DOI: 10.1126/science.7902614. Map-Based Cloning of a Protein Kinase Gene Conferring Disease Resistance in Tomato

Map-Based Cloning of a Protein Kinase Gene Conferring Disease Resistance in Tomato

10.1126/science.7902614

Crossref journal-article

American Association for the Advancement of Science (AAAS)

Science (221)

Abstract

The Pto gene in tomato confers resistance to races of Pseudomonas syringae pv. tomato that carry the avirulence gene avrPto . A yeast artificial chromosome clone that spans the Pto region was identified and used to probe a leaf complementary DNA (cDNA) library. A cDNA clone was isolated that represents a gene family, at least six members of which genetically cosegregate with Pto . When susceptible tomato plants were transformed with a cDNA from this family, they were resistant to the pathogen. Analysis of the amino acid sequence revealed similarity to serine-threonine protein kinases, suggesting a role for Pto in a signal transduction pathway.

Bibliography

Martin, G. B., Brommonschenkel, S. H., Chunwongse, J., Frary, A., Ganal, M. W., Spivey, R., Wu, T., Earle, E. D., & Tanksley, S. D. (1993). Map-Based Cloning of a Protein Kinase Gene Conferring Disease Resistance in Tomato. Science, 262(5138), 1432â1436.

Authors 9

Gregory B. Martin (first)
Sergio H. Brommonschenkel (additional)
Julapark Chunwongse (additional)
Anne Frary (additional)
Martin W. Ganal (additional)
Rody Spivey (additional)
Tiyun Wu (additional)
Elizabeth D. Earle (additional)
Steven D. Tanksley (additional)

References 55 Referenced 990

ALTSCHUL, S.F., BASIC LOCAL ALIGNMENT SEARCH TOOL, JOURNAL OF MOLECULAR BIOLOGY 215: 403 (1990). (10.1016/S0022-2836(05)80360-2) / JOURNAL OF MOLECULAR BIOLOGY (1990)
Arumuganathan, K., Plant Molecular Biology Reporter 9: 229 (1991). (10.1007/BF02672073) / Plant Molecular Biology Reporter (1991)
BENNETZEN, J.L., EXTRAMARITAL SEX AMONGST THE BEETS - ORGANIZATION, INSTABILITY AND EVOLUTION OF PLANT-DISEASE RESISTANCE GENES, PLANT MOLECULAR BIOLOGY 20: 575 (1992). (10.1007/BF00046442) / PLANT MOLECULAR BIOLOGY (1992)
BERNATZKY, R, TOWARD A SATURATED LINKAGE MAP IN TOMATO BASED ON ISOZYMES AND RANDOM CDNA SEQUENCES, GENETICS 112: 887 (1986). (10.1093/genetics/112.4.887) / GENETICS (1986)
BLISKA, J.B., SIGNAL-TRANSDUCTION IN THE MAMMALIAN-CELL DURING BACTERIAL ATTACHMENT AND ENTRY, CELL 73: 903 (1993). (10.1016/0092-8674(93)90270-Z) / CELL (1993)
BLISKA, J.B., TYROSINE PHOSPHATE HYDROLYSIS OF HOST PROTEINS BY AN ESSENTIAL YERSINIA-VIRULENCE DETERMINANT, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 88: 1187 (1991). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1991)
BONNER, T.I., THE COMPLETE CODING SEQUENCE OF THE HUMAN RAF ONCOGENE AND THE CORRESPONDING STRUCTURE OF THE C-RAF-1 GENE, NUCLEIC ACIDS RESEARCH 14: 1009 (1986). (10.1093/nar/14.2.1009) / NUCLEIC ACIDS RESEARCH (1986)
BUSS, J.E., THE ABSENCE OF MYRISTIC ACID DECREASES MEMBRANE-BINDING OF P60SRC BUT DOES NOT AFFECT TYROSINE PROTEIN-KINASE ACTIVITY, JOURNAL OF VIROLOGY 58: 468 (1986). (10.1128/jvi.58.2.468-474.1986) / JOURNAL OF VIROLOGY (1986)
CHANG, C, THE TMK1-GENE FROM ARABIDOPSIS CODES FOR A PROTEIN WITH STRUCTURAL AND BIOCHEMICAL CHARACTERISTICS OF A RECEPTOR PROTEIN-KINASE, PLANT CELL 4: 1263 (1992). / PLANT CELL (1992)
10.1126/science.3538420
CHUNWONGSE J unpublished data.
DEBENER, T, PLANT JOURNAL 1: 289 (1991). (10.1046/j.1365-313X.1991.t01-7-00999.x) / PLANT JOURNAL (1991)
DICKINSON, M. J., MOLECULAR PLANT-MICROBE INTERACTIONS 6: 341 (1993). (10.1094/MPMI-6-341) / MOLECULAR PLANT-MICROBE INTERACTIONS (1993)
DONG, X.N., INDUCTION OF ARABIDOPSIS DEFENSE GENES BY VIRULENT AND AVIRULENT PSEUDOMONAS-SYRINGAE STRAINS AND BY A CLONED AVIRULENCE GENE, PLANT CELL 3: 61 (1991). / PLANT CELL (1991)
FARMER, E.E., OLIGOSACCHARIDE SIGNALING IN PLANTS - SPECIFICITY OF OLIGOURONIDE-ENHANCED PLASMA-MEMBRANE PROTEIN-PHOSPHORYLATION, JOURNAL OF BIOLOGICAL CHEMISTRY 266: 3140 (1991). (10.1016/S0021-9258(18)49965-6) / JOURNAL OF BIOLOGICAL CHEMISTRY (1991)
10.1126/science.8484117
10.1016/0003-2697(83)90418-9
FELIX, G, RAPID CHANGES OF PROTEIN-PHOSPHORYLATION ARE INVOLVED IN TRANSDUCTION OF THE ELICITOR SIGNAL IN PLANT-CELLS, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 88: 8831 (1991). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1991)
FENSELAU, S, MOLECULAR PLANT-MICROBE INTERACTIONS 5: 390 (1992). (10.1094/MPMI-5-390) / MOLECULAR PLANT-MICROBE INTERACTIONS (1992)
FRARY A unpublished data.
GABRIEL, D.W., WORKING MODELS OF SPECIFIC RECOGNITION IN PLANT-MICROBE INTERACTIONS, ANNUAL REVIEW OF PHYTOPATHOLOGY 28: 365 (1990). (10.1146/annurev.py.28.090190.002053) / ANNUAL REVIEW OF PHYTOPATHOLOGY (1990)
GABRIEL, D.W., GENE-FOR-GENE INTERACTIONS OF 5 CLONED AVIRULENCE GENES FROM XANTHOMONAS-CAMPESTRIS PV MALVACEARUM WITH SPECIFIC RESISTANCE GENES IN COTTON, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 83: 6415 (1986). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1986)
GOUGH, C. L., MOLECULAR PLANT-MICROBE INTERACTIONS 5: 384 (1992). (10.1094/MPMI-5-384) / MOLECULAR PLANT-MICROBE INTERACTIONS (1992)
GRAND, RJA, ACYLATION OF VIRAL AND EUKARYOTIC PROTEINS, BIOCHEMICAL JOURNAL 258: 625 (1989). (10.1042/bj2580625) / BIOCHEMICAL JOURNAL (1989)
10.1126/science.2166336
10.1016/0076-6879(91)00126-H
10.1126/science.3291115
HUANG, H.C., THE PSEUDOMONAS-SYRINGAE PV SYRINGAE-61 HRPH PRODUCT, AN ENVELOPE PROTEIN REQUIRED FOR ELICITATION OF THE HYPERSENSITIVE RESPONSE IN PLANTS, JOURNAL OF BACTERIOLOGY 174: 6878 (1992). (10.1128/jb.174.21.6878-6885.1992) / JOURNAL OF BACTERIOLOGY (1992)
HULBERT, S.H., LINKAGE ANALYSIS OF GENES FOR RESISTANCE TO DOWNY MILDEW (BREMIA-LACTUCAE) IN LETTUCE (LACTUCA-SATIVA), THEORETICAL AND APPLIED GENETICS 70: 520 (1985). (10.1007/BF00305985) / THEORETICAL AND APPLIED GENETICS (1985)
JONES, D. A., MOLECULAR PLANT-MICROBE INTERACTIONS 6: 348 (1993). (10.1094/MPMI-6-348) / MOLECULAR PLANT-MICROBE INTERACTIONS (1993)
KEEN, N.T., NEW DISEASE RESISTANCE GENES IN SOYBEAN AGAINST PSEUDOMONAS-SYRINGAE PV GLYCINEA - EVIDENCE THAT ONE OF THEM INTERACTS WITH A BACTERIAL ELICITOR, THEORETICAL AND APPLIED GENETICS 81: 133 (1991). (10.1007/BF00226123) / THEORETICAL AND APPLIED GENETICS (1991)
KING, E.O., 2 SIMPLE MEDIA FOR THE DEMONSTRATION OF PYOCYANIN AND FLUORESCIN, JOURNAL OF LABORATORY AND CLINICAL MEDICINE 44: 301 (1954). / JOURNAL OF LABORATORY AND CLINICAL MEDICINE (1954)
KOBAYASHI, D.Y., CLONED AVIRULENCE GENES FROM THE TOMATO PATHOGEN PSEUDOMONAS-SYRINGAE PV TOMATO CONFER CULTIVAR SPECIFICITY ON SOYBEAN, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 86: 157 (1989). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1989)
MARK, G.E., DROSOPHILA-MELANOGASTER HOMOLOGS OF THE RAF ONCOGENE, MOLECULAR AND CELLULAR BIOLOGY 7: 2134 (1987). / MOLECULAR AND CELLULAR BIOLOGY (1987)
MARTIN, G. B., MOLECULAR & GENERAL GENETICS 233: 25 (1992). (10.1007/BF00587557) / MOLECULAR & GENERAL GENETICS (1992)
MARTIN, G. B., MOLECULAR PLANT-MICROBE INTERACTIONS 6: 26 (1993). (10.1094/MPMI-6-026) / MOLECULAR PLANT-MICROBE INTERACTIONS (1993)
MARTIN, G.B., RAPID IDENTIFICATION OF MARKERS LINKED TO A PSEUDOMONAS RESISTANCE GENE IN TOMATO BY USING RANDOM PRIMERS AND NEAR-ISOGENIC LINES, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 88: 2336 (1991). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1991)
MARTIN G.B. unpublished data.
10.1126/science.8503004
MESHI, T, MUTATIONS IN THE TOBACCO MOSAIC-VIRUS 30-KD PROTEIN GENE OVERCOME TM-2 RESISTANCE IN TOMATO, PLANT CELL 1: 515 (1989). / PLANT CELL (1989)
MESSEGUER, R, HIGH-RESOLUTION RFLP MAP AROUND THE ROOT-KNOT NEMATODE RESISTANCE GENE (MI) IN TOMATO, THEORETICAL AND APPLIED GENETICS 82: 529 (1991). (10.1007/BF00226787) / THEORETICAL AND APPLIED GENETICS (1991)
OCHMAN, H, GENETIC APPLICATIONS OF AN INVERSE POLYMERASE CHAIN-REACTION, GENETICS 120: 621 (1988). (10.1093/genetics/120.3.621) / GENETICS (1988)
RAZ, V, ETHYLENE SIGNAL IS TRANSDUCED VIA PROTEIN-PHOSPHORYLATION EVENTS IN PLANTS, PLANT CELL 5: 523 (1993). (10.2307/3869707) / PLANT CELL (1993)
RONALD, P.C., THE CLONED AVIRULENCE GENE AVRPTO INDUCES DISEASE RESISTANCE IN TOMATO CULTIVARS CONTAINING THE PTO RESISTANCE GENE, JOURNAL OF BACTERIOLOGY 174: 1604 (1992). (10.1128/jb.174.5.1604-1611.1992) / JOURNAL OF BACTERIOLOGY (1992)
Sambrook J. Molecular Cloning: A Laboratory Manual (1989).
SARFATTI, M, AN RFLP MARKER IN TOMATO LINKED TO THE FUSARIUM-OXYSPORUM RESISTANCE GENE I2, THEORETICAL AND APPLIED GENETICS 78: 755 (1989). (10.1007/BF00262574) / THEORETICAL AND APPLIED GENETICS (1989)
10.1126/science.3917576
Staskawicz, B. J., Proceedings of the National Academy of Sciences of the United States of America 81: 6024 (1984). / Proceedings of the National Academy of Sciences of the United States of America (1984)
STEIN, J.C., MOLECULAR-CLONING OF A PUTATIVE RECEPTOR PROTEIN-KINASE GENE ENCODED AT THE SELF-INCOMPATIBILITY LOCUS OF BRASSICA-OLERACEA, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 88: 8816 (1991). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1991)
TANKSLEY, S.D., HIGH-DENSITY MOLECULAR LINKAGE MAPS OF THE TOMATO AND POTATO GENOMES, GENETICS 132: 1141 (1992). (10.1093/genetics/132.4.1141) / GENETICS (1992)
TOBIAS, C.M., AN ARABIDOPSIS-THALIANA GENE WITH SEQUENCE SIMILARITY TO THE S-LOCUS RECEPTOR KINASE OF BRASSICA-OLERACEA - SEQUENCE AND EXPRESSION, PLANT PHYSIOLOGY 99: 284 (1992). (10.1104/pp.99.1.284) / PLANT PHYSIOLOGY (1992)
VANKAN, J. A. L.,MOLECULAR PLANT-MICROBE INTERACTIONS 4: 52 (1991). (10.1094/MPMI-4-052) / MOLECULAR PLANT-MICROBE INTERACTIONS (1991)
WALKER, J.C., RELATIONSHIP OF A PUTATIVE RECEPTOR PROTEIN-KINASE FROM MAIZE TO THE S-LOCUS GLYCOPROTEINS OF BRASSICA, NATURE 345: 743 (1990). (10.1038/345743a0) / NATURE (1990)
Watterson, J. C., The Tomato Crop: A Scientific Basis for Improvement: 443 (1986). / The Tomato Crop: A Scientific Basis for Improvement (1986)
ZAMIR, D, TOMATO GENOME IS COMPRISED LARGELY OF FAST-EVOLVING, LOW COPY-NUMBER SEQUENCES, MOLECULAR & GENERAL GENETICS 213: 254 (1988). (10.1007/BF00339589) / MOLECULAR & GENERAL GENETICS (1988)

Dates

Type	When
Created	18 years, 10 months ago (Oct. 5, 2006, 7:05 p.m.)
Deposited	1 year, 7 months ago (Jan. 14, 2024, 11:31 p.m.)
Indexed	2 weeks ago (Aug. 7, 2025, 4:31 p.m.)
Issued	31 years, 8 months ago (Nov. 26, 1993)
Published	31 years, 8 months ago (Nov. 26, 1993)
Published Print	31 years, 8 months ago (Nov. 26, 1993)

Funders 0

None

BibTeX

@article{Martin_1993, title={Map-Based Cloning of a Protein Kinase Gene Conferring Disease Resistance in Tomato}, volume={262}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.7902614}, DOI={10.1126/science.7902614}, number={5138}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={Martin, Gregory B. and Brommonschenkel, Sergio H. and Chunwongse, Julapark and Frary, Anne and Ganal, Martin W. and Spivey, Rody and Wu, Tiyun and Earle, Elizabeth D. and Tanksley, Steven D.}, year={1993}, month=nov, pages={1432–1436} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        7
      ]
    ],
    "date-time": "2025-08-07T20:31:52Z",
    "timestamp": 1754598712885
  },
  "reference-count": 55,
  "publisher": "American Association for the Advancement of Science (AAAS)",
  "issue": "5138",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        1993,
        11,
        26
      ]
    ]
  },
  "abstract": "<jats:p>\n            The\n            <jats:italic>Pto</jats:italic>\n            gene in tomato confers resistance to races of\n            <jats:italic>Pseudomonas syringae</jats:italic>\n            pv.\n            <jats:italic>tomato</jats:italic>\n            that carry the avirulence gene\n            <jats:italic>avrPto</jats:italic>\n            . A yeast artificial chromosome clone that spans the\n            <jats:italic>Pto</jats:italic>\n            region was identified and used to probe a leaf complementary DNA (cDNA) library. A cDNA clone was isolated that represents a gene family, at least six members of which genetically cosegregate with\n            <jats:italic>Pto</jats:italic>\n            . When susceptible tomato plants were transformed with a cDNA from this family, they were resistant to the pathogen. Analysis of the amino acid sequence revealed similarity to serine-threonine protein kinases, suggesting a role for\n            <jats:italic>Pto</jats:italic>\n            in a signal transduction pathway.\n          </jats:p>",
  "DOI": "10.1126/science.7902614",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2006,
        10,
        5
      ]
    ],
    "date-time": "2006-10-05T23:05:09Z",
    "timestamp": 1160089509000
  },
  "page": "1432-1436",
  "source": "Crossref",
  "is-referenced-by-count": 990,
  "title": "Map-Based Cloning of a Protein Kinase Gene Conferring Disease Resistance in Tomato",
  "prefix": "10.1126",
  "volume": "262",
  "author": [
    {
      "given": "Gregory B.",
      "family": "Martin",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Department of Plant Breeding and Biometry, Cornell University, Ithaca, NY 14853-1902."
        },
        {
          "name": "Department of Agronomy, Purdue University, West Lafayette, IN 47907-1150."
        }
      ]
    },
    {
      "given": "Sergio H.",
      "family": "Brommonschenkel",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Plant Breeding and Biometry, Cornell University, Ithaca, NY 14853-1902."
        }
      ]
    },
    {
      "given": "Julapark",
      "family": "Chunwongse",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Plant Breeding and Biometry, Cornell University, Ithaca, NY 14853-1902."
        }
      ]
    },
    {
      "given": "Anne",
      "family": "Frary",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Plant Breeding and Biometry, Cornell University, Ithaca, NY 14853-1902."
        }
      ]
    },
    {
      "given": "Martin W.",
      "family": "Ganal",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Plant Breeding and Biometry, Cornell University, Ithaca, NY 14853-1902."
        }
      ]
    },
    {
      "given": "Rody",
      "family": "Spivey",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Plant Breeding and Biometry, Cornell University, Ithaca, NY 14853-1902."
        }
      ]
    },
    {
      "given": "Tiyun",
      "family": "Wu",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Plant Breeding and Biometry, Cornell University, Ithaca, NY 14853-1902."
        }
      ]
    },
    {
      "given": "Elizabeth D.",
      "family": "Earle",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Plant Breeding and Biometry, Cornell University, Ithaca, NY 14853-1902."
        }
      ]
    },
    {
      "given": "Steven D.",
      "family": "Tanksley",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Plant Breeding and Biometry, Cornell University, Ithaca, NY 14853-1902."
        }
      ]
    }
  ],
  "member": "221",
  "reference": [
    {
      "key": "e_1_2_1_1_1",
      "doi-asserted-by": "crossref",
      "first-page": "403",
      "DOI": "10.1016/S0022-2836(05)80360-2",
      "volume": "215",
      "year": "1990",
      "unstructured": "ALTSCHUL, S.F., BASIC LOCAL ALIGNMENT SEARCH TOOL, JOURNAL OF MOLECULAR BIOLOGY 215: 403 (1990).",
      "journal-title": "JOURNAL OF MOLECULAR BIOLOGY"
    },
    {
      "key": "e_1_2_1_2_1",
      "doi-asserted-by": "crossref",
      "first-page": "229",
      "DOI": "10.1007/BF02672073",
      "volume": "9",
      "year": "1991",
      "unstructured": "Arumuganathan, K., Plant Molecular Biology Reporter 9: 229 (1991).",
      "journal-title": "Plant Molecular Biology Reporter"
    },
    {
      "key": "e_1_2_1_3_1",
      "doi-asserted-by": "crossref",
      "first-page": "575",
      "DOI": "10.1007/BF00046442",
      "volume": "20",
      "year": "1992",
      "unstructured": "BENNETZEN, J.L., EXTRAMARITAL SEX AMONGST THE BEETS - ORGANIZATION, INSTABILITY AND EVOLUTION OF PLANT-DISEASE RESISTANCE GENES, PLANT MOLECULAR BIOLOGY 20: 575 (1992).",
      "journal-title": "PLANT MOLECULAR BIOLOGY"
    },
    {
      "key": "e_1_2_1_4_1",
      "doi-asserted-by": "crossref",
      "first-page": "887",
      "DOI": "10.1093/genetics/112.4.887",
      "volume": "112",
      "year": "1986",
      "unstructured": "BERNATZKY, R, TOWARD A SATURATED LINKAGE MAP IN TOMATO BASED ON ISOZYMES AND RANDOM CDNA SEQUENCES, GENETICS 112: 887 (1986).",
      "journal-title": "GENETICS"
    },
    {
      "key": "e_1_2_1_5_1",
      "doi-asserted-by": "crossref",
      "first-page": "903",
      "DOI": "10.1016/0092-8674(93)90270-Z",
      "volume": "73",
      "year": "1993",
      "unstructured": "BLISKA, J.B., SIGNAL-TRANSDUCTION IN THE MAMMALIAN-CELL DURING BACTERIAL ATTACHMENT AND ENTRY, CELL 73: 903 (1993).",
      "journal-title": "CELL"
    },
    {
      "key": "e_1_2_1_6_1",
      "first-page": "1187",
      "volume": "88",
      "year": "1991",
      "unstructured": "BLISKA, J.B., TYROSINE PHOSPHATE HYDROLYSIS OF HOST PROTEINS BY AN ESSENTIAL YERSINIA-VIRULENCE DETERMINANT, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 88: 1187 (1991).",
      "journal-title": "PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA"
    },
    {
      "key": "e_1_2_1_7_1",
      "doi-asserted-by": "crossref",
      "first-page": "1009",
      "DOI": "10.1093/nar/14.2.1009",
      "volume": "14",
      "year": "1986",
      "unstructured": "BONNER, T.I., THE COMPLETE CODING SEQUENCE OF THE HUMAN RAF ONCOGENE AND THE CORRESPONDING STRUCTURE OF THE C-RAF-1 GENE, NUCLEIC ACIDS RESEARCH 14: 1009 (1986).",
      "journal-title": "NUCLEIC ACIDS RESEARCH"
    },
    {
      "key": "e_1_2_1_8_1",
      "doi-asserted-by": "crossref",
      "first-page": "468",
      "DOI": "10.1128/jvi.58.2.468-474.1986",
      "volume": "58",
      "year": "1986",
      "unstructured": "BUSS, J.E., THE ABSENCE OF MYRISTIC ACID DECREASES MEMBRANE-BINDING OF P60SRC BUT DOES NOT AFFECT TYROSINE PROTEIN-KINASE ACTIVITY, JOURNAL OF VIROLOGY 58: 468 (1986).",
      "journal-title": "JOURNAL OF VIROLOGY"
    },
    {
      "key": "e_1_2_1_9_1",
      "first-page": "1263",
      "volume": "4",
      "year": "1992",
      "unstructured": "CHANG, C, THE TMK1-GENE FROM ARABIDOPSIS CODES FOR A PROTEIN WITH STRUCTURAL AND BIOCHEMICAL CHARACTERISTICS OF A RECEPTOR PROTEIN-KINASE, PLANT CELL 4: 1263 (1992).",
      "journal-title": "PLANT CELL"
    },
    {
      "key": "e_1_2_1_10_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.3538420"
    },
    {
      "key": "e_1_2_1_11_1",
      "unstructured": "CHUNWONGSE J unpublished data."
    },
    {
      "key": "e_1_2_1_12_1",
      "doi-asserted-by": "crossref",
      "first-page": "289",
      "DOI": "10.1046/j.1365-313X.1991.t01-7-00999.x",
      "volume": "1",
      "year": "1991",
      "unstructured": "DEBENER, T, PLANT JOURNAL 1: 289 (1991).",
      "journal-title": "PLANT JOURNAL"
    },
    {
      "key": "e_1_2_1_13_1",
      "doi-asserted-by": "crossref",
      "first-page": "341",
      "DOI": "10.1094/MPMI-6-341",
      "volume": "6",
      "year": "1993",
      "unstructured": "DICKINSON, M. J., MOLECULAR PLANT-MICROBE INTERACTIONS 6: 341 (1993).",
      "journal-title": "MOLECULAR PLANT-MICROBE INTERACTIONS"
    },
    {
      "key": "e_1_2_1_14_1",
      "first-page": "61",
      "volume": "3",
      "year": "1991",
      "unstructured": "DONG, X.N., INDUCTION OF ARABIDOPSIS DEFENSE GENES BY VIRULENT AND AVIRULENT PSEUDOMONAS-SYRINGAE STRAINS AND BY A CLONED AVIRULENCE GENE, PLANT CELL 3: 61 (1991).",
      "journal-title": "PLANT CELL"
    },
    {
      "key": "e_1_2_1_15_1",
      "doi-asserted-by": "crossref",
      "first-page": "3140",
      "DOI": "10.1016/S0021-9258(18)49965-6",
      "volume": "266",
      "year": "1991",
      "unstructured": "FARMER, E.E., OLIGOSACCHARIDE SIGNALING IN PLANTS - SPECIFICITY OF OLIGOURONIDE-ENHANCED PLASMA-MEMBRANE PROTEIN-PHOSPHORYLATION, JOURNAL OF BIOLOGICAL CHEMISTRY 266: 3140 (1991).",
      "journal-title": "JOURNAL OF BIOLOGICAL CHEMISTRY"
    },
    {
      "key": "e_1_2_1_16_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.8484117"
    },
    {
      "key": "e_1_2_1_17_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0003-2697(83)90418-9"
    },
    {
      "key": "e_1_2_1_18_1",
      "first-page": "8831",
      "volume": "88",
      "year": "1991",
      "unstructured": "FELIX, G, RAPID CHANGES OF PROTEIN-PHOSPHORYLATION ARE INVOLVED IN TRANSDUCTION OF THE ELICITOR SIGNAL IN PLANT-CELLS, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 88: 8831 (1991).",
      "journal-title": "PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA"
    },
    {
      "key": "e_1_2_1_19_1",
      "doi-asserted-by": "crossref",
      "first-page": "390",
      "DOI": "10.1094/MPMI-5-390",
      "volume": "5",
      "year": "1992",
      "unstructured": "FENSELAU, S, MOLECULAR PLANT-MICROBE INTERACTIONS 5: 390 (1992).",
      "journal-title": "MOLECULAR PLANT-MICROBE INTERACTIONS"
    },
    {
      "key": "e_1_2_1_20_1",
      "unstructured": "FRARY A unpublished data."
    },
    {
      "key": "e_1_2_1_21_1",
      "doi-asserted-by": "crossref",
      "first-page": "365",
      "DOI": "10.1146/annurev.py.28.090190.002053",
      "volume": "28",
      "year": "1990",
      "unstructured": "GABRIEL, D.W., WORKING MODELS OF SPECIFIC RECOGNITION IN PLANT-MICROBE INTERACTIONS, ANNUAL REVIEW OF PHYTOPATHOLOGY 28: 365 (1990).",
      "journal-title": "ANNUAL REVIEW OF PHYTOPATHOLOGY"
    },
    {
      "key": "e_1_2_1_22_1",
      "first-page": "6415",
      "volume": "83",
      "year": "1986",
      "unstructured": "GABRIEL, D.W., GENE-FOR-GENE INTERACTIONS OF 5 CLONED AVIRULENCE GENES FROM XANTHOMONAS-CAMPESTRIS PV MALVACEARUM WITH SPECIFIC RESISTANCE GENES IN COTTON, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 83: 6415 (1986).",
      "journal-title": "PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA"
    },
    {
      "key": "e_1_2_1_23_1",
      "doi-asserted-by": "crossref",
      "first-page": "384",
      "DOI": "10.1094/MPMI-5-384",
      "volume": "5",
      "year": "1992",
      "unstructured": "GOUGH, C. L., MOLECULAR PLANT-MICROBE INTERACTIONS 5: 384 (1992).",
      "journal-title": "MOLECULAR PLANT-MICROBE INTERACTIONS"
    },
    {
      "key": "e_1_2_1_24_1",
      "doi-asserted-by": "crossref",
      "first-page": "625",
      "DOI": "10.1042/bj2580625",
      "volume": "258",
      "year": "1989",
      "unstructured": "GRAND, RJA, ACYLATION OF VIRAL AND EUKARYOTIC PROTEINS, BIOCHEMICAL JOURNAL 258: 625 (1989).",
      "journal-title": "BIOCHEMICAL JOURNAL"
    },
    {
      "key": "e_1_2_1_25_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.2166336"
    },
    {
      "key": "e_1_2_1_26_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0076-6879(91)00126-H"
    },
    {
      "key": "e_1_2_1_27_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.3291115"
    },
    {
      "key": "e_1_2_1_28_1",
      "doi-asserted-by": "crossref",
      "first-page": "6878",
      "DOI": "10.1128/jb.174.21.6878-6885.1992",
      "volume": "174",
      "year": "1992",
      "unstructured": "HUANG, H.C., THE PSEUDOMONAS-SYRINGAE PV SYRINGAE-61 HRPH PRODUCT, AN ENVELOPE PROTEIN REQUIRED FOR ELICITATION OF THE HYPERSENSITIVE RESPONSE IN PLANTS, JOURNAL OF BACTERIOLOGY 174: 6878 (1992).",
      "journal-title": "JOURNAL OF BACTERIOLOGY"
    },
    {
      "key": "e_1_2_1_29_1",
      "doi-asserted-by": "crossref",
      "first-page": "520",
      "DOI": "10.1007/BF00305985",
      "volume": "70",
      "year": "1985",
      "unstructured": "HULBERT, S.H., LINKAGE ANALYSIS OF GENES FOR RESISTANCE TO DOWNY MILDEW (BREMIA-LACTUCAE) IN LETTUCE (LACTUCA-SATIVA), THEORETICAL AND APPLIED GENETICS 70: 520 (1985).",
      "journal-title": "THEORETICAL AND APPLIED GENETICS"
    },
    {
      "key": "e_1_2_1_30_1",
      "doi-asserted-by": "crossref",
      "first-page": "348",
      "DOI": "10.1094/MPMI-6-348",
      "volume": "6",
      "year": "1993",
      "unstructured": "JONES, D. A., MOLECULAR PLANT-MICROBE INTERACTIONS 6: 348 (1993).",
      "journal-title": "MOLECULAR PLANT-MICROBE INTERACTIONS"
    },
    {
      "key": "e_1_2_1_31_1",
      "doi-asserted-by": "crossref",
      "first-page": "133",
      "DOI": "10.1007/BF00226123",
      "volume": "81",
      "year": "1991",
      "unstructured": "KEEN, N.T., NEW DISEASE RESISTANCE GENES IN SOYBEAN AGAINST PSEUDOMONAS-SYRINGAE PV GLYCINEA - EVIDENCE THAT ONE OF THEM INTERACTS WITH A BACTERIAL ELICITOR, THEORETICAL AND APPLIED GENETICS 81: 133 (1991).",
      "journal-title": "THEORETICAL AND APPLIED GENETICS"
    },
    {
      "key": "e_1_2_1_32_1",
      "first-page": "301",
      "volume": "44",
      "year": "1954",
      "unstructured": "KING, E.O., 2 SIMPLE MEDIA FOR THE DEMONSTRATION OF PYOCYANIN AND FLUORESCIN, JOURNAL OF LABORATORY AND CLINICAL MEDICINE 44: 301 (1954).",
      "journal-title": "JOURNAL OF LABORATORY AND CLINICAL MEDICINE"
    },
    {
      "key": "e_1_2_1_33_1",
      "first-page": "157",
      "volume": "86",
      "year": "1989",
      "unstructured": "KOBAYASHI, D.Y., CLONED AVIRULENCE GENES FROM THE TOMATO PATHOGEN PSEUDOMONAS-SYRINGAE PV TOMATO CONFER CULTIVAR SPECIFICITY ON SOYBEAN, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 86: 157 (1989).",
      "journal-title": "PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA"
    },
    {
      "key": "e_1_2_1_34_1",
      "first-page": "2134",
      "volume": "7",
      "year": "1987",
      "unstructured": "MARK, G.E., DROSOPHILA-MELANOGASTER HOMOLOGS OF THE RAF ONCOGENE, MOLECULAR AND CELLULAR BIOLOGY 7: 2134 (1987).",
      "journal-title": "MOLECULAR AND CELLULAR BIOLOGY"
    },
    {
      "key": "e_1_2_1_35_1",
      "doi-asserted-by": "crossref",
      "first-page": "25",
      "DOI": "10.1007/BF00587557",
      "volume": "233",
      "year": "1992",
      "unstructured": "MARTIN, G. B., MOLECULAR & GENERAL GENETICS 233: 25 (1992).",
      "journal-title": "MOLECULAR & GENERAL GENETICS"
    },
    {
      "key": "e_1_2_1_36_1",
      "doi-asserted-by": "crossref",
      "first-page": "26",
      "DOI": "10.1094/MPMI-6-026",
      "volume": "6",
      "year": "1993",
      "unstructured": "MARTIN, G. B., MOLECULAR PLANT-MICROBE INTERACTIONS 6: 26 (1993).",
      "journal-title": "MOLECULAR PLANT-MICROBE INTERACTIONS"
    },
    {
      "key": "e_1_2_1_37_1",
      "first-page": "2336",
      "volume": "88",
      "year": "1991",
      "unstructured": "MARTIN, G.B., RAPID IDENTIFICATION OF MARKERS LINKED TO A PSEUDOMONAS RESISTANCE GENE IN TOMATO BY USING RANDOM PRIMERS AND NEAR-ISOGENIC LINES, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 88: 2336 (1991).",
      "journal-title": "PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA"
    },
    {
      "key": "e_1_2_1_38_1",
      "unstructured": "MARTIN G.B. unpublished data."
    },
    {
      "key": "e_1_2_1_39_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.8503004"
    },
    {
      "key": "e_1_2_1_40_1",
      "first-page": "515",
      "volume": "1",
      "year": "1989",
      "unstructured": "MESHI, T, MUTATIONS IN THE TOBACCO MOSAIC-VIRUS 30-KD PROTEIN GENE OVERCOME TM-2 RESISTANCE IN TOMATO, PLANT CELL 1: 515 (1989).",
      "journal-title": "PLANT CELL"
    },
    {
      "key": "e_1_2_1_41_1",
      "doi-asserted-by": "crossref",
      "first-page": "529",
      "DOI": "10.1007/BF00226787",
      "volume": "82",
      "year": "1991",
      "unstructured": "MESSEGUER, R, HIGH-RESOLUTION RFLP MAP AROUND THE ROOT-KNOT NEMATODE RESISTANCE GENE (MI) IN TOMATO, THEORETICAL AND APPLIED GENETICS 82: 529 (1991).",
      "journal-title": "THEORETICAL AND APPLIED GENETICS"
    },
    {
      "key": "e_1_2_1_42_1",
      "doi-asserted-by": "crossref",
      "first-page": "621",
      "DOI": "10.1093/genetics/120.3.621",
      "volume": "120",
      "year": "1988",
      "unstructured": "OCHMAN, H, GENETIC APPLICATIONS OF AN INVERSE POLYMERASE CHAIN-REACTION, GENETICS 120: 621 (1988).",
      "journal-title": "GENETICS"
    },
    {
      "key": "e_1_2_1_43_1",
      "doi-asserted-by": "crossref",
      "first-page": "523",
      "DOI": "10.2307/3869707",
      "volume": "5",
      "year": "1993",
      "unstructured": "RAZ, V, ETHYLENE SIGNAL IS TRANSDUCED VIA PROTEIN-PHOSPHORYLATION EVENTS IN PLANTS, PLANT CELL 5: 523 (1993).",
      "journal-title": "PLANT CELL"
    },
    {
      "key": "e_1_2_1_44_1",
      "doi-asserted-by": "crossref",
      "first-page": "1604",
      "DOI": "10.1128/jb.174.5.1604-1611.1992",
      "volume": "174",
      "year": "1992",
      "unstructured": "RONALD, P.C., THE CLONED AVIRULENCE GENE AVRPTO INDUCES DISEASE RESISTANCE IN TOMATO CULTIVARS CONTAINING THE PTO RESISTANCE GENE, JOURNAL OF BACTERIOLOGY 174: 1604 (1992).",
      "journal-title": "JOURNAL OF BACTERIOLOGY"
    },
    {
      "key": "e_1_2_1_45_1",
      "unstructured": "Sambrook J. Molecular Cloning: A Laboratory Manual (1989)."
    },
    {
      "key": "e_1_2_1_46_1",
      "doi-asserted-by": "crossref",
      "first-page": "755",
      "DOI": "10.1007/BF00262574",
      "volume": "78",
      "year": "1989",
      "unstructured": "SARFATTI, M, AN RFLP MARKER IN TOMATO LINKED TO THE FUSARIUM-OXYSPORUM RESISTANCE GENE I2, THEORETICAL AND APPLIED GENETICS 78: 755 (1989).",
      "journal-title": "THEORETICAL AND APPLIED GENETICS"
    },
    {
      "key": "e_1_2_1_47_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.3917576"
    },
    {
      "key": "e_1_2_1_48_1",
      "first-page": "6024",
      "volume": "81",
      "year": "1984",
      "unstructured": "Staskawicz, B. J., Proceedings of the National Academy of Sciences of the United States of America 81: 6024 (1984).",
      "journal-title": "Proceedings of the National Academy of Sciences of the United States of America"
    },
    {
      "key": "e_1_2_1_49_1",
      "first-page": "8816",
      "volume": "88",
      "year": "1991",
      "unstructured": "STEIN, J.C., MOLECULAR-CLONING OF A PUTATIVE RECEPTOR PROTEIN-KINASE GENE ENCODED AT THE SELF-INCOMPATIBILITY LOCUS OF BRASSICA-OLERACEA, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 88: 8816 (1991).",
      "journal-title": "PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA"
    },
    {
      "key": "e_1_2_1_50_1",
      "doi-asserted-by": "crossref",
      "first-page": "1141",
      "DOI": "10.1093/genetics/132.4.1141",
      "volume": "132",
      "year": "1992",
      "unstructured": "TANKSLEY, S.D., HIGH-DENSITY MOLECULAR LINKAGE MAPS OF THE TOMATO AND POTATO GENOMES, GENETICS 132: 1141 (1992).",
      "journal-title": "GENETICS"
    },
    {
      "key": "e_1_2_1_51_1",
      "doi-asserted-by": "crossref",
      "first-page": "284",
      "DOI": "10.1104/pp.99.1.284",
      "volume": "99",
      "year": "1992",
      "unstructured": "TOBIAS, C.M., AN ARABIDOPSIS-THALIANA GENE WITH SEQUENCE SIMILARITY TO THE S-LOCUS RECEPTOR KINASE OF BRASSICA-OLERACEA - SEQUENCE AND EXPRESSION, PLANT PHYSIOLOGY 99: 284 (1992).",
      "journal-title": "PLANT PHYSIOLOGY"
    },
    {
      "key": "e_1_2_1_52_1",
      "doi-asserted-by": "crossref",
      "first-page": "52",
      "DOI": "10.1094/MPMI-4-052",
      "volume": "4",
      "year": "1991",
      "unstructured": "VANKAN, J. A. L.,MOLECULAR PLANT-MICROBE INTERACTIONS 4: 52 (1991).",
      "journal-title": "MOLECULAR PLANT-MICROBE INTERACTIONS"
    },
    {
      "key": "e_1_2_1_53_1",
      "doi-asserted-by": "crossref",
      "first-page": "743",
      "DOI": "10.1038/345743a0",
      "volume": "345",
      "year": "1990",
      "unstructured": "WALKER, J.C., RELATIONSHIP OF A PUTATIVE RECEPTOR PROTEIN-KINASE FROM MAIZE TO THE S-LOCUS GLYCOPROTEINS OF BRASSICA, NATURE 345: 743 (1990).",
      "journal-title": "NATURE"
    },
    {
      "key": "e_1_2_1_54_1",
      "first-page": "443",
      "year": "1986",
      "unstructured": "Watterson, J. C., The Tomato Crop: A Scientific Basis for Improvement: 443 (1986).",
      "journal-title": "The Tomato Crop: A Scientific Basis for Improvement"
    },
    {
      "key": "e_1_2_1_55_1",
      "doi-asserted-by": "crossref",
      "first-page": "254",
      "DOI": "10.1007/BF00339589",
      "volume": "213",
      "year": "1988",
      "unstructured": "ZAMIR, D, TOMATO GENOME IS COMPRISED LARGELY OF FAST-EVOLVING, LOW COPY-NUMBER SEQUENCES, MOLECULAR & GENERAL GENETICS 213: 254 (1988).",
      "journal-title": "MOLECULAR & GENERAL GENETICS"
    }
  ],
  "container-title": "Science",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://www.science.org/doi/pdf/10.1126/science.7902614",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2024,
        1,
        15
      ]
    ],
    "date-time": "2024-01-15T04:31:57Z",
    "timestamp": 1705293117000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://www.science.org/doi/10.1126/science.7902614"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1993,
        11,
        26
      ]
    ]
  },
  "references-count": 55,
  "journal-issue": {
    "issue": "5138",
    "published-print": {
      "date-parts": [
        [
          1993,
          11,
          26
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1126/science.7902614"
  ],
  "URL": "http://dx.doi.org/10.1126/science.7902614",
  "relation": {},
  "ISSN": [
    "0036-8075",
    "1095-9203"
  ],
  "subject": [],
  "container-title-short": "Science",
  "published": {
    "date-parts": [
      [
        1993,
        11,
        26
      ]
    ]
  }
}