DOI: 10.1128/jb.169.5.2086-2091.1987. Common loci for Agrobacterium tumefaciens and Rhizobium meliloti exopolysaccharide synthesis and their roles in plant interactions

Common loci for Agrobacterium tumefaciens and Rhizobium meliloti exopolysaccharide synthesis and their roles in plant interactions

10.1128/jb.169.5.2086-2091.1987

Crossref journal-article

American Society for Microbiology

Journal of Bacteriology (235)

Abstract

Mutants of Rhizobium meliloti have been isolated which are deficient in exopolysaccharide (EPS) production and effective nodulation of alfalfa (J. A. Leigh, E. R. Signer, and G. C. Walker, Proc. Natl. Acad. Sci. USA 82:6231-6235, 1985). We isolated approximately 100 analogous EPS-deficient (Exo) mutants of the closely related plant pathogen Agrobacterium tumefaciens, including strains whose EPS deficiencies were specifically complemented by each of five cloned R. meliloti exo loci. We also cloned A. tumefaciens genes which complemented EPS defects in three of the R. meliloti Exo mutants. In two of these cases, symbiotic defects were also complemented. All of the A. tumefaciens Exo mutants formed normal crown gall tumors on four different plant hosts, except ExoC mutants, which were nontumorigenic and unable to attach to plant cells in vitro. Like their R. meliloti counterparts, A. tumefaciens Exo mutants were deficient in production of succinoglycan, the major acidic EPS species produced by both genera. A. tumefaciens ExoC mutants also produced extremely low levels of another major EPS, cyclic 1,2-beta-D-glucan. This deficiency has been noted previously in a different set of nontumorigenic, attachment-defective A. tumefaciens mutants.

Bibliography

Cangelosi, G. A., Hung, L., Puvanesarajah, V., Stacey, G., Ozga, D. A., Leigh, J. A., & Nester, E. W. (1987). Common loci for Agrobacterium tumefaciens and Rhizobium meliloti exopolysaccharide synthesis and their roles in plant interactions. Journal of Bacteriology, 169(5), 2086â2091.

Authors 7

G A Cangelosi (first)
L Hung (additional)
V Puvanesarajah (additional)
G Stacey (additional)
D A Ozga (additional)
J A Leigh (additional)
E W Nester (additional)

References 31 Referenced 127

Ashwell , G. 1966 . New colorimetric methods for sugar analysis . Methods Enzymol. 8 : 85 - 94 . (10.1016/0076-6879(66)08010-8) / Methods Enzymol. / New colorimetric methods for sugar analysis by Ashwell G. (1966)
Beringer , J. E. 1974 . R factor transfer in Rhizobium leguminosarum . J. Gen. Microbiol. 84 : 188 - 189 . / J. Gen. Microbiol. / R factor transfer in Rhizobium leguminosarum by Beringer J. E. (1974)
Chilton , M. - D. , M. H. Drummond , D. J. Merlo , D. Skiaky , A. L. Montoya , M. P. Gordon , and E. W. Nester . 1977 . Stable incorporation of plasmid DNA into higher plant cells: the molecular basis of crown gall tumorigenesis . Cell 11 : 263 - 271 . (10.1016/0092-8674(77)90043-5) / Cell / Stable incorporation of plasmid DNA into higher plant cells: the molecular basis of crown gall tumorigenesis by Chilton M. (1977)
Close , T. J. , R. C. Tait , and C. I. Kado . 1985 . Regulation of Ti plasmid virulence genes by a chromosomal locus of Agrobacterium tumefaciens . J. Bacteriol. 164 : 774 - 781 . (10.1128/jb.164.2.774-781.1985) / J. Bacteriol. / Regulation of Ti plasmid virulence genes by a chromosomal locus of Agrobacterium tumefaciens by Close T. J. (1985)
Deli , A. , W. S. York , M. McNeil , A. G. Darvil , and P. Albersheim . 1983 . The cyclic structure of P-D-(1,2)-linked Dglucans secreted by Rhizobia and Agrobacteria . Carbohydr. Res. 117 : 185 - 200 . (10.1016/0008-6215(83)88086-0) / Carbohydr. Res. / The cyclic structure of P-D-(1,2)-linked Dglucans secreted by Rhizobia and Agrobacteria by Deli A. (1983)
De Vos , G. F. , G. C. Walker , and E. R. Signer . 1986 . Genetic manipulations in Rhizobium meliloti utilizing two new transposon Tn 5 derivatives . Mol. Gen. Genet. 204 : 485 - 491 . (10.1007/BF00331029) / Mol. Gen. Genet. / Genetic manipulations in Rhizobium meliloti utilizing two new transposon Tn 5 derivatives by De Vos G. F. (1986)
Dische , Z. 1962 . General color reactions . Methods Carbohydr. Chem. 1 : 478 - 492 . / Methods Carbohydr. Chem. / General color reactions by Dische Z. (1962)
Douglas , C. J. , W. Halperin , and E. W. Nester . 1982 . Agrobacterium tumefaciens mutants affected in attachment to plant cells . J. Bacteriol. 152 : 1265 - 1275 . (10.1128/jb.152.3.1265-1275.1982) / J. Bacteriol. / Agrobacterium tumefaciens mutants affected in attachment to plant cells by Douglas C. J. (1982)
Douglas , C. J. , R. J. Staneloni , R. A. Rubin , and E. W. Nester . 1985 . Identification and genetic analysis of an Agrobacterium tumefaciens chromosomal virulence region . J. Bacteriol. 161 : 850 - 860 . (10.1128/jb.161.3.850-860.1985) / J. Bacteriol. / Identification and genetic analysis of an Agrobacterium tumefaciens chromosomal virulence region by Douglas C. J. (1985)
Dylan , T. , L. lelpi, S. Stanfield , L. Kashyap , C. Douglas , M. Yanofsky , E. Nester , D. R. Helinski , and G. Ditta . 1986 . Rhizobium meliloti genes required for nodule development are related to chromosomal virulence genes in Agrobacterium tumefaciens . Proc. Natl. Acad. Sci. USA 83 : 4403 4407. (10.1073/pnas.83.12.4403) / Proc. Natl. Acad. Sci. USA / Rhizobium meliloti genes required for nodule development are related to chromosomal virulence genes in Agrobacterium tumefaciens by Dylan T. (1986)
Finan , T. M. , A. M. Hirsch , J. A. Leigh , E. Johansen , G. A. Kuldau , S. Deegan , G. C. Walker , and E. R. Signer . 1985 . Symbiotic mutants of Rhizobium meliloti that uncouple plant from bacterial differentiation . Cell 40 : 869 - 877 . (10.1016/0092-8674(85)90346-0) / Cell / Symbiotic mutants of Rhizobium meliloti that uncouple plant from bacterial differentiation by Finan T. M. (1985)
Finan , T. M. , B. Kunkel , G. F. De Vos , and E. R. Signer . 1986 . Second symbiotic plasmid in Rhizobium meliloti carrying exopolysaccharide and thiamine synthetis genes . J. Bacteriol. 167 : 66 - 72 . (10.1128/jb.167.1.66-72.1986) / J. Bacteriol. / Second symbiotic plasmid in Rhizobium meliloti carrying exopolysaccharide and thiamine synthetis genes by Finan T. M. (1986)
Garfinkel , D. J. , and E. W. Nester . 1980 . Agrobacterium tumefaciens mutants affected in crown gall tumorigenesis and octopine catabolism . J. Bacteriol. 144 : 732 - 743 . (10.1128/jb.144.2.732-743.1980) / J. Bacteriol. / Agrobacterium tumefaciens mutants affected in crown gall tumorigenesis and octopine catabolism by Garfinkel D. J. (1980)
Garfinkel , D. J. , R. B. Simpson , L. W. Ream , F. F. White , M. P. Gordon , and E. W. Nester . 1981 . Genetic analysis of crown gall: fine structure map of T-DNA by site-directed mutagenesis . Cell 27 : 143 - 153 . (10.1016/0092-8674(81)90368-8) / Cell / Genetic analysis of crown gall: fine structure map of T-DNA by site-directed mutagenesis by Garfinkel D. J. (1981)
Hisamatsu , M. , J. Abe , A. Amemura , and T. Harada . 1980 . Structural elucidation of succinoglycan and related polysaccharides from Agrobacterium and Rhizobium by fragmentation with two special ,-D-glycanases and methylation analysis . Agric. Biol. Chem. 44 : 1049 - 1055 . / Agric. Biol. Chem. / Structural elucidation of succinoglycan and related polysaccharides from Agrobacterium and Rhizobium by fragmentation with two special ,-D-glycanases and methylation analysis by Hisamatsu M. (1980)
Klee , H. J. , F. F. White , V. N. Iyer , M. P. Gordon , and E. W. Nester . 1983 . Mutational analysis of the virulence region of an Agrobacterium tumefaciens Ti plasmid . J. Bacteriol. 153 : 878 - 883 . (10.1128/jb.153.2.878-883.1983) / J. Bacteriol. / Mutational analysis of the virulence region of an Agrobacterium tumefaciens Ti plasmid by Klee H. J. (1983)
Knauf , V. C. , and E. W. Nester . 1982 . Wide host range cloning vectors: a cosmid clone bank of an Agrobacterium Ti plasmid . Plasmid 8 : 45 - 54 . (10.1016/0147-619X(82)90040-3) / Plasmid / Wide host range cloning vectors: a cosmid clone bank of an Agrobacterium Ti plasmid by Knauf V. C. (1982)
Krieg N. R. and J. G. Holt. (ed.). 1984. Bergey's manual of systematic bacteriology vol. 1. The Williams & Wilkins Co. Baltimore.
Leigh , J. A. , E. R. Signer , and G. C. Walker . 1985 . Exopolysaccharide-deficient mutants of Rhizobium meliloti that form ineffective nodules . Proc. Natl. Acad. Sci. USA 82 : 6231 - 6235 . (10.1073/pnas.82.18.6231) / Proc. Natl. Acad. Sci. USA / Exopolysaccharide-deficient mutants of Rhizobium meliloti that form ineffective nodules by Leigh J. A. (1985)
Leong , S. A. , G. S. Ditta , and D. R. Helinski . 1982 . Heme biosynthesis in Rhizobium . J. Biol. Chem. 257 : 8724 - 8730 . / J. Biol. Chem. / Heme biosynthesis in Rhizobium by Leong S. A. (1982)
Long S. R. 1984. Genetics ofRhizobium nodulation p. 265-306. In T. Kosuge and E. W. Nester (ed.) Plant-microbe interactions: molecular and genetic perspectives vol. 1. Macmillan Publishing Co. Inc. New York.
Matthysse , A. G. 1983 . Role of bacterial cellulose fibrils in Agrobacterium tumefaciens infection . J. Bacteriol. 154 : 906 - 915 . (10.1128/jb.154.2.906-915.1983) / J. Bacteriol. / Role of bacterial cellulose fibrils in Agrobacterium tumefaciens infection by Matthysse A. G. (1983)
Puvanesarajah , V. , F. M. Schell , G. Stacey , C. J. Douglas , and E. W. Nester . 1985 . A role for 2-linked-13-D-glucan in the virulence of Agrobacterium tumefaciens . J. Bacteriol. 164 : 102 - 106 . (10.1128/jb.164.1.102-106.1985) / J. Bacteriol. / A role for 2-linked-13-D-glucan in the virulence of Agrobacterium tumefaciens by Puvanesarajah V. (1985)
Rosenberg , C. , and T. Huguet . 1984 . The pAtC58 plasmid of Agrobacterium tumefaciens is not essential for tumor induction . Mol. Gen. Genet. 196 : 533 - 536 . (10.1007/BF00436205) / Mol. Gen. Genet. / The pAtC58 plasmid of Agrobacterium tumefaciens is not essential for tumor induction by Rosenberg C. (1984)
Schleif R. F. and P. C. Wensink. 1981. Practical methods in molecular biology p. 17. Springer-Verlag New York. (10.1007/978-1-4612-5956-5)
Shaw P. D. 1987. Plasmid ecology p. 3-39. In T. Kosuge and E. W. Nester (ed.) Plant-microbe interactions: molecular and genetic perspectives vol. 2. Macmillan Publishing Co. Inc. New York.
Sutherland , I. W. 1985 . Biosynthesis and composition of gramnegative bacterial extracellular and wall polysaccharides. Annu . Rev. Microbiol. 39 : 243 - 270 . (10.1146/annurev.mi.39.100185.001331) / Rev. Microbiol. / Biosynthesis and composition of gramnegative bacterial extracellular and wall polysaccharides. Annu by Sutherland I. W. (1985)
Thomashow , M. F. , R. Nutter , A. L. Montoya , M. P. Gordon , and E. W. Nester . 1980 . Integration and organization of Tiplasmid sequences in crown gall tumors . Cell 19 : 729 - 739 . (10.1016/S0092-8674(80)80049-3) / Cell / Integration and organization of Tiplasmid sequences in crown gall tumors by Thomashow M. F. (1980)
Van Larabeke , N. , G. Engler , M. Holsters , S. Van den Elsacker , I. Zaenen , R. Schilperoort , and J. Schell . 1974 . Large plasmids of A. tumefaciens essential for crown gall inducing activity . Nature (London) 252 : 169 - 170 . (10.1038/252169a0) / Nature (London) / Large plasmids of A. tumefaciens essential for crown gall inducing activity by Van Larabeke N. (1974)
Zambryski , P. , M. Holsters , K. Kruger , A. Kepicker , J. Schell , M. Van Montagu , and H. M. Goodman . 1980 . Tumor DNA structure in plant cells transformed by A. tumefaciens . Science 209 : 1385 - 1391 . (10.1126/science.6251546) / Science / Tumor DNA structure in plant cells transformed by A. tumefaciens by Zambryski P. (1980)
Zevenhuizen , L. P. T. M. , and A. R. W. van Neerven . 1983 . (1,2)-f-D-glucan and acidic oligosaccharides produced by Rhizobium meliloti . Carbohydr. Res. 118 : 127 - 134 . (10.1016/0008-6215(83)88041-0) / Carbohydr. Res. / (1,2)-f-D-glucan and acidic oligosaccharides produced by Rhizobium meliloti by Zevenhuizen L. P. T. M. (1983)

Dates

Type	When
Created	8 years, 10 months ago (Nov. 2, 2016, 7:42 p.m.)
Deposited	4 years, 1 month ago (July 29, 2021, 1:37 p.m.)
Indexed	1 week, 4 days ago (Aug. 22, 2025, 12:55 a.m.)
Issued	38 years, 4 months ago (May 1, 1987)
Published	38 years, 4 months ago (May 1, 1987)
Published Print	38 years, 4 months ago (May 1, 1987)

Funders 0

None

BibTeX

@article{Cangelosi_1987, title={Common loci for Agrobacterium tumefaciens and Rhizobium meliloti exopolysaccharide synthesis and their roles in plant interactions}, volume={169}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.169.5.2086-2091.1987}, DOI={10.1128/jb.169.5.2086-2091.1987}, number={5}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Cangelosi, G A and Hung, L and Puvanesarajah, V and Stacey, G and Ozga, D A and Leigh, J A and Nester, E W}, year={1987}, month=may, pages={2086–2091} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        22
      ]
    ],
    "date-time": "2025-08-22T04:55:48Z",
    "timestamp": 1755838548476
  },
  "reference-count": 31,
  "publisher": "American Society for Microbiology",
  "issue": "5",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            1987,
            5,
            1
          ]
        ],
        "date-time": "1987-05-01T00:00:00Z",
        "timestamp": 546825600000
      },
      "content-version": "tdm",
      "delay-in-days": 0,
      "URL": "https://journals.asm.org/non-commercial-tdm-license"
    }
  ],
  "content-domain": {
    "domain": [
      "journals.asm.org"
    ],
    "crossmark-restriction": true
  },
  "published-print": {
    "date-parts": [
      [
        1987,
        5
      ]
    ]
  },
  "abstract": "<jats:p>Mutants of Rhizobium meliloti have been isolated which are deficient in exopolysaccharide (EPS) production and effective nodulation of alfalfa (J. A. Leigh, E. R. Signer, and G. C. Walker, Proc. Natl. Acad. Sci. USA 82:6231-6235, 1985). We isolated approximately 100 analogous EPS-deficient (Exo) mutants of the closely related plant pathogen Agrobacterium tumefaciens, including strains whose EPS deficiencies were specifically complemented by each of five cloned R. meliloti exo loci. We also cloned A. tumefaciens genes which complemented EPS defects in three of the R. meliloti Exo mutants. In two of these cases, symbiotic defects were also complemented. All of the A. tumefaciens Exo mutants formed normal crown gall tumors on four different plant hosts, except ExoC mutants, which were nontumorigenic and unable to attach to plant cells in vitro. Like their R. meliloti counterparts, A. tumefaciens Exo mutants were deficient in production of succinoglycan, the major acidic EPS species produced by both genera. A. tumefaciens ExoC mutants also produced extremely low levels of another major EPS, cyclic 1,2-beta-D-glucan. This deficiency has been noted previously in a different set of nontumorigenic, attachment-defective A. tumefaciens mutants.</jats:p>",
  "DOI": "10.1128/jb.169.5.2086-2091.1987",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2016,
        11,
        2
      ]
    ],
    "date-time": "2016-11-02T23:42:21Z",
    "timestamp": 1478130141000
  },
  "page": "2086-2091",
  "update-policy": "http://dx.doi.org/10.1128/asmj-crossmark-policy-page",
  "source": "Crossref",
  "is-referenced-by-count": 127,
  "title": "Common loci for Agrobacterium tumefaciens and Rhizobium meliloti exopolysaccharide synthesis and their roles in plant interactions",
  "prefix": "10.1128",
  "volume": "169",
  "author": [
    {
      "given": "G A",
      "family": "Cangelosi",
      "sequence": "first",
      "affiliation": []
    },
    {
      "given": "L",
      "family": "Hung",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "V",
      "family": "Puvanesarajah",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "G",
      "family": "Stacey",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "D A",
      "family": "Ozga",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "J A",
      "family": "Leigh",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "E W",
      "family": "Nester",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "member": "235",
  "reference": [
    {
      "key": "p_1",
      "doi-asserted-by": "crossref",
      "first-page": "85",
      "DOI": "10.1016/0076-6879(66)08010-8",
      "article-title": "New colorimetric methods for sugar analysis",
      "volume": "8",
      "author": "Ashwell G.",
      "year": "1966",
      "unstructured": "Ashwell , G. 1966 . New colorimetric methods for sugar analysis . Methods Enzymol. 8 : 85 - 94 .",
      "journal-title": "Methods Enzymol."
    },
    {
      "key": "p_2",
      "first-page": "188",
      "article-title": "R factor transfer in Rhizobium leguminosarum",
      "volume": "84",
      "author": "Beringer J. E.",
      "year": "1974",
      "unstructured": "Beringer , J. E. 1974 . R factor transfer in Rhizobium leguminosarum . J. Gen. Microbiol. 84 : 188 - 189 .",
      "journal-title": "J. Gen. Microbiol."
    },
    {
      "key": "p_3",
      "doi-asserted-by": "crossref",
      "first-page": "263",
      "DOI": "10.1016/0092-8674(77)90043-5",
      "article-title": "Stable incorporation of plasmid DNA into higher plant cells: the molecular basis of crown gall tumorigenesis",
      "volume": "11",
      "author": "Chilton M.",
      "year": "1977",
      "unstructured": "Chilton , M. - D. , M. H. Drummond , D. J. Merlo , D. Skiaky , A. L. Montoya , M. P. Gordon , and E. W. Nester . 1977 . Stable incorporation of plasmid DNA into higher plant cells: the molecular basis of crown gall tumorigenesis . Cell 11 : 263 - 271 .",
      "journal-title": "Cell"
    },
    {
      "key": "p_4",
      "doi-asserted-by": "crossref",
      "first-page": "774",
      "DOI": "10.1128/jb.164.2.774-781.1985",
      "article-title": "Regulation of Ti plasmid virulence genes by a chromosomal locus of Agrobacterium tumefaciens",
      "volume": "164",
      "author": "Close T. J.",
      "year": "1985",
      "unstructured": "Close , T. J. , R. C. Tait , and C. I. Kado . 1985 . Regulation of Ti plasmid virulence genes by a chromosomal locus of Agrobacterium tumefaciens . J. Bacteriol. 164 : 774 - 781 .",
      "journal-title": "J. Bacteriol."
    },
    {
      "key": "p_5",
      "doi-asserted-by": "crossref",
      "first-page": "185",
      "DOI": "10.1016/0008-6215(83)88086-0",
      "article-title": "The cyclic structure of P-D-(1,2)-linked Dglucans secreted by Rhizobia and Agrobacteria",
      "volume": "117",
      "author": "Deli A.",
      "year": "1983",
      "unstructured": "Deli , A. , W. S. York , M. McNeil , A. G. Darvil , and P. Albersheim . 1983 . The cyclic structure of P-D-(1,2)-linked Dglucans secreted by Rhizobia and Agrobacteria . Carbohydr. Res. 117 : 185 - 200 .",
      "journal-title": "Carbohydr. Res."
    },
    {
      "key": "p_6",
      "doi-asserted-by": "crossref",
      "first-page": "485",
      "DOI": "10.1007/BF00331029",
      "article-title": "Genetic manipulations in Rhizobium meliloti utilizing two new transposon Tn 5 derivatives",
      "volume": "204",
      "author": "De Vos G. F.",
      "year": "1986",
      "unstructured": "De Vos , G. F. , G. C. Walker , and E. R. Signer . 1986 . Genetic manipulations in Rhizobium meliloti utilizing two new transposon Tn 5 derivatives . Mol. Gen. Genet. 204 : 485 - 491 .",
      "journal-title": "Mol. Gen. Genet."
    },
    {
      "key": "p_7",
      "first-page": "478",
      "article-title": "General color reactions",
      "volume": "1",
      "author": "Dische Z.",
      "year": "1962",
      "unstructured": "Dische , Z. 1962 . General color reactions . Methods Carbohydr. Chem. 1 : 478 - 492 .",
      "journal-title": "Methods Carbohydr. Chem."
    },
    {
      "key": "p_8",
      "doi-asserted-by": "crossref",
      "first-page": "1265",
      "DOI": "10.1128/jb.152.3.1265-1275.1982",
      "article-title": "Agrobacterium tumefaciens mutants affected in attachment to plant cells",
      "volume": "152",
      "author": "Douglas C. J.",
      "year": "1982",
      "unstructured": "Douglas , C. J. , W. Halperin , and E. W. Nester . 1982 . Agrobacterium tumefaciens mutants affected in attachment to plant cells . J. Bacteriol. 152 : 1265 - 1275 .",
      "journal-title": "J. Bacteriol."
    },
    {
      "key": "p_9",
      "doi-asserted-by": "crossref",
      "first-page": "850",
      "DOI": "10.1128/jb.161.3.850-860.1985",
      "article-title": "Identification and genetic analysis of an Agrobacterium tumefaciens chromosomal virulence region",
      "volume": "161",
      "author": "Douglas C. J.",
      "year": "1985",
      "unstructured": "Douglas , C. J. , R. J. Staneloni , R. A. Rubin , and E. W. Nester . 1985 . Identification and genetic analysis of an Agrobacterium tumefaciens chromosomal virulence region . J. Bacteriol. 161 : 850 - 860 .",
      "journal-title": "J. Bacteriol."
    },
    {
      "key": "p_10",
      "doi-asserted-by": "crossref",
      "first-page": "4403",
      "DOI": "10.1073/pnas.83.12.4403",
      "article-title": "Rhizobium meliloti genes required for nodule development are related to chromosomal virulence genes in Agrobacterium tumefaciens",
      "volume": "83",
      "author": "Dylan T.",
      "year": "1986",
      "unstructured": "Dylan , T. , L. lelpi, S. Stanfield , L. Kashyap , C. Douglas , M. Yanofsky , E. Nester , D. R. Helinski , and G. Ditta . 1986 . Rhizobium meliloti genes required for nodule development are related to chromosomal virulence genes in Agrobacterium tumefaciens . Proc. Natl. Acad. Sci. USA 83 : 4403 4407.",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "p_11",
      "doi-asserted-by": "crossref",
      "first-page": "869",
      "DOI": "10.1016/0092-8674(85)90346-0",
      "article-title": "Symbiotic mutants of Rhizobium meliloti that uncouple plant from bacterial differentiation",
      "volume": "40",
      "author": "Finan T. M.",
      "year": "1985",
      "unstructured": "Finan , T. M. , A. M. Hirsch , J. A. Leigh , E. Johansen , G. A. Kuldau , S. Deegan , G. C. Walker , and E. R. Signer . 1985 . Symbiotic mutants of Rhizobium meliloti that uncouple plant from bacterial differentiation . Cell 40 : 869 - 877 .",
      "journal-title": "Cell"
    },
    {
      "key": "p_12",
      "doi-asserted-by": "crossref",
      "first-page": "66",
      "DOI": "10.1128/jb.167.1.66-72.1986",
      "article-title": "Second symbiotic plasmid in Rhizobium meliloti carrying exopolysaccharide and thiamine synthetis genes",
      "volume": "167",
      "author": "Finan T. M.",
      "year": "1986",
      "unstructured": "Finan , T. M. , B. Kunkel , G. F. De Vos , and E. R. Signer . 1986 . Second symbiotic plasmid in Rhizobium meliloti carrying exopolysaccharide and thiamine synthetis genes . J. Bacteriol. 167 : 66 - 72 .",
      "journal-title": "J. Bacteriol."
    },
    {
      "key": "p_13",
      "doi-asserted-by": "crossref",
      "first-page": "732",
      "DOI": "10.1128/jb.144.2.732-743.1980",
      "article-title": "Agrobacterium tumefaciens mutants affected in crown gall tumorigenesis and octopine catabolism",
      "volume": "144",
      "author": "Garfinkel D. J.",
      "year": "1980",
      "unstructured": "Garfinkel , D. J. , and E. W. Nester . 1980 . Agrobacterium tumefaciens mutants affected in crown gall tumorigenesis and octopine catabolism . J. Bacteriol. 144 : 732 - 743 .",
      "journal-title": "J. Bacteriol."
    },
    {
      "key": "p_14",
      "doi-asserted-by": "crossref",
      "first-page": "143",
      "DOI": "10.1016/0092-8674(81)90368-8",
      "article-title": "Genetic analysis of crown gall: fine structure map of T-DNA by site-directed mutagenesis",
      "volume": "27",
      "author": "Garfinkel D. J.",
      "year": "1981",
      "unstructured": "Garfinkel , D. J. , R. B. Simpson , L. W. Ream , F. F. White , M. P. Gordon , and E. W. Nester . 1981 . Genetic analysis of crown gall: fine structure map of T-DNA by site-directed mutagenesis . Cell 27 : 143 - 153 .",
      "journal-title": "Cell"
    },
    {
      "key": "p_15",
      "first-page": "1049",
      "article-title": "Structural elucidation of succinoglycan and related polysaccharides from Agrobacterium and Rhizobium by fragmentation with two special ,-D-glycanases and methylation analysis",
      "volume": "44",
      "author": "Hisamatsu M.",
      "year": "1980",
      "unstructured": "Hisamatsu , M. , J. Abe , A. Amemura , and T. Harada . 1980 . Structural elucidation of succinoglycan and related polysaccharides from Agrobacterium and Rhizobium by fragmentation with two special ,-D-glycanases and methylation analysis . Agric. Biol. Chem. 44 : 1049 - 1055 .",
      "journal-title": "Agric. Biol. Chem."
    },
    {
      "key": "p_16",
      "doi-asserted-by": "crossref",
      "first-page": "878",
      "DOI": "10.1128/jb.153.2.878-883.1983",
      "article-title": "Mutational analysis of the virulence region of an Agrobacterium tumefaciens Ti plasmid",
      "volume": "153",
      "author": "Klee H. J.",
      "year": "1983",
      "unstructured": "Klee , H. J. , F. F. White , V. N. Iyer , M. P. Gordon , and E. W. Nester . 1983 . Mutational analysis of the virulence region of an Agrobacterium tumefaciens Ti plasmid . J. Bacteriol. 153 : 878 - 883 .",
      "journal-title": "J. Bacteriol."
    },
    {
      "key": "p_17",
      "doi-asserted-by": "crossref",
      "first-page": "45",
      "DOI": "10.1016/0147-619X(82)90040-3",
      "article-title": "Wide host range cloning vectors: a cosmid clone bank of an Agrobacterium Ti plasmid",
      "volume": "8",
      "author": "Knauf V. C.",
      "year": "1982",
      "unstructured": "Knauf , V. C. , and E. W. Nester . 1982 . Wide host range cloning vectors: a cosmid clone bank of an Agrobacterium Ti plasmid . Plasmid 8 : 45 - 54 .",
      "journal-title": "Plasmid"
    },
    {
      "key": "p_18",
      "unstructured": "Krieg N. R. and J. G. Holt. (ed.). 1984. Bergey's manual of systematic bacteriology vol. 1. The Williams & Wilkins Co. Baltimore."
    },
    {
      "key": "p_19",
      "doi-asserted-by": "crossref",
      "first-page": "6231",
      "DOI": "10.1073/pnas.82.18.6231",
      "article-title": "Exopolysaccharide-deficient mutants of Rhizobium meliloti that form ineffective nodules",
      "volume": "82",
      "author": "Leigh J. A.",
      "year": "1985",
      "unstructured": "Leigh , J. A. , E. R. Signer , and G. C. Walker . 1985 . Exopolysaccharide-deficient mutants of Rhizobium meliloti that form ineffective nodules . Proc. Natl. Acad. Sci. USA 82 : 6231 - 6235 .",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "p_20",
      "first-page": "8724",
      "article-title": "Heme biosynthesis in Rhizobium",
      "volume": "257",
      "author": "Leong S. A.",
      "year": "1982",
      "unstructured": "Leong , S. A. , G. S. Ditta , and D. R. Helinski . 1982 . Heme biosynthesis in Rhizobium . J. Biol. Chem. 257 : 8724 - 8730 .",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "p_21",
      "unstructured": "Long S. R. 1984. Genetics ofRhizobium nodulation p. 265-306. In T. Kosuge and E. W. Nester (ed.) Plant-microbe interactions: molecular and genetic perspectives vol. 1. Macmillan Publishing Co. Inc. New York."
    },
    {
      "key": "p_22",
      "doi-asserted-by": "crossref",
      "first-page": "906",
      "DOI": "10.1128/jb.154.2.906-915.1983",
      "article-title": "Role of bacterial cellulose fibrils in Agrobacterium tumefaciens infection",
      "volume": "154",
      "author": "Matthysse A. G.",
      "year": "1983",
      "unstructured": "Matthysse , A. G. 1983 . Role of bacterial cellulose fibrils in Agrobacterium tumefaciens infection . J. Bacteriol. 154 : 906 - 915 .",
      "journal-title": "J. Bacteriol."
    },
    {
      "key": "p_23",
      "doi-asserted-by": "crossref",
      "first-page": "102",
      "DOI": "10.1128/jb.164.1.102-106.1985",
      "article-title": "A role for 2-linked-13-D-glucan in the virulence of Agrobacterium tumefaciens",
      "volume": "164",
      "author": "Puvanesarajah V.",
      "year": "1985",
      "unstructured": "Puvanesarajah , V. , F. M. Schell , G. Stacey , C. J. Douglas , and E. W. Nester . 1985 . A role for 2-linked-13-D-glucan in the virulence of Agrobacterium tumefaciens . J. Bacteriol. 164 : 102 - 106 .",
      "journal-title": "J. Bacteriol."
    },
    {
      "key": "p_24",
      "doi-asserted-by": "crossref",
      "first-page": "533",
      "DOI": "10.1007/BF00436205",
      "article-title": "The pAtC58 plasmid of Agrobacterium tumefaciens is not essential for tumor induction",
      "volume": "196",
      "author": "Rosenberg C.",
      "year": "1984",
      "unstructured": "Rosenberg , C. , and T. Huguet . 1984 . The pAtC58 plasmid of Agrobacterium tumefaciens is not essential for tumor induction . Mol. Gen. Genet. 196 : 533 - 536 .",
      "journal-title": "Mol. Gen. Genet."
    },
    {
      "key": "p_25",
      "doi-asserted-by": "crossref",
      "unstructured": "Schleif R. F. and P. C. Wensink. 1981. Practical methods in molecular biology p. 17. Springer-Verlag New York.",
      "DOI": "10.1007/978-1-4612-5956-5"
    },
    {
      "key": "p_26",
      "unstructured": "Shaw P. D. 1987. Plasmid ecology p. 3-39. In T. Kosuge and E. W. Nester (ed.) Plant-microbe interactions: molecular and genetic perspectives vol. 2. Macmillan Publishing Co. Inc. New York."
    },
    {
      "key": "p_27",
      "doi-asserted-by": "crossref",
      "first-page": "243",
      "DOI": "10.1146/annurev.mi.39.100185.001331",
      "article-title": "Biosynthesis and composition of gramnegative bacterial extracellular and wall polysaccharides. Annu",
      "volume": "39",
      "author": "Sutherland I. W.",
      "year": "1985",
      "unstructured": "Sutherland , I. W. 1985 . Biosynthesis and composition of gramnegative bacterial extracellular and wall polysaccharides. Annu . Rev. Microbiol. 39 : 243 - 270 .",
      "journal-title": "Rev. Microbiol."
    },
    {
      "key": "p_28",
      "doi-asserted-by": "crossref",
      "first-page": "729",
      "DOI": "10.1016/S0092-8674(80)80049-3",
      "article-title": "Integration and organization of Tiplasmid sequences in crown gall tumors",
      "volume": "19",
      "author": "Thomashow M. F.",
      "year": "1980",
      "unstructured": "Thomashow , M. F. , R. Nutter , A. L. Montoya , M. P. Gordon , and E. W. Nester . 1980 . Integration and organization of Tiplasmid sequences in crown gall tumors . Cell 19 : 729 - 739 .",
      "journal-title": "Cell"
    },
    {
      "key": "p_29",
      "doi-asserted-by": "crossref",
      "first-page": "169",
      "DOI": "10.1038/252169a0",
      "article-title": "Large plasmids of A. tumefaciens essential for crown gall inducing activity",
      "volume": "252",
      "author": "Van Larabeke N.",
      "year": "1974",
      "unstructured": "Van Larabeke , N. , G. Engler , M. Holsters , S. Van den Elsacker , I. Zaenen , R. Schilperoort , and J. Schell . 1974 . Large plasmids of A. tumefaciens essential for crown gall inducing activity . Nature (London) 252 : 169 - 170 .",
      "journal-title": "Nature (London)"
    },
    {
      "key": "p_30",
      "doi-asserted-by": "crossref",
      "first-page": "1385",
      "DOI": "10.1126/science.6251546",
      "article-title": "Tumor DNA structure in plant cells transformed by A. tumefaciens",
      "volume": "209",
      "author": "Zambryski P.",
      "year": "1980",
      "unstructured": "Zambryski , P. , M. Holsters , K. Kruger , A. Kepicker , J. Schell , M. Van Montagu , and H. M. Goodman . 1980 . Tumor DNA structure in plant cells transformed by A. tumefaciens . Science 209 : 1385 - 1391 .",
      "journal-title": "Science"
    },
    {
      "key": "p_31",
      "doi-asserted-by": "crossref",
      "first-page": "127",
      "DOI": "10.1016/0008-6215(83)88041-0",
      "article-title": "(1,2)-f-D-glucan and acidic oligosaccharides produced by Rhizobium meliloti",
      "volume": "118",
      "author": "Zevenhuizen L. P. T. M.",
      "year": "1983",
      "unstructured": "Zevenhuizen , L. P. T. M. , and A. R. W. van Neerven . 1983 . (1,2)-f-D-glucan and acidic oligosaccharides produced by Rhizobium meliloti . Carbohydr. Res. 118 : 127 - 134 .",
      "journal-title": "Carbohydr. Res."
    }
  ],
  "container-title": "Journal of Bacteriology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://journals.asm.org/doi/pdf/10.1128/jb.169.5.2086-2091.1987",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://journals.asm.org/doi/pdf/10.1128/jb.169.5.2086-2091.1987",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2021,
        7,
        29
      ]
    ],
    "date-time": "2021-07-29T17:37:09Z",
    "timestamp": 1627580229000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://journals.asm.org/doi/10.1128/jb.169.5.2086-2091.1987"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1987,
        5
      ]
    ]
  },
  "references-count": 31,
  "journal-issue": {
    "issue": "5",
    "published-print": {
      "date-parts": [
        [
          1987,
          5
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1128/jb.169.5.2086-2091.1987"
  ],
  "URL": "http://dx.doi.org/10.1128/jb.169.5.2086-2091.1987",
  "relation": {},
  "ISSN": [
    "0021-9193",
    "1098-5530"
  ],
  "subject": [],
  "container-title-short": "J Bacteriol",
  "published": {
    "date-parts": [
      [
        1987,
        5
      ]
    ]
  },
  "assertion": [
    {
      "value": "2021-02-02",
      "order": 2,
      "name": "published",
      "label": "Published",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    }
  ]
}