DOI: 10.1126/science.7638602. Structure of the <i>Arabidopsis RPM1</i> Gene Enabling Dual Specificity Disease Resistance

Structure of the Arabidopsis RPM1 Gene Enabling Dual Specificity Disease Resistance

10.1126/science.7638602

Crossref journal-article

American Association for the Advancement of Science (AAAS)

Science (221)

Abstract

Plants can recognize pathogens through the action of disease resistance ( R ) genes, which confer resistance to pathogens expressing unique corresponding avirulence ( avr ) genes. The molecular basis of this gene-for-gene specificity is unknown. The Arabidopsis thaliana RPM1 gene enables dual specificity to pathogens expressing either of two unrelated Pseudomonas syringae avr genes. Despite this function, RPM1 encodes a protein sharing molecular features with recently described single-specificity R genes. Surprisingly, RPM1 is lacking from naturally occurring, disease-susceptible Arabidopsis accessions.

Bibliography

Grant, M. R., Godiard, L., Straube, E., Ashfield, T., Lewald, J., Sattler, A., Innes, R. W., & Dangl, J. L. (1995). Structure of the Arabidopsis RPM1 Gene Enabling Dual Specificity Disease Resistance. Science, 269(5225), 843â846.

Authors 8

Murray R. Grant (first)
Laurence Godiard (additional)
Esther Straube (additional)
Tom Ashfield (additional)
Jürgen Lewald (additional)
Airlie Sattler (additional)
Roger W. Innes (additional)
Jeffery L. Dangl (additional)

References 41 Referenced 689

Ausubel F. Current Protocols in Molecular Biology (1987).
BECHTOLD, N, IN-PLANTA AGROBACTERIUM-MEDIATED GENE-TRANSFER BY INFILTRATION OF ADULT ARABIDOPSIS-THALIANA PLANTS, COMPTES RENDUS DE L ACADEMIE DES SCIENCES SERIE III-SCIENCES DE LA VIE-LIFE SCIENCES 316: 1194 (1993). / COMPTES RENDUS DE L ACADEMIE DES SCIENCES SERIE III-SCIENCES DE LA VIE-LIFE SCIENCES (1993)
10.1126/science.8091210
BISGROVE, S.R., A DISEASE RESISTANCE GENE IN ARABIDOPSIS WITH SPECIFICITY FOR 2 DIFFERENT PATHOGEN AVIRULENCE GENES, PLANT CELL 6: 927 (1994). / PLANT CELL (1994)
Crute, I., Arabidopsis: 705 (1994). / Arabidopsis (1994)
Dangl, J. L., Bacterial Pathogenesis of Plants and Animals: Molecular and Cellular Mechanisms 192: 99 (1994). (10.1007/978-3-642-78624-2_5) / Bacterial Pathogenesis of Plants and Animals: Molecular and Cellular Mechanisms (1994)
DANGL, J.L., PIECE DE RESISTANCE - NOVEL CLASSES OF PLANT-DISEASE RESISTANCE GENES, CELL 80: 363 (1995). (10.1016/0092-8674(95)90485-9) / CELL (1995)
DANGL, J.L., APPLICATIONS OF ARABIDOPSIS-THALIANA TO OUTSTANDING ISSUES IN PLANT-PATHOGEN INTERACTIONS, INTERNATIONAL REVIEW OF CYTOLOGY - A SURVEY OF CELL BIOLOGY, VOL 144 144: 53 (1993). (10.1016/S0074-7696(08)61513-2) / INTERNATIONAL REVIEW OF CYTOLOGY - A SURVEY OF CELL BIOLOGY, VOL 144 (1993)
DANGL, J.L., FUNCTIONAL HOMOLOGS OF THE ARABIDOPSIS RPM1 DISEASE RESISTANCE GENE IN BEAN AND PEA, PLANT CELL 4: 1359 (1992). / PLANT CELL (1992)
DANGL, J.L., THE MAJOR HISTOCOMPATIBILITY COMPLEX A-LA-CARTE - ARE THERE ANALOGIES TO PLANT-DISEASE RESISTANCE GENES ON THE MENU, PLANT JOURNAL 2: 3 (1992). (10.1111/j.1365-313X.1992.00003.x) / PLANT JOURNAL (1992)
DEBENER, T, IDENTIFICATION AND MOLECULAR MAPPING OF A SINGLE ARABIDOPSIS-THALIANA LOCUS DETERMINING RESISTANCE TO A PHYTOPATHOGENIC PSEUDOMONAS-SYRINGAE ISOLATE, PLANT JOURNAL 1: 289 (1991). (10.1046/j.1365-313X.1991.t01-7-00999.x) / PLANT JOURNAL (1991)
ECKER, J.R., METHODS 1: 186 (1990). (10.1016/S1046-2023(05)80134-3) / METHODS (1990)
ELLIS, J.G., CONTRASTING COMPLEXITY OF 2 RUST RESISTANCE LOCI IN FLAX, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 92: 4185 (1995). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1995)
10.1146/annurev.py.09.090171.001423
GRILL, E, CONSTRUCTION AND CHARACTERIZATION OF A YEAST ARTIFICIAL CHROMOSOME LIBRARY OF ARABIDOPSIS WHICH IS SUITABLE FOR CHROMOSOME WALKING, MOLECULAR & GENERAL GENETICS 226: 484 (1991). (10.1007/BF00260662) / MOLECULAR & GENERAL GENETICS (1991)
INNES, R.W., IDENTIFICATION OF A DISEASE RESISTANCE LOCUS IN ARABIDOPSIS THAT IS FUNCTIONALLY HOMOLOGOUS TO THE RPG1 LOCUS OF SOYBEAN, PLANT JOURNAL 4: 813 (1993). (10.1046/j.1365-313X.1993.04050813.x) / PLANT JOURNAL (1993)
INNES R.W. unpublished data.
JONES, D.A., ISOLATION OF THE TOMATO CF-9 GENE FOR RESISTANCE TO CLADOSPORIUM-FULVUM BY TRANSPOSON TAGGING, SCIENCE 266: 789 (1994). (10.1126/science.7973631) / SCIENCE (1994)
KEEN, N.T., GENE-FOR-GENE COMPLEMENTARITY IN PLANT-PATHOGEN INTERACTIONS, ANNUAL REVIEW OF GENETICS 24: 447 (1990). (10.1146/annurev.ge.24.120190.002311) / ANNUAL REVIEW OF GENETICS (1990)
10.1038/366751a0
10.1038/374183a0
KOBE, B, THE LEUCINE-RICH REPEAT - A VERSATILE BINDING MOTIF, TRENDS IN BIOCHEMICAL SCIENCES 19: 415 (1994). (10.1016/0968-0004(94)90090-6) / TRENDS IN BIOCHEMICAL SCIENCES (1994)
KONCZ, C, THE PROMOTER OF TL-DNA GENE 5 CONTROLS THE TISSUE-SPECIFIC EXPRESSION OF CHIMERIC GENES CARRIED BY A NOVEL TYPE OF AGROBACTERIUM BINARY VECTOR, MOLECULAR & GENERAL GENETICS 204: 383 (1986). (10.1007/BF00331014) / MOLECULAR & GENERAL GENETICS (1986)
LEWALD J unpublished data.
10.1126/science.7902614
Matallana, E., Methods in Arabidopsis Research: 144 (1992). / Methods in Arabidopsis Research (1992)
MINDRINOS, M, THE A-THALIANA DISEASE RESISTANCE GENE RPS2 ENCODES A PROTEIN CONTAINING A NUCLEOTIDE-BINDING SITE AND LEUCINE-RICH REPEATS, CELL 78: 1089 (1994). (10.1016/0092-8674(94)90282-8) / CELL (1994)
MOWERY P unpublished data.
PUTTERILL, J, CHROMOSOME WALKING WITH YAC CLONES IN ARABIDOPSIS - ISOLATION OF 1700 KB OF CONTIGUOUS DNA ON CHROMOSOME-5, INCLUDING A 300 KB REGION CONTAINING THE FLOWERING-TIME GENE CO, MOLECULAR & GENERAL GENETICS 239: 145 (1993). (10.1007/BF00281613) / MOLECULAR & GENERAL GENETICS (1993)
RILEY, J, A NOVEL, RAPID METHOD FOR THE ISOLATION OF TERMINAL SEQUENCES FROM YEAST ARTIFICIAL CHROMOSOME (YAC) CLONES, NUCLEIC ACIDS RESEARCH 18: 2887 (1990). (10.1093/nar/18.10.2887) / NUCLEIC ACIDS RESEARCH (1990)
Sambrook J. Molecular Cloning: A Laboratory Manual 2 (1989).
SARASTE, M, THE P-LOOP - A COMMON MOTIF IN ATP-BINDING AND GTP-BINDING PROTEINS, TRENDS IN BIOCHEMICAL SCIENCES 15: 430 (1990). (10.1016/0968-0004(90)90281-F) / TRENDS IN BIOCHEMICAL SCIENCES (1990)
Schmidt, R., Genome Analysis: Strategies for Physical Mapping 4: 71 (1992). / Genome Analysis: Strategies for Physical Mapping (1992)
SCHMIDT, R, ANALYSIS OF CLONES CARRYING REPEATED DNA-SEQUENCES IN 2 YAC LIBRARIES OF ARABIDOPSIS-THALIANA DNA, PLANT JOURNAL 5: 735 (1994). (10.1111/j.1365-313X.1994.00735.x) / PLANT JOURNAL (1994)
STASKAWICZ, B.J., CLONED AVIRULENCE GENE OF PSEUDOMONAS-SYRINGAE PV GLYCINEA DETERMINES RACE-SPECIFIC INCOMPATIBILITY ON GLYCINE-MAX (L) MERR, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES 81: 6024 (1984). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES (1984)
10.1126/science.7732374
TAMAKI, S, CHARACTERIZATION AND EXPRESSION OF 2 AVIRULENCE GENES CLONED FROM PSEUDOMONAS-SYRINGAE PV GLYCINEA, JOURNAL OF BACTERIOLOGY 170: 4846 (1988). (10.1128/jb.170.10.4846-4854.1988) / JOURNAL OF BACTERIOLOGY (1988)
Traut, T. W., European Journal of Biochemistry 222: 9 (1994). (10.1111/j.1432-1033.1994.tb18835.x) / European Journal of Biochemistry (1994)
WARD, E.R., ISOLATION OF SINGLE-COPY-SEQUENCE CLONES FROM A YEAST ARTIFICIAL CHROMOSOME LIBRARY OF RANDOMLY-SHEARED ARABIDOPSIS-THALIANA DNA, PLANT MOLECULAR BIOLOGY 14: 561 (1990). (10.1007/BF00027501) / PLANT MOLECULAR BIOLOGY (1990)
WHALEN, M.C., IDENTIFICATION OF PSEUDOMONAS-SYRINGAE PATHOGENS OF ARABIDOPSIS AND A BACTERIAL LOCUS DETERMINING AVIRULENCE ON BOTH ARABIDOPSIS AND SOYBEAN, PLANT CELL 3: 49 (1991). / PLANT CELL (1991)
10.1016/0092-8674(94)90283-6

Dates

Type	When
Created	18 years, 10 months ago (Oct. 27, 2006, 2:19 p.m.)
Deposited	1 year, 7 months ago (Jan. 14, 2024, 11:53 p.m.)
Indexed	1 week, 6 days ago (Aug. 19, 2025, 6:44 a.m.)
Issued	30 years ago (Aug. 11, 1995)
Published	30 years ago (Aug. 11, 1995)
Published Print	30 years ago (Aug. 11, 1995)

Funders 0

None

BibTeX

@article{Grant_1995, title={Structure of the Arabidopsis RPM1 Gene Enabling Dual Specificity Disease Resistance}, volume={269}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.7638602}, DOI={10.1126/science.7638602}, number={5225}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={Grant, Murray R. and Godiard, Laurence and Straube, Esther and Ashfield, Tom and Lewald, Jürgen and Sattler, Airlie and Innes, Roger W. and Dangl, Jeffery L.}, year={1995}, month=aug, pages={843–846} }

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