4 Genetic Analysis and Evolution of Plant Disease Resistance Genes
Annual Plant Reviews book series, Volume 4: Molecular Plant Pathology
Peter N. Dodds,
Gregory J. Lawrence,
A. Pryor,
Jeffrey G. Ellis,
Peter N. Dodds
Division of Plant Industry, CSIRO, GPO Box 1600, Canberra, ACT 2617 Australia
Search for more papers by this authorGregory J. Lawrence
Division of Plant Industry, CSIRO, GPO Box 1600, Canberra, ACT 2617 Australia
Search for more papers by this authorA. Pryor
Division of Plant Industry, CSIRO, GPO Box 1600, Canberra, ACT 2617 Australia
Search for more papers by this authorJeffrey G. Ellis
Division of Plant Industry, CSIRO, GPO Box 1600, Canberra, ACT 2617 Australia
Search for more papers by this authorPeter N. Dodds,
Gregory J. Lawrence,
A. Pryor,
Jeffrey G. Ellis,
Peter N. Dodds
Division of Plant Industry, CSIRO, GPO Box 1600, Canberra, ACT 2617 Australia
Search for more papers by this authorGregory J. Lawrence
Division of Plant Industry, CSIRO, GPO Box 1600, Canberra, ACT 2617 Australia
Search for more papers by this authorA. Pryor
Division of Plant Industry, CSIRO, GPO Box 1600, Canberra, ACT 2617 Australia
Search for more papers by this authorJeffrey G. Ellis
Division of Plant Industry, CSIRO, GPO Box 1600, Canberra, ACT 2617 Australia
Search for more papers by this authorThis article was originally published in 2000 in Molecular Plant Pathology, Volume 4 (ISBN 9781841271088) of the Annual Plant Reviews book series, this volume edited by Matthew Dickinson and Jim Beynon. The article was republished in Annual Plant Reviews online in April 2018.
Abstract
The sections in this article are
- Introduction
- Features of Cloned Resistance Genes
- Control of Resistance Gene Specificity
- Do Resistance Proteins Interact Directly with Avirulence Determinants?
- Organisation of Resistance Gene Loci
- Evolution of Resistance Genes by Divergent Selection
- Evolution of Resistance Genes by Recombination
- Concluding Remarks
References
- Aarts, N., Metz, M., Holub, E., Staskawicz, B.J., Daniels, M.J. and Parker, J.E. (1998) Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R-gene-mediated pathways in Arabidopsis . Proc. Natl. Acad. Sci. USA, 95 10306-11.
- Andersson, L. and Mikko, S. (1995) Generation of MHC class II diversity by intra- and intergenic recombination. Immunol. Rev., 143 6-12.
- Anderson, P.A., Lawrence, G.J., Morrish, B.C., Ayliffe, M.A., Finnegan, E.J. and Ellis, J.G. (1997) Inactivation of the flax rust resistance gene, M, associated with loss of a repeated unit within the leucine-rich repeat coding region. Plant Cell, 9 641-51.
- Bevan, J.R., Crute, I.R. and Clarke, D.D. (1993) Variation for virulence in Erysiphe fischeri from Senecio vulgaris . Plant Pathol., 42 622-35.
- Bevan, M., Bancroft, I., Bent, E., Love, K., Goodman, H., Dean, C., et al. (1998) Analysis of 1.9 Mb of contiguous sequence from chromosome 4 of Arabidopsis thaliana . Nature, 391 485-88.
- Bisgrove, S.R., Simonich, M.T., Smith, N.M., Sattler, A. and Innes, R.W. (1994) A disease resistance gene in Arabidopsis with specificity for two different pathogen avirulence genes. Plant Cell, 6 927-33.
- Botella, M.A., Coleman, M.J., Hughes, D.E., Nishimura, M.T., Jones, J.D.G. and Somerville, S.C. (1997) Map positions of 47 Arabidopsis sequences with sequence similarity to disease resistance genes. Plant J., 12 1197-211.
- Botella, M.A., Parker, J.E., Frost, L.N., Bittner-Eddy, P.D., Beynon, J.L., Daniels, M.J., Holub, E.B. and Jones, J.D.G. (1998) Three genes of the Arabidopsis Rpp1 complex resistance locus recognise distinct Peronospora parasitica avirulence determinants. Plant Cell, 10 1847-60.
- Braun, T., Schofield, P.R. and Sprengel, R. (1991) Amino-terminal leucine-rich repeats in gonadotropin receptors determine hormone selectivity. EMBO J., 10 1885-90.
- Cai, D., Kleine, M., Kifle, S., Harloff, H.-J., Sandal, N.N., Marcker, K.A., Klein-Lankhorst, R.M., Salentjin, E.M.J., Lange, W., Stiekema, W.J., et al. (1997) Positional cloning of a gene for nematode resistance in sugar beet. Science, 275 832-34.
- Century, K.S., Holub, E.B. and Staskawicz, B.J. (1995) NDR1, a locus of Arabidopsis thaliana that is required for disease resistance to both a bacterial and a fungal pathogen. Proc. Natl. Acad. Sci. USA, 92 6597-601.
- Century, K.S., Shapiro, A.D., Repetti, P.P., Dahlbeck, D., Holub, E. and Staskawicz, B.J. (1997) NDR1, a pathogen-induced component required for Arabidopsis disease resistance. Science, 278 1963-65.
- Cheng, J., Smith-Becker, J. and Keen, N.T. (1998) Genetics of plant-pathogen interactions. Curr. Opin. Plant Biotechnol., 9 202-207.
- Chinnaiyan, A.M., Chaudhary, D., O'Rourke, K., Koonin, E.V. and Dixit, V.M. (1997) Role of CED-4 in the activation of CED-3. Nature, 338 728-29.
- Collins, N.C., Webb, C.A., Seah, S., Ellis, J.G., Hulbert, S.H. and Pryor, A. (1998) The isolation and mapping of disease resistance gene analogs in maize. Mol. Plant-Microbe Interact., 11 968-78.
- Collins, N., Drake, J., Ayliffe, M., Sun, Q., Ellis, J., Hulbert, S. and Pryor, T. (1999) Molecular characterisation of the maize Rp1-D rust resistance haplotype and its mutants. Plant Cell, 11 1365-76.
- Collmer, A. (1998) Determinants of pathogenicity and avirulence in plant pathogenic bacteria. Curr. Opin. Plant Biol., 1 329-35.
- Delaney, D.E., Webb, C.A. and Hulbert, S.H. (1998) A novel rust resistance gene showing overdominance. Mol. Plant-Microbe Interact., 11 242-45.
- De Wit, P.J.G.M. (1997) Pathogen avirulence and plant resistance: a key role for recognition. Trends Plant Sci., 2 452-58.
- Dixon, M.S., Jones, D.A., Keddie, J.S., Thomas, C.M., Harrison, K. and Jones, J.D.G. (1996) The tomato Cf-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins. Cell, 84 451-59.
- Dixon, M.S., Hatzixanthis, K., Jones, D.A., Harrison, K. and Jones, J.D.G. (1998) The tomato Cf-5 disease resistance gene and six homologues show pronounced allelic variation in leucine-rich repeat copy number. Plant Cell, 10 1915-25.
- Ellis, J. and Jones, D. (1998) Structure and function of proteins controlling strain-specific pathogen resistance in plants. Curr. Opin. Plant Biol., 1 288-93.
- Ellis, J.G., Lawrence, G., Ayliffe, M., Anderson, P., Collins, N., Finnegan, J., Frost, D., Luck, J. and Pryor, T. (1997) Advances in the molecular genetic analysis of the flax-flax rust interaction. Annu. Rev. Phytopathol., 35 271-91.
- Ellis, J.G., Lawrence, G.J., Luck, J.E. and Dodds, P.N. (1999) Identification of regions in alleles of the flax rust resistance gene, L, that determine differences in gene-for-gene specificity. Plant Cell, 11 495-506.
- Endo, T., Ikeo, K. and Gojobori, T. (1996) Large scale search for genes on which positive selection may operate. Mol. Biol. Evolut., 13 685-90.
- Falk, A., Feys, B.J., Frost, L.N., Jones, J.D.G., Daniels, M.J. and Parker, J.E. (1999) EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases. Proc. Natl. Acad. Sci. USA, 96 3292-97.
- Flor, H.H. (1971) Current status of the gene-for-gene concept. Annu. Rev. Phytopathol., 9 275-96.
- Frank, S.A. (1992) Models of plant-pathogen co-evolution. Trends Genet., 8 213-19.
- Grant, M.R., Godiard, L., Straube, E., Ashfield, T., Lewald, J., Sattler, A., Innes, R.W. and Dangl, J.L. (1995) Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science, 269 843-46.
- Grant, M.R., McDowell, J.M., Sharpe, A., de Torres Zabala, M., Lydiates, D.J. and Dangl, J.E. (1998) Independent deletions of a pathogen-resistance gene in Brassica and Arabidopsis . Proc. Natl. Acad. Sci. USA, 95 15843-48.
- Hu, G. and Hulbert, S. (1996) Construction of ‘compound’ rust resistance genes in maize. Euphytica, 87 47-51.
- Hu, G., Richter, T.E., Hulbert, S. and Pryor, T. (1996) Disease lesion mimicry caused by mutations in the rust resistance gene, Rp1 . Plant Cell, 8 1367-76.
- Hughes, A.L. (1995) Origin and evolution of HLA class I pseudogenes. Mol. Biol. Evolut., 12 247-58.
- Hughes, A.L. and Nei, M. (1988) Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature, 335 167-70.
- Ishimizu, T., Endo, T., Yamaguchi-Kabata, Y., Nakamura, K.T., Sakiyama, F. and Norioka, S. (1998) Identification of regions in which positive selection may act in S-RNase of Rosaceae: implication for S-allele-specific recognition sites in S-RNases. FEBS Lett., 440 337-42.
- Islam, M.R. and Shepherd, K.W. (1991) Present status of genetics of rust resistance in flax. Euphytica, 55 255-67.
- Jones, D.A., Thomas, C.M., Hammond-Kossack, K.E., Balint-Kurti, P.J. and Jones, J.D.G. (1994) Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science, 266 789-93.
- Kanazin, V., Marek, L.F. and Shoemaker, R.C. (1996) Resistance gene analogs are conserved and clustered in soybean. Proc. Natl. Acad. Sci. USA, 93 11746-50.
- Kobe, B. and Diesenhofer, J. (1994) The leucine-rich repeat: a versatile binding motif. Trends Biol. Sci., 19 415-21.
- Kobe, B. and Diesenhofer, J. (1995) A structural basis of the interactions between leucine-rich repeats and protein ligands. Nature, 374 183-86.
- Kooman-Gersmann, M., Honee, G., Bonnema, G. and de Wit, P.J.G.M. (1996) A high-affinity binding site for the AVR9 peptide elicitor of Cladosporium fulvum is present on plasma membranes of tomato and other solanaceous plants. Plant Cell, 8 929-38.
- Kunkel, B.N. (1996) A useful weed put to work: genetic analysis of disease resistance in Arabidopsis thaliana . Trends Genet., 12 63-69.
- Lagudah, E.S., Moullet, O. and Appels, R. (1997) Map-based cloning of a gene sequence encoding a nucleotide-binding domain and leucine-rich region at the Cre3 nematode resistance locus of wheat. Genome, 40 659-65.
- Lauge, R. and de Wit, P.J.G.M. (1998) Fungal avirulence genes—structure and possible functions. Fungal Genet. Biol., 24 285-97.
- Lawrence, G.J., Finnegan, E.J., Ayliffe, M.A. and Ellis J.G. (1995) The L6 gene for flax resistance is related to the Arabidopsis bacterial resistance gene, Rps2, and the tobacco viral resistance gene, N. Plant Cell, 7 1195-206.
- Leister, D., Ballvora, A., Salamini, F. and Gebhardt, C. (1996) A PCR-based approach for isolating pathogen resistance genes from potato with potential for wide application in plants. Nature Genet., 14 421-29.
- Leister, D., Kurth, J., Laurie, D.A., Yano, D.A., Sasaki, T., Devos, K., Graner. A. and Schulze-Lefert, P. (1998) Rapid reorganisation of resistance gene homologues in cereal genomes. Proc. Natl. Acad. Sci. USA, 95 370-75.
- Leister, D., Kurth, J., Laurie, D.A., Yano, D.A., Sasaki, T., Graner, A. and Schulze-Lefert, P. (1999) RFLP and physical mapping of resistance gene homologues in rice (O. sativa) and barley (H. vulgare). Theor. Appl. Genet., 98 509-20.
- Lemaitre, B., Nicolas, E., Michaut, L., Reichhart, J.-M. and Hoffmann, J.A. (1996) The dorsoventral regulatory cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell, 86 973-83.
- Li, H.-W., Lucy, A.P., Guo, H.-S., Li, W.-X., Ji, L.-H., Wong, S.-M. and Ding, S.-W. (1999) Strong host resistance targeted against a viral suppressor of the plant gene silencing defence mechanism. EMBO J., 18 2683-91.
- Luck, J.E. (1998) Transposition and recombination events in flax rust resistance genes. PhD thesis, Australian National University, Australia.
- Martin, G.B., Brommonschenkel, S.H., Chunwongse, J., Frary, A., Gana, M.W., Spivey, R., Wu, T., Earle, E.D. and Tanksley, S.D. (1993) Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science, 262 1432-36.
- Martin, G.B., Frary, A., Wu, T., Brommonschenkel, S., Chunwongse, J., Earle, E.D. and Tanksley, S.D. (1994) A member of the Pto gene family confers sensitivity to fenthion resulting in rapid cell death. Plant Cell, 6 1543-52.
- Matthieu, H.A.J.J., Cozijnsen, T.J. and de Wit, P.J.G.M. (1994) Host resistance to a fungal tomato pathogen lost by a single base-pair change in an avirulence gene. Nature, 367 384-86.
- McDowell, J.M., Dhandaydham, M., Long, T.A., Aarts, M.G.M., Goff, S., Holub, E.B. and Dangl, J.E. (1998) Intragenic recombination and diversifying selection contribute to the evolution of downy mildew resistance at the Rpp8 locus of Arabidopsis . Plant Cell, 10 1861-74.
- Medzhitov, R., Preston-Hurlburt, P. and Janeway, C.A. (1997) A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature, 338 394-97.
- Meyers, B.C., Chin, D.B., Shen, K.A., Sivaramakrishnan, S., Lavelle, D.O., Zhang, Z. and Michelmore, R.W. (1998a) The major resistance gene cluster in lettuce is highly duplicated and spans several megabases. Plant Cell, 10 1817-32.
- Meyers, B.C., Shen, K.A., Rohani, P., Gaut, B.S. and Michelmore, R.W. (1998b) Receptor-like genes in the major resistance locus of lettuce are subject to divergent selection. Plant Cell, 10 1833-46.
- Milligan, S.B., Bodeau, J., Yaghoobi, J., Kaloshian, I., Zabel, P. and Williamson, V.M. (1998) The root knot nematode resistance gene, Mi, from tomato is a member of the leucine zipper, nucleotide-binding, leucine-rich repeat family of plant genes. Plant Cell, 10 1307-19.
- Mindrinos, M., Katagiri, F., Yu, G.L. and Ausubel, F. (1994) The A. thaliana disease resistance gene, RPS2, encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell, 78 1089-99.
- Ori, N., Eshed, Y., Paran, I., Presting, G., Aviv, D., Tanksley, S., Zamir, D. and Fluhr, R. (1997) The 12C family from the wilt disease resistance locus 12 belongs to the nucleotide-binding, leucine-rich repeat superfamily of plant resistance genes. Plant Cell, 9 521-32.
- Papageorgiou, A.C., Shapiro, R. and Acharya, K.R. (1997) Molecular recognition of human angiogenin by placental ribonuclease inhibitor—an X-ray crystallographic study at 2.0 Å resolution. EMBO J., 16 5162-77.
- Parham, P. and Ohta, T. (1996) Population biology of antigen presentation by MHC class I molecules. Science, 272 67-74.
- Parker, J.E., Holub, E.B., Frost, L.N., Falk, A., Gunn, N.D. and Daniels, M.J. (1996) Characterisation of eds1, a mutation in Arabidopsis suppressing resistance to Peronospora parasitica specified by several different RPP genes. Plant Cell, 8 2033-46.
- Parker, J.E., Coleman, M.J., Szabo, V., Frost, L.N., Schmidt, R., van der Biezen, E.A., Moores, T., Dean, C., Daniels, M.J. and Jones, J.D.G. (1997) The Arabidopsis downy mildew resistance gene, Rpp5, shares similarity to the Toll and interleukin-1 receptors with N and L6 . Plant Cell, 9 879-94.
- Parniske, M., Hammond-Kosack, K.E., Golstein, C., Thomas, C.M., Jones, D.A., Harrison, K., Wulff, B.B.H. and Jones, J.D.G. (1997) Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomato. Cell, 91 821-32.
- Rausher, M.D. (1996) Genetic analysis of co-evolution between plants and their natural enemies. Trends Genet., 12 212-17.
- Richter, T.E., Pryor, T.J., Bennetzen, J.L. and Hulbert, S.H. (1995) New rust resistance specificities associated with recombination in the Rp1 complex in maize. Genetics, 141 373-81.
- Rossi, M., Goggin, F.L., Milligan, S.B., Kaloshian, I., Ullman, D.E. and Williamson, V.M. (1998) The nematode resistance gene, Mi, of tomato confers resistance against the potato aphid. Proc. Natl. Acad. Sci. USA, 95 9750-54.
- Salmeron, J.M., Barker, S.J., Carland, F.M., Mehta, A.Y. and Staskawicz, B.J. (1994) Tomato mutants altered in bacterial disease resistance provide evidence for a new locus controlling pathogen recognition. Plant Cell, 6 511-20.
- Salmeron, J.M., Oldroyd, G.E.D., Rommens, C.M.T., Scofield, S.R., Kim, H.-S., Lavelle, D.T., Dahlbeck, D. and Staskawicz, B.J. (1996) Tomato Prf is a member of the leucine-rich repeat class of plant disease resistance genes and lies embedded within the Pto kinase gene cluster. Cell, 86 123-33.
- Scofield, S.R., Tobias, C.M., Rathjen, J.P., Chang, J.H., Lavelle, D.T., Michelmore, R.W. and Staskawicz, B.J. (1996) Molecular basis of gene-for-gene specificity in bacterial speck disease of tomato. Science, 274 2063-65.
- Seah, S., Sivasithamparan, K., Karakousis, A. and Lagudah, E.S. (1998) Cloning and characterisation of a family of disease resistance gene analogs from wheat and barley. Theor. Appl. Genet., 97 937-45.
- Shen, K.A., Meyers, B.C., Islam-Faridi, M.N., Chin, D.B., Stelly, M. and Michelmore R.W. (1998) Resistance gene candidates identified using PCR with degenerate oligonucleotide primers map to resistance gene clusters in lettuce. Mol. Plant-Microbe Interact., 11 815-23.
- Song, W.-Y., Wang, G.-L., Chen, L.-L., Kim, H.-S., Pi, L.-Y., Holsten, T., Gardner, J., Wang, B., Zhai, W.-X., Zhu, L.-H., Fauquet, C. and Ronald, P. (1995) A receptor-like protein encoded by the rice disease resistance gene, Xa21. Science, 270 1804-806.
- Song, W.-Y., Pi, L.-Y., Wang, G.-L., Gardner, J., Holsten, T. and Ronald, P. (1997) Evolution of the rice Xa21 disease resistance gene family. Plant Cell, 9 1279-87.
- Sudupak, M.A., Bennetzen, J.L. and Hulbert, S.H. (1993) Unequal exchange and meiotic instability of disease resistance genes in the Rp1 region of maize. Genetics, 131 119-25.
- Suzuki, N., Choe, H.-R., Nishida, Y., Yamawaki-Kataoka, Y., Ohnishi, S., Tamaoki, T. and Katoka, T. (1990) Leucine-rich repeats and carboxyl terminus regions are required for interaction of yeast adenylate cyclase with RAS proteins. Proc. Natl. Acad. Sci. USA, 87 8711-15.
- Tang, X., Frederick, R.D., Zhou, J., Halterman, D.A., Jia, Y. and Martin, G.B. (1996) Physical interaction of avrPto and the Pto kinase defines a recognition event involved in plant disease resistance. Science, 274 2060-63.
- Thomas, C.M., Jones, D.A., Parniske, M., Harrison, K., Balint-Kurti, P., Hatzixanthis, K. and Jones, J.D.G. (1997) Characterisation of the tomato Cf-4 gene for resistance to Cladosporium fulvum identifies sequences that determine recognitional specificity in Cf-4 and Cf-9. Plant Cell, 9 2209-24.
- Traut, T.W. (1994) The functions and consensus motifs of nine types of peptide segments that form different types of nucleotide-binding sites. Eur. J. Biochem., 222 9-19.
- van den Ackerveken, G.F.J.M., Vossen, P. and de Wit, P.J.G.M. (1993) The avr9 race specific elicitor of Cladosporium fulvum is processed by endogenous and plant proteases. Plant Physiol., 103 91-96.
- van der Biezen, E.A. and Jones, J.D.G. (1998) The NB-ARC domain: a novel signalling motif shared by plant resistance genes products and regulators of cell death in animals. Curr. Biol., 8 R226-R227.
- Volpe, F., Clatworthy, J., Kaptein, A., Maschera, B., Griffin, A.-M. and Ray, K. (1997) The IL-1 receptor accessory protein is responsible for the recruitment of the interleukin-1 receptor associated kinase to the IL-1/IL-1 receptor I complex. FEBS Lett., 419 41-44.
- Warren, R.F., Henk, A.. Mowery, P., Holub, E. and Innes, R.W. (1998) A mutation within the leucine-rich repeat domain of the Arabidopsis disease resistance gene, Rps5, partially suppresses multiple bacterial and downy mildew resistance genes. Plant Cell, 10 1439-52.
- Whitham, S., Dinesh-Kumar, S.P., Choi, D., Hehl, R., Corr, C. and Baker, B. (1994) The product of the tobacco mosaic virus resistance gene, N: similarity to Toll and the interleukin-1 receptor. Cell, 78 1101-15.
- Yang, J. and Steward, R. (1997) A multimeric complex and the nuclear targeting of the Drosophila rel protein dorsal. Proc. Natl. Acad. Sci. USA, 94 14524-29.
- Yoshimura, S., Yamanouchi, U., Katayose, Y., Toki, S., Wang, Z.-Z., Kono, I., Kurata, N., Yano, M., Iwata, N. and Sasaki, T. (1998) Expression of Xa1, a bacterial blight-resistance gene in rice, is induced by bacterial inoculation. Proc. Natl. Acad. Sci. USA, 95 1663-68.
- Yu, Y.G., Buss, G.R. and Maroof, M.A.S. (1996) Isolation of a superfamily of candidate disease resistance genes in soybean, based on a conserved nucleotide-binding site. Proc. Natl. Acad. Sci. USA, 93 11751-56.
- Yucel, I., Midland, S.L., Sims, J.J. and Keen, N.T. (1994) Class I and Class II avrD alleles direct the production of different products in Gram-negative bacteria. Mol. Plant-Microbe Interact., 7 148-50.
- Zhou, J., Loh, Y.-T., Bressan, R.A. and Martin, G.B. (1995) The tomato gene, Pti1, encodes a serine/threonine kinase that is phosphorylated by Pto and is involved in the hypersensitive response. Cell, 83 925-35.
- Zhou, J., Tang, X. and Martin, G.B. (1997) The Pto kinase conferring resistance to tomato bacterial speck disease interacts with proteins that bind a cis-element of pathogenesis-related genes. EMBO J., 16 3207-18.
Citing Literature
Browse other articles of this reference work:
