentially involved in Agrobacterium-mediated plant transformation. Plant Cell 20:102661–80
    [Google Scholar]
  7. 7.
    Büttner D. 2016. Behind the lines—actions of bacterial type III effector proteins in plant cells. FEMS Microbiol. Rev. 40:6894–937
    [Google Scholar]
  8. 8.
    Cangelosi GA, Ankenbauer RG, Nester EW. 1990. Sugars induce the Agrobacterium virulence genes through a periplasmic binding protein and a transmembrane signal protein. PNAS 87:176708–12
    [Google Scholar]
  9. 9.
    Cascales E, Christie PJ. 2004. Definition of a bacterial type IV secretion pathway for a DNA substrate. Science 304:56741170–73
    [Google Scholar]
  10. 10.
    Chou L, Lin Y-C, Haryono M, Santos MNM, Cho S-T et al. 2022. Modular evolution of secretion systems and virulence plasmids in a bacterial species complex. BMC Biol. 20:116
    [Google Scholar]
  11. 11.
    Cleene MD, Ley JD. 1976. The host range of crown gall. Bot. Rev. 42:4389–466
    [Google Scholar]
  12. 12.
    Costechareyre D, Rhouma A, Lavire C, Portier P, Chapulliot D et al. 2010. Rapid and efficient identification of Agrobacterium species by recA allele analysis: Agrobacterium recA diversity. Microb. Ecol. 60:4862–72
    [Google Scholar]
  13. 13.
    Coulthurst S. 2019. The type VI secretion system: a versatile bacterial weapon. Microbiology 165:5503–15
    [Google Scholar]
  14. 14.
    de Lajudie PM, Andrews M, Ardley J, Eardly B, Jumas-Bilak E et al. 2019. Minimal standards for the description of new genera and species of rhizobia and agrobacteria. Int. J. Syst. Evol. Microbiol. 69:71852–63
    [Google Scholar]
  15. 15.
    Deakin WJ, Broughton WJ. 2009. Symbiotic use of pathogenic strategies: rhizobial protein secretion systems. Nat. Rev. Microbiol. 7:4312–20
    [Google Scholar]
  16. 16.
    Deeken R, Engelmann JC, Efetova M, Czirjak T, Müller T et al. 2006. An integrated view of gene expression and solute profiles of Arabidopsis tumors: a genome-wide approach. Plant Cell 18:123617–34
    [Google Scholar]
  17. 17.
    Dequivre M, Diel B, Villard C, Sismeiro O, Durot M et al. 2015. Small RNA deep-sequencing analyses reveal a new regulator of virulence in Agrobacterium fabrum C58. Mol. Plant-Microbe Interact. 28:5580–89
    [Google Scholar]
  18. 18.
    Dessaux Y, Petit A, Farrand SK, Murphy PJ 1998. Opines and opine-like molecules involved in plant-Rhizobiaceae interactions. The Rhizobiaceae: Molecular Biology of Model Plant-Associated Bacteria HP Spaink, A Kondorosi, PJJ Hooykaas 173–97. Dordrecht, Neth: Springer
    [Google Scholar]
  19. 19.
    Douglas CJ, Staneloni RJ, Rubin RA, Nester EW. 1985. Identification and genetic analysis of an Agrobacterium tumefaciens chromosomal virulence region. J. Bacteriol. 161:3850–60
    [Google Scholar]
  20. 20.
    Ellis JG. 2017. Can plant microbiome studies lead to effective biocontrol of plant diseases?. Mol. Plant-Microbe Interact. 30:3190–93
    [Google Scholar]
  21. 21.
    Faist H, Keller A, Hentschel U, Deeken R. 2016. Grapevine (Vitis vinifera) crown galls host distinct microbiota. Appl. Environ. Microbiol. 82:185542–52
    [Google Scholar]
  22. 22.
    Felix G, Duran JD, Volko S, Boller T. 1999. Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 18:3265–76
    [Google Scholar]
  23. 23.
    Fuller SL, Savory EA, Weisberg AJ, Buser JZ, Gordon MI et al. 2017. Isothermal amplification and lateral-flow assay for detecting crown-gall-causing Agrobacterium spp. Phytopathology 107:91062–68
    [Google Scholar]
  24. 24.
    Fürst U, Zeng Y, Albert M, Witte AK, Fliegmann J, Felix G. 2020. Perception of Agrobacterium tumefaciens flagellin by FLS2XL confers resistance to crown gall disease. Nat. Plants 6:122–27
    [Google Scholar]
  25. 25.
    Gan HM, Szegedi E, Fersi R, Chebil S, Kovács L et al. 2019. Insight into the microbial co-occurrence and diversity of 73 grapevine (Vitis vinifera) crown galls collected across the Northern Hemisphere. Front. Microbiol. 10:1896
    [Google Scholar]
  26. 26.
    García-Cano E, Hak H, Magori S, Lazarowitz SG, Citovsky V. 2018. The Agrobacterium F-box protein effector VirF destabilizes the Arabidopsis GLABROUS1 enhancer/binding protein-like transcription factor VFP4, a transcriptional activator of defense response genes. Mol. Plant-Microbe Interact. 31:5576–86
    [Google Scholar]
  27. 27.
    Garfinkel DJ, Nester EW. 1980. Agrobacterium tumefaciens mutants affected in crown gall tumorigenesis and octopine catabolism. J. Bacteriol. 144:2732–43
    [Google Scholar]
  28. 28.
    Garza I, Christie PJ. 2013. A putative transmembrane leucine zipper of Agrobacterium VirB10 is essential for T-pilus biogenesis but not type IV secretion. J. Bacteriol. 195:133022–34
    [Google Scholar]
  29. 29.
    Goodner B, Hinkle G, Gattung S, Miller N, Blanchard M et al. 2001. Genome sequence of the plant pathogen and biotechnology agent Agrobacterium tumefaciens C58. Science 294:55502323–28
    [Google Scholar]
  30. 30.
    Groenewold MK, Hebecker S, Fritz C, Czolkoss S, Wiesselmann M et al. 2019. Virulence of Agrobacterium tumefaciens requires lipid homeostasis mediated by the lysyl-phosphatidylglycerol hydrolase AcvB. Mol. Microbiol. 111:1269–86
    [Google Scholar]
  31. 31.
    Guidolin LS, Arce-Gorvel V, Ciocchini AE, Comerci DJ, Gorvel J-P. 2018. Cyclic β-glucans at the bacteria-host cells interphase: one sugar ring to rule them all. Cell Microbiol. 20:6e12850
    [Google Scholar]
  32. 32.
    Guo M, Hou Q, Hew CL, Pan SQ. 2007. Agrobacterium VirD2-binding protein is involved in tumorigenesis and redundantly encoded in conjugative transfer gene clusters. Mol. Plant-Microbe Interact. 20:101201–12
    [Google Scholar]
  33. 33.
    Hachani A, Wood TE, Filloux A. 2016. Type VI secretion and anti-host effectors. Curr. Opin. Microbiol. 29:81–93
    [Google Scholar]
  34. 34.
    Harrison PW, Lower RPJ, Kim NKD, Young JPW. 2010. Introducing the bacterial ‘chromid’: not a chromosome, not a plasmid. Trends Microbiol. 18:4141–48
    [Google Scholar]
  35. 35.
    Haryono M, Cho S-T, Fang M-J, Chen A-P, Chou S-J et al. 2019. Differentiations in gene content and expression response to virulence induction between two Agrobacterium strains. Front. Microbiol. 10:1554
    [Google Scholar]
  36. 36.
    Haryono M, Tsai Y-M, Lin C-T, Huang F-C, Ye Y-C et al. 2018. Presence of an Agrobacterium-type tumor-inducing plasmid in Neorhizobium sp. NCHU2750 and the link to phytopathogenicity. Genome Biol. Evol. 10:123188–95
    [Google Scholar]
  37. 37.
    Heckel BC, Tomlinson AD, Morton ER, Choi J-H, Fuqua C. 2014. Agrobacterium tumefaciens ExoR controls acid response genes and impacts exopolysaccharide synthesis, horizontal gene transfer, and virulence gene expression. J. Bacteriol. 196:183221–33
    [Google Scholar]
  38. 38.
    Heindl JE, Wang Y, Heckel BC, Mohari B, Feirer N, Fuqua C. 2014. Mechanisms and regulation of surface interactions and biofilm formation in Agrobacterium. Front. Plant Sci. 5:176
    [Google Scholar]
  39. 39.
    Herrera-Estrella A, Chen ZM, Van Montagu M, Wang K. 1988. VirD proteins of Agrobacterium tumefaciens are required for the formation of a covalent DNA-protein complex at the 5′ terminus of T-strand molecules. EMBO J. 7:134055–62
    [Google Scholar]
  40. 40.
    Hodges LD, Cuperus J, Ream W. 2004. Agrobacterium rhizogenes GALLS protein substitutes for Agrobacterium tumefaciens single-stranded DNA-binding protein VirE2. J. Bacteriol. 186:103065–77
    [Google Scholar]
  41. 41.
    Hooykaas MJG, Hooykaas PJJ. 2021. Complete genomic sequence and phylogenomics analysis of Agrobacterium strain AB2/73: a new Rhizobium species with a unique mega-Ti plasmid. BMC Microbiol. 21:1295
    [Google Scholar]
  42. 42.
    Hwang H-H, Wang M-H, Lee Y-L, Tsai Y-L, Li Y-H et al. 2010. Agrobacterium-produced and exogenous cytokinin-modulated Agrobacterium-mediated plant transformation. Mol. Plant Pathol. 11:5677–90
    [Google Scholar]
  43. 43.
    Hwang H-H, Wu ET, Liu S-Y, Chang S-C, Tzeng K-C, Kado CI. 2013. Characterization and host range of five tumorigenic Agrobacterium tumefaciens strains and possible application in plant transient transformation assays. Plant Pathol. 62:61384–97
    [Google Scholar]
  44. 44.
    Hwang H-H, Yu M, Lai E-M 2017. Agrobacterium-mediated plant transformation: biology and applications. Arabidopsis Book 15:e0186
    [Google Scholar]
  45. 45.
    Iyer VN, Klee HJ, Nester EW. 1982. Units of genetic expression in the virulence region of a plant tumor-inducing plasmid of Agrobacterium tumefaciens. Mol. Gen. Genet. 188:3418–24
    [Google Scholar]
  46. 46.
    Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S 2018. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat. Commun. 9:15114
    [Google Scholar]
  47. 47.
    Jones JDG, Dangl JL. 2006. The plant immune system. Nature 444:7117323–29
    [Google Scholar]
  48. 48.
    Kado CI. 2014. Historical account on gaining insights on the mechanism of crown gall tumorigenesis induced by Agrobacterium tumefaciens. Front. Microbiol. 5:340
    [Google Scholar]
  49. 49.
    Kao JC, Perry KL, Kado CI. 1982. Indoleacetic acid complementation and its relation to host range specifying genes on the Ti plasmid of Agrobacterium tumefaciens. Mol. Gen. Genet. 188:3425–32
    [Google Scholar]
  50. 50.
    Knauf VC. 1982. Genetic factors controlling the host range of Agrobacterium tumefaciens. Phytopathology 72:121545–49
    [Google Scholar]
  51. 51.
    Kuzmanović N, Biondi E, Overmann J, Puławska J, Verbarg S et al. 2022. Genomic analysis provides novel insights into diversification and taxonomy of Allorhizobium vitis (i.e., Agrobacterium vitis). BMC Genom. 23:1462
    [Google Scholar]
  52. 52.
    Kuzmanović N, Puławska J. 2019. Evolutionary relatedness and classification of tumor-inducing and opine-catabolic plasmids in three Rhizobium rhizogenes strains isolated from the same crown gall tumor. Genome Biol. Evol. 11:61525–40
    [Google Scholar]
  53. 53.
    Kuzmanović N, Puławska J, Smalla K, Nesme X. 2018. Agrobacterium rosae sp. nov., isolated from galls on different agricultural crops. Syst. Appl. Microbiol. 41:3191–97
    [Google Scholar]
  54. 54.
    Kuzmanović N, Smalla K, Gronow S, Puławska J. 2018. Rhizobium tumorigenes sp. nov., a novel plant tumorigenic bacterium isolated from cane gall tumors on thornless blackberry. Sci. Rep. 8:19051
    [Google Scholar]
  55. 55.
    Lacroix B, Citovsky V. 2016. A functional bacterium-to-plant DNA transfer machinery of Rhizobium etli. PLOS Pathog. 12:3e1005502
    [Google Scholar]
  56. 56.
    Lai E-M, Chesnokova O, Banta LM, Kado CI. 2000. Genetic and environmental factors affecting T-pilin export and T-pilus biogenesis in relation to flagellation of Agrobacterium tumefaciens. J. Bacteriol. 182:133705–16
    [Google Scholar]
  57. 57.
    Lai E-M, Kado CI. 2000. The T-pilus of Agrobacterium tumefaciens. Trend Microbiol. 8:8361–69
    [Google Scholar]
  58. 58.
    Lassalle F, Campillo T, Vial L, Baude J, Costechareyre D et al. 2011. Genomic species are ecological species as revealed by comparative genomics in Agrobacterium tumefaciens. Genome Biol. Evol. 3:762–81
    [Google Scholar]
  59. 59.
    Lassalle F, Planel R, Penel S, Chapulliot D, Barbe V et al. 2017. Ancestral genome estimation reveals the history of ecological diversification in Agrobacterium. Genome Biol. Evol. 9:123413–31
    [Google Scholar]
  60. 60.
    Lee K, Huang X, Yang C, Lee D, Ho V et al. 2013. A genome-wide survey of highly expressed non-coding RNAs and biological validation of selected candidates in Agrobacterium tumefaciens. PLOS ONE 8:8e70720
    [Google Scholar]
  61. 61.
    Lee YW, Jin S, Sim WS, Nester EW 1995. Genetic evidence for direct sensing of phenolic compounds by the VirA protein of Agrobacterium tumefaciens. PNAS 92:2612245–49
    [Google Scholar]
  62. 62.
    Li L, Jia Y, Hou Q, Charles TC, Nester EW, Pan SQ. 2002. A global pH sensor: Agrobacterium sensor protein ChvG regulates acid-inducible genes on its two chromosomes and Ti plasmid. PNAS 99:1912369–74
    [Google Scholar]
  63. 63.
    Li X, Yang Q, Peng L, Tu H, Lee L-Y et al. 2020. Agrobacterium-delivered VirE2 interacts with host nucleoporin CG1 to facilitate the nuclear import of VirE2-coated T complex. PNAS 117:4226389–97
    [Google Scholar]
  64. 64.
    Li YG, Hu B, Christie PJ. 2019. Biological and structural diversity of type IV secretion systems. Microbiol. Spectr. 7:230
    [Google Scholar]
  65. 65.
    Liao Q, Ren Z, Wiesler EE, Fuqua C, Wang X. 2022. A dicentric bacterial chromosome requires XerC/D site-specific recombinases for resolution. Curr. Biol. 32:163609–18.e7
    [Google Scholar]
  66. 66.
    Lien Y-W, Lai E-M. 2017. Type VI secretion effectors: methodologies and biology. Front. Cell. Infect. Microbiol. 7:254
    [Google Scholar]
  67. 67.
    Lin B-C, Kado CI. 1977. Studies on Agrobacterium tumefaciens. VII. Avirulence induced by temperature and ethidium bromide. Can. J. Microbiol. 23:111554–61
    [Google Scholar]
  68. 68.
    Lin H-H, Yu M, Sriramoju MK, Hsu S-TD, Liu C-T, Lai E-M. 2020. A high-throughput interbacterial competition screen identifies ClpAP in enhancing recipient susceptibility to type VI secretion system-mediated attack by Agrobacterium tumefaciens. Front. Microbiol. 10:3077
    [Google Scholar]
  69. 69.
    Lindström K, Young JPW. 2011. International Committee on Systematics of Prokaryotes Subcommittee on the taxonomy of Agrobacterium and Rhizobium: minutes of the meeting, 7 September 2010, Geneva, Switzerland. Int. J. Syst. Evol. Microbiol. 61:123089–93
    [Google Scholar]
  70. 70.
    Liu P, Wood D, Nester EW. 2005. Phosphoenolpyruvate carboxykinase is an acid-induced, chromosomally encoded virulence factor in Agrobacterium tumefaciens. J. Bacteriol. 187:176039–45
    [Google Scholar]
  71. 71.
    Loper JE, Kado CI. 1979. Host range conferred by the virulence-specifying plasmid of Agrobacterium tumefaciens. J. Bacteriol. 139:2591–96
    [Google Scholar]
  72. 72.
    Lu J, den Dulk-Ras A, Hooykaas PJJ, Glover JNM. 2009. Agrobacterium tumefaciens VirC2 enhances T-DNA transfer and virulence through its C-terminal ribbon-helix-helix DNA-binding fold. PNAS 106:249643–48
    [Google Scholar]
  73. 73.
    Ma L-S, Hachani A, Lin J-S, Filloux A, Lai E-M. 2014. Agrobacterium tumefaciens deploys a superfamily of type VI secretion DNase effectors as weapons for interbacterial competition in planta. Cell Host Microbe 16:194–104
    [Google Scholar]
  74. 74.
    Macé K, Vadakkepat AK, Redzej A, Lukoyanova N, Oomen C et al. 2022. Cryo-EM structure of a type IV secretion system. Nature 607:7917191–96
    [Google Scholar]
  75. 75.
    Matthysse AG. 2014. Attachment of Agrobacterium to plant surfaces. Front. Plant Sci. 5:252
    [Google Scholar]
  76. 76.
    Matthysse AG, Marry M, Krall L, Kaye M, Ramey BE et al. 2005. The effect of cellulose overproduction on binding and biofilm formation on roots by Agrobacterium tumefaciens. Mol. Plant-Microbe Interact. 18:91002–10
    [Google Scholar]
  77. 77.
    Möller P, Overlöper A, Förstner KU, Wen T-N, Sharma CM et al. 2014. Profound impact of Hfq on nutrient acquisition, metabolism and motility in the plant pathogen Agrobacterium tumefaciens. PLOS ONE 9:10e110427
    [Google Scholar]
  78. 78.
    Moore LW, Warren G. 1979. Agrobacterium radiobacter strain 84 and biological control of crown gall. Annu. Rev. Phytopathol. 17:163–79
    [Google Scholar]
  79. 79.
    Morris CE, Moury B. 2019. Revisiting the concept of host range of plant pathogens. Annu. Rev. Phytopathol. 57:63–90
    [Google Scholar]
  80. 80.
    Mougel C, Thioulouse J, Perrière G, Nesme X. 2002. A mathematical method for determining genome divergence and species delineation using AFLP. Int. J. Syst. Evol. Microbiol. 52:2573–86
    [Google Scholar]
  81. 81.
    Mousavi SA, Österman J, Wahlberg N, Nesme X, Lavire C et al. 2014. Phylogeny of the Rhizobium-Allorhizobium-Agrobacterium clade supports the delineation of Neorhizobium gen. nov. Syst. Appl. Microbiol. 37:3208–15
    [Google Scholar]
  82. 82.
    Mousavi SA, Willems A, Nesme X, de Lajudie P, Lindström K. 2015. Revised phylogeny of Rhizobiaceae: proposal of the delineation of Pararhizobium gen. nov., and 13 new species combinations. Syst. Appl. Microbiol. 38:284–90
    [Google Scholar]
  83. 83.
    Mozo T, Hooykaas JJ. 1992. Factors affecting the rate of T-DNA transfer from Agrobacterium tumefaciens to Nicotiana glauca plant cells. Plant Mol. Biol. 19:61019–30
    [Google Scholar]
  84. 84.
    Nabi N, Ben Hafsa A, Gaillard V, Nesme X, Chaouachi M, Vial L. 2022. Evolutionary classification of tumor- and root-inducing plasmids based on T-DNAs and virulence regions. Mol. Phylogenet. Evol. 169:107388
    [Google Scholar]
  85. 85.
    Nautiyal CS, Dion P. 1990. Characterization of the opine-utilizing microflora associated with samples of soil and plants. Appl. Environ. Microbiol. 56:82576–79
    [Google Scholar]
  86. 86.
    Nester EW. 2015. Agrobacterium: nature's genetic engineer. Front. Plant Sci. 5:730
    [Google Scholar]
  87. 87.
    Ooms G, Hooykaas PJ, Moolenaar G, Schilperoort RA. 1981. Grown gall plant tumors of abnormal morphology, induced by Agrobacterium tumefaciens carrying mutated octopine Ti plasmids; analysis of T-DNA functions. Gene 14:1–233–50
    [Google Scholar]
  88. 88.
    Ophel K, Kerr A. 1990. Agrobacterium vitis sp. nov. for strains of Agrobacterium biovar 3 from grapevines. Int. J. Syst. Bacteriol. 40:3236–41
    [Google Scholar]
  89. 89.
    Ormeño-Orrillo E, Servín-Garcidueñas LE, Rogel MA, González V, Peralta H et al. 2015. Taxonomy of rhizobia and agrobacteria from the Rhizobiaceae family in light of genomics. Syst. Appl. Microbiol. 38:4287–91
    [Google Scholar]
  90. 90.
    Otten L. 2021. T-DNA regions from 350 Agrobacterium genomes: maps and phylogeny. Plant Mol. Biol. 106:3239–58
    [Google Scholar]
  91. 91.
    Otten L, Burr T, Szegedi E 2008. Agrobacterium: a disease-causing bacterium. Agrobacterium: From Biology to Biotechnology T Tzfira, V Citovsky 1–46. New York: Springer
    [Google Scholar]
  92. 92.
    Otten L, Canaday J, Gérard J-C, Fournier P, Crouzet P, Paulus F. 1992. Evolution of agrobacteria and their Ti plasmids: a review. Mol. Plant-Microbe Interact. 5:4279–87
    [Google Scholar]
  93. 93.
    Palumbo JD, Phillips DA, Kado CI. 1998. Characterization of a new Agrobacterium tumefaciens strain from alfalfa (Medicago sativa L.). Arch. Microbiol. 169:5381–86
    [Google Scholar]
  94. 94.
    Pan SQ, Jin S, Boulton MI, Hawes M, Gordon MP, Nester EW 1995. An Agrobacterium virulence factor encoded by a Ti plasmid gene or a chromosomal gene is required for T-DNA transfer into plants. Mol. Microbiol. 17:2259–69
    [Google Scholar]
  95. 95.
    Parkhill J, Sebaihia M, Preston A, Murphy LD, Thomson N et al. 2003. Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nat. Genet. 35:132–40
    [Google Scholar]
  96. 96.
    Popoff MY, Kersters K, Kiredjian M, Miras I, Coynault C. 1984. Position taxonomique de souches de Agrobacterium d'origine hospitalière. Ann. Inst. Pasteur Microbiol. 135:3, Suppl. A427–42
    [Google Scholar]
  97. 97.
    Raja I, Kumar V, Sabapathy H, Kumariah M, Rajendran K, Tennyson J. 2018. Prediction and identification of novel sRNAs involved in Agrobacterium strains by integrated genome-wide and transcriptome-based methods. FEMS Microbiol. Lett. 365:23fny247
    [Google Scholar]
  98. 98.
    Raman V, Rojas CM, Vasudevan B, Dunning K, Kolape J et al. 2022. Agrobacterium expressing a type III secretion system delivers Pseudomonas effectors into plant cells to enhance transformation. Nat. Commun. 13:12581
    [Google Scholar]
  99. 99.
    Ramírez-Bahena MH, Vial L, Lassalle F, Diel B, Chapulliot D et al. 2014. Single acquisition of protelomerase gave rise to speciation of a large and diverse clade within the Agrobacterium/Rhizobium supercluster characterized by the presence of a linear chromid. Mol. Phylogenet. Evol. 73:202–7
    [Google Scholar]
  100. 100.
    Ream W. 2009. Agrobacterium tumefaciens and A. rhizogenes use different proteins to transport bacterial DNA into the plant cell nucleus. Microb. Biotechnol. 2:4416–27
    [Google Scholar]
  101. 101.
    Ren Z, Liao Q, Barton IS, Wiesler EE, Fuqua C, Wang X. 2022. Centromere interactions promote the maintenance of the multipartite genome in Agrobacterium tumefaciens. mBio 13:3e00508–22
    [Google Scholar]
  102. 102.
    Ren Z, Liao Q, Karaboja X, Barton IS, Schantz EG et al. 2022. Conformation and dynamic interactions of the multipartite genome in Agrobacterium tumefaciens. PNAS 119:6e2115854119
    [Google Scholar]
  103. 103.
    Rogowsky PM, Close TJ, Chimera JA, Shaw JJ, Kado CI. 1987. Regulation of the vir genes of Agrobacterium tumefaciens plasmid pTiC58. J. Bacteriol. 169:115101–12
    [Google Scholar]
  104. 104.
    Santos MNM, Cho S-T, Wu C-F, Chang C-J, Kuo C-H, Lai E-M. 2020. Redundancy and specificity of type VI secretion vgrG loci in antibacterial activity of Agrobacterium tumefaciens 1D1609 strain. Front. Microbiol. 10:3004
    [Google Scholar]
  105. 105.
    Shao S, van Heusden GPH, Hooykaas PJJ. 2019. Complete sequence of succinamopine Ti-plasmid pTiEU6 reveals its evolutionary relatedness with nopaline-type Ti-plasmids. Genome Biol. Evol. 11:92480–91
    [Google Scholar]
  106. 106.
    Slater SC, Goldman BS, Goodner B, Setubal JC, Farrand SK et al. 2009. Genome sequences of three Agrobacterium biovars help elucidate the evolution of multichromosome genomes in bacteria. J. Bacteriol. 191:82501–11
    [Google Scholar]
  107. 107.
    Swackhammer A, Provencher EAP, Donkor AK, Garofalo J, Dowling S et al. 2022. Mechanistic analysis of the VirA sensor kinase in Agrobacterium tumefaciens using structural models. Front. Microbiol. 13:898785
    [Google Scholar]
  108. 108.
    Thomashow MF, Karlinsey JE, Marks JR, Hurlbert RE. 1987. Identification of a new virulence locus in Agrobacterium tumefaciens that affects polysaccharide composition and plant cell attachment. J. Bacteriol. 169:73209–16
    [Google Scholar]
  109. 109.
    Thomashow MF, Panagopoulos CG, Gordon MP, Nester EW. 1980. Host range of Agrobacterium tumefaciens is determined by the Ti plasmid. Nature 283:5749794–96
    [Google Scholar]
  110. 110.
    Tomlinson AD, Ramey-Hartung B, Day TW, Merritt PM, Fuqua C. 2010. Agrobacterium tumefaciens ExoR represses succinoglycan biosynthesis and is required for biofilm formation and motility. Microbiology 156:92670–81
    [Google Scholar]
  111. 111.
    Torres M, Jiquel A, Jeanne E, Naquin D, Dessaux Y, Faure D 2022. Agrobacterium tumefaciens fitness genes involved in the colonization of plant tumors and roots. New Phytol. 233:2905–18
    [Google Scholar]
  112. 112.
    Tu H, Li X, Yang Q, Peng L, Pan SQ. 2018. Real-time trafficking of Agrobacterium virulence protein VirE2 inside host cells. Agrobacterium Biology: From Basic Science to Biotechnology SB Gelvin 261–86. Cham, Switz: Springer
    [Google Scholar]
  113. 113.
    Unger L, Ziegler SF, Huffman GA, Knauf VC, Peet R et al. 1985. New class of limited-host-range Agrobacterium mega-tumor-inducing plasmids lacking homology to the transferred DNA of a wide-host-range, tumor-inducing plasmid. J. Bacteriol. 164:2723–30
    [Google Scholar]
  114. 114.
    Velázquez E, Palomo JL, Rivas R, Guerra H, Peix A et al. 2010. Analysis of core genes supports the reclassification of strains Agrobacterium radiobacter K84 and Agrobacterium tumefaciens AKE10 into the species Rhizobium rhizogenes. Syst. Appl. Microbiol. 33:5247–51
    [Google Scholar]
  115. 115.
    Vergunst AC, Schrammeijer B, den Dulk-Ras A, de Vlaam CMT, Regensburg-Tuınk TJG, Hooykaas PJJ. 2000. VirB/D4-dependent protein translocation from Agrobacterium into plant cells. Science 290:5493979–82
    [Google Scholar]
  116. 116.
    Wang J, Brodmann M, Basler M. 2019. Assembly and subcellular localization of bacterial type VI secretion systems. Annu. Rev. Microbiol. 73:621–38
    [Google Scholar]
  117. 117.
    Wang S-C, Chen A-P, Chou S-J, Kuo C-H, Lai E-M. 2023. Soil inoculation and blocker-mediated sequencing show effects of the antibacterial T6SS on agrobacterial tumorigenesis and gallobiome. mBio 142e00177–23
    [Google Scholar]
  118. 118.
    Wang Y-C, Yu M, Shih P-Y, Wu H-Y, Lai E-M. 2018. Stable pH suppresses defense signaling and is the key to enhance Agrobacterium-mediated transient expression in Arabidopsis seedlings. Sci. Rep. 8:117071
    [Google Scholar]
  119. 119.
    Warabieda M, Mikiciński A, Oleszczak M, Puławska J. 2021. Identification of the causal agents of crazy root disease on hydroponically cultivated cucumber plants in Poland. Eur. J. Plant Pathol. 161:3543–52
    [Google Scholar]
  120. 120.
    Weisberg AJ, Davis EW, Tabima J, Belcher MS, Miller M et al. 2020. Unexpected conservation and global transmission of agrobacterial virulence plasmids. Science 368:6495eaba5256
    [Google Scholar]
  121. 121.
    Weisberg AJ, Miller M, Ream W, Grünwald NJ, Chang JH. 2022. Diversification of plasmids in a genus of pathogenic and nitrogen-fixing bacteria. Philos. Trans. R. Soc. Lond. B 377:184220200466
    [Google Scholar]
  122. 122.
    Weller SA, Stead DE, Young JPW. 2004. Acquisition of an Agrobacterium Ri plasmid and pathogenicity by other α-proteobacteria in cucumber and tomato crops affected by root mat. Appl. Environ. Microbiol. 70:52779–85
    [Google Scholar]
  123. 123.
    Wessel M, Klüsener S, Gödeke J, Fritz C, Hacker S, Narberhaus F. 2006. Virulence of Agrobacterium tumefaciens requires phosphatidylcholine in the bacterial membrane. Mol. Microbiol. 62:3906–15
    [Google Scholar]
  124. 124.
    Williams MA, Kysela DT, Brown PJB. 2022. Diversity of growth patterns in the Alphaproteobacteria. Cell Cycle Regulation and Development in Alphaproteobacteria E Biondi 185–220. Cham, Switz: Springer
    [Google Scholar]
  125. 125.
    Wilms I, Overlöper A, Nowrousian M, Sharma CM, Narberhaus F. 2012. Deep sequencing uncovers numerous small RNAs on all four replicons of the plant pathogen Agrobacterium tumefaciens. RNA Biol. 9:4446–57
    [Google Scholar]
  126. 126.
    Winans SC. 1992. Two-way chemical signaling in Agrobacterium-plant interactions. Microbiol. Rev. 56:112–31
    [Google Scholar]
  127. 127.
    Wood DW, Setubal JC, Kaul R, Monks DE, Kitajima JP et al. 2001. The genome of the natural genetic engineer Agrobacterium tumefaciens C58. Science 294:55502317–23
    [Google Scholar]
  128. 128.
    Wroblewski T, Tomczak A, Michelmore R. 2005. Optimization of Agrobacterium-mediated transient assays of gene expression in lettuce, tomato and Arabidopsis. Plant Biotechnol. J. 3:2259–73
    [Google Scholar]
  129. 129.
    Wu C-F, Lin J-S, Shaw G-C, Lai E-M. 2012. Acid-induced type VI secretion system is regulated by ExoR-ChvG/ChvI signaling cascade in Agrobacterium tumefaciens. PLOS Pathog. 8:9e1002938
    [Google Scholar]
  130. 130.
    Wu C-F, Santos MNM, Cho S-T, Chang H-H, Tsai Y-M et al. 2019. Plant-pathogenic Agrobacterium tumefaciens strains have diverse type VI effector-immunity pairs and vary in in-planta competitiveness. Mol. Plant-Microbe Interact. 32:8961–71
    [Google Scholar]
  131. 131.
    Wu C-F, Weisberg AJ, Davis EW, Chou L, Khan S et al. 2021. Diversification of the type VI secretion system in agrobacteria. mBio 12:e01927–21
    [Google Scholar]
  132. 132.
    Wu H-Y, Chen C-Y, Lai E-M. 2014. Expression and functional characterization of the Agrobacterium VirB2 amino acid substitution variants in T-pilus biogenesis, virulence, and transient transformation efficiency. PLOS ONE 9:6e101142
    [Google Scholar]
  133. 133.
    Wu H-Y, Chung P-C, Shih H-W, Wen S-R, Lai E-M. 2008. Secretome analysis uncovers an Hcp-family protein secreted via a type VI secretion system in Agrobacterium tumefaciens. J. Bacteriol. 190:82841–50
    [Google Scholar]
  134. 134.
    Yang L-L, Jiang Z, Li Y, Wang E-T, Zhi X-Y. 2020. Plasmids related to the symbiotic nitrogen fixation are not only cooperated functionally but also may have evolved over a time span in family Rhizobiaceae. Genome Biol. Evol. 12:112002–14
    [Google Scholar]
  135. 135.
    Yang S, Tang F, Gao M, Krishnan HB, Zhu H. 2010. R gene-controlled host specificity in the legume-rhizobia symbiosis. PNAS 107:4318735–40
    [Google Scholar]
  136. 136.
    Yanofsky M, Lowe B, Montoya A, Rubin R, Krul W et al. 1985. Molecular and genetic analysis of factors controlling host range in Agrobacterium tumefaciens. Mol. Gen. Genet. 201:2237–46
    [Google Scholar]
  137. 137.
    Young JM, Kerr A, Sawada H. 2015. Agrobacterium. In Bergey's Manual of Systematics of Archaea and Bacteria WB Whitman 1–15. New York: John Wiley & Sons
    [Google Scholar]
  138. 138.
    Yu M, Wang Y-C, Huang C-J, Ma L-S, Lai E-M. 2021. Agrobacterium tumefaciens deploys a versatile antibacterial strategy to increase its competitiveness. J. Bacteriol. 203:3e00490–20
    [Google Scholar]
  139. 139.
    Yuan Z-C, Edlind MP, Liu P, Saenkham P, Banta LM et al. 2007. The plant signal salicylic acid shuts down expression of the vir regulon and activates quormone-quenching genes in Agrobacterium. PNAS 104:2811790–95
    [Google Scholar]
  140. 140.
    Yuan Z-C, Liu P, Saenkham P, Kerr K, Nester EW. 2008. Transcriptome profiling and functional analysis of Agrobacterium tumefaciens reveals a general conserved response to acidic conditions (pH 5.5) and a complex acid-mediated signaling involved in Agrobacterium-plant interactions. J. Bacteriol. 190:2494–507
    [Google Scholar]
  141. 141.
    Zheng D, Burr TJ. 2013. An Sfp-type PPTase and associated polyketide and nonribosomal peptide synthases in Agrobacterium vitis are essential for induction of tobacco hypersensitive response and grape necrosis. Mol. Plant-Microbe Interact. 26:7812–22
    [Google Scholar]
  142. 142.
    Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JDG et al. 2006. Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125:4749–60
    [Google Scholar]
/content/journals/10.1146/annurev-phyto-021622-125009
Loading
/content/journals/10.1146/annurev-phyto-021622-125009
Loading

Data & Media loading...

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error