Abstract
Plants have developed efficient mechanisms to avoid infection or to mount responses that render them resistant upon attack by a pathogen. One of the best-studied defence mechanisms is based on gene-for-gene resistance through which plants, harbouring specific resistance (R) genes, specifically recognise pathogens carrying matching avirulence (Avr) genes. Here a review of the R genes that have been cloned is given. Although in most cases it is not clear how R gene encoded proteins initiate pathways leading to disease resistance, we will show that there are clear parallels with disease prevention in animal systems. Furthermore, some evolutionary mechanisms acting on R genes to create novel recognitional specificities will be discussed.
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Aarts N, Metz M, Holub E, Staskawicz BJ, Daniels MJ and Parker JE (1998) Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. Proc Natl Acad Sci USA 95: 10306–10311
Anderson PA, Lawrence GJ, Morrish BC, Ayliffe MA, Finnegan EJ and Ellis JG (1997) Inactivation of the flax rust resistance geneMassociated with loss of a repeated unit within the leucine-rich repeat coding region. Plant Cell 9: 641–651
Baker B, Zambryski P, Staskawicz B and Dinesh-Kumar SP (1997) Signaling in plant-microbe interactions. Science 276: 726–733
Bendahmane A, Kanyuka K and Baulcombe DC (1999) The Rx gene from potato controls separate virus resistance and cell death responses. Plant Cell 11: 781–791
Bent AF (1996) Plant disease resistance genes-function meets structure. Plant Cell 8: 1757–1771
Bent AF, Kunkel BN, Dahlbeck D, Brown KL, Schmidt R, Giraudat J, Leung J and Staskawicz BJ (1994) RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. Science 265: 1856–1860
Bonas U and Van den Ackerveken G (1999) Gene-for-gene interactions: bacterial avirulence proteins specify plant disease resistance. Curr Opin Microbiol 2: 94–98
Botella MA, Parker JA, Frost LN, Bittner-Eddu PD, Beydon JL, Daniels MJ, Holub EB and Jones JDG (1998) Three genes of the Arabidopsis RPP1 complex resistance locus recognize distinct Peronospora parasitica avirulence determinants. Plant Cell 10: 1847–1860
Bourne HR, Sanders DA and McCormick F (1991) The GTPase superfamily: conserved structure and molecular mechanism. Nature 349: 117–127
Boyes DC, Nam J and Dangl JL (1998) The Arabidopsis thaliana RPM1 disease resistance gene product is a peripheral plasma membrane protein that is degraded coincident with the hypersensitive response. Proc Natl Acad Sci USA 95: 15849–15854
Braun CJ, Siedow JN, Williams ME and Levings CSD (1989) Mutations in the maize mitochondrial T-urf13 gene eliminate sensitivity to a fungal pathotoxin. Proc Natl Acad Sci USA 86: 4435–4439
Brosch G, Ransom R, Lechner T, Walton JD and Loidl P (1995) Inhibition of maize histone deacetylases by HC toxin, the host-selective toxin of Cochliobolus carbonum. Plant Cell 7: 1941–1950
Bryan CT, Jia Y, Farrall KS, Hershey HP, McAdams SA, Faulk KN, Donaldson GK, Tarchini R and Valent B (1999) Molecular characterization of resistance gene/avirulence gene interactions in the rice blast system. 9th International Congress on Molecular Plant-Microbe Interactions, Amsterdam. In: Wit PJGM, Bisseling T and Stiekema WJ (eds) Biology of Plant-Microbe Interactions, Vol 2 (pp 35–39) De 0–9654625–1-X
Büschges R, Hollricher K, Panstruga R, Simons G, Wolter M, Frijters A, van Daelen R, van der Lee T, Diergaarde P, Groenendijk J, Topsch S, Vos P, Salamini F and Schulze-Lefert P (1997) The barley Mlo gene: a novel control element of plant pathogen resistance. Cell 88: 695–705
Cai D, Kleine M, Kifle S, Harloff HJ, Sandal NN, Marcker KA, Klein-Lankhorst RM, Salentijn EMJ, Lange W, Stiekema WJ, Wyss U, Grundler FMW and Jung C (1997) Positional cloning of a gene for nematode resistance in sugar beet. Science 275: 832–834
Cao H, Glazebrook J, Clarke JD, Volko S and Dong XN (1997) The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88: 57–63
Cao H, Li X and Dong XN (1998) Generation of broad-spectrum disease resistance by overexpression of an essential regulatory gene in systemic acquired resistance. Proc Natl Acad Sci USA 95: 6531–6536
Century KS, Shapiro AD, Repetti PP, Dahlbeck D, Holub E and Staskawicz BJ (1997) NDR1, a pathogen-induced component required for Arabidopsis disease resistance. Science 278: 1963–1965
Collins N, Drake J, Ayliffe M, Sun Q, Ellis J, Hulbert S and Pryor T (1999) Molecular characterization of the maize Rp1-D rust resistance haplotype and its mutants. Plant Cell 11: 1365–1376
Dangl JL (1999) Mechanisms of specific disease resistance: current understanding and future challenges. 9th International Congress on Molecular Plant-Microbe Interactions, Amsterdam
Dangl JL, Dietrich RA and Richberg MH (1996) Death don't have no mercy: cell death programs in plant-microbe interactions. Plant Cell 8: 1793–1807
Delaney TP (1997) Genetic dissection of acquired resistance to disease. Plant Phys 113: 5–12
Dixon MS, Jones DA, Keddie JS, Thomas CM, Harrison K and Jones JDG (1996) The tomato Cf-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins. Cell 84: 451–459
Dixon MS, Hatzixanthis K, Jones DA, Harrison K and Jones JDG (1998) The tomato Cf-5 disease resistance gene and six homologs show pronounced allelic variation in leucine-rich repeat copy number. Plant Cell 10: 1915–1925
Doke N, Miura Y, Sanchez LM, Park HJ, Noritake T, Yoshioka H and Kawakita K (1996) The oxidative burst protects plants against pathogen attack: mechanism and role as an emergency signal for plant bio-defence. Gene 179: 45–51
Ellis J, 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-rust interaction. Annu Rev Phytopathol 35: 271–291
Endo T, Ikeo K and Gojobori T (1996) Large-scale search for genes on which positive selection may operate. Mol Biol Evol 13: 685–690
Falk A, Feys BJ, Frost LN, Jones JDG, Daniels MJ and Parker JE (1999) EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases. Proc Natl Acad Sci USA 96: 3292–3297
Fields S and Song O (1989) A novel genetic system to detect protein-protein interactions. Nature 340: 245–246
Fletcher JC, Brand U, Running MP, Simon R and Meyerowitz EM (1999) Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283: 1911–1914
Freialdenhoven A, Peterhansel C, Kurth J, Kreuzaler F and Schulze-Lefert P (1996) Identification of genes required for the function of non-race-specific Mlo resistance to powdery mildew in barley. Plant Cell 8: 5–14
Gassmann W, Hinsch ME and Staskawicz BJ (1999) The Arabidopsis RPS4 bacterial-resistance gene is a member of the TIR-NBS-LRR family of disease-resistance genes. Plant J 20: 265–277
Glazebrook J (1999) Genes controlling expression of defense responses in Arabidopsis. Curr Opin Plant Biol 2: 280–286
Grant MR, Godiard L, Straube E, Ashfield T, Lewald J, Sattler A, Innes RW and Dangl JL (1995) Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science 269: 843–846
Greenberg JT (1997) Programmed cell death in plant-pathogen interactions. Annu Rev Plant Physiol Plant Mol Biol 48: 525–545
Groom QJ, Torres MA, Fordham-Skelton AP, Hammond-Kosack KE, Robinson NJ and Jones JDG (1996) rbohA, a rice homologue of the mammalian gp91phox respiratory burst oxidase gene. Plant J 10: 515–522
Haanstra JPW (2000) Characterization of resistance genes to Cladosporium fulvum on the short arm of chromosome 1 of tomato. PhD thesis Plant breeding, Wageningen University, Wageningen.
Hammond-Kosack KE and Jones JDG (1996) Resistance genedependent plant defense responses. Plant Cell 8: 1773–1791
Hammond-Kosack KE and Jones JDG (1997) Plant disease resistance genes. Annu Rev Plant Physiol Plant Mol Biol 48: 575–607
Hammond-Kosack KE, Jones DA and Jones JDG (1994) Identifi-cation of two genes required in tomato for full Cf-9-dependent resistance to Cladosporium fulvum. Plant Cell 6: 361–374
Hashimoto C, Hudson KL and Anderson KV (1988) The Toll gene of Drosophila, required for dorsal-ventral embryonic polarity, appears to encode a transmembrane protein. Cell 52: 269–279
Heath MC (1998) Apoptosis, programmed cell death and the hypersensitive response. Eur J Plant Pathol 104: 117–124
Higgins VJ, Lu HG, Xing T, Gelli A and Blumwald E (1998) The gene-for-gene concept and beyond: interactions and signals. Can J Plant Path 20: 150–157
Hughes AL and Nei M (1988) Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335: 167–170
Jarosch B, Kogel KH and Schaffrath U (1999) The ambivalence of the barley Mlo locus: mutations conferring resistance against powdery mildew (Blumeria graminis f.sp, hordei) enhance susceptibility to the rice blast fungus Magnaporthe grisea. Mol Plant-Microbe Interact 12: 508–514
Jeong S, Trotochaud AE and Clark SE (1999) The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability of the CLAVATA1 receptor-like kinase. Plant Cell 11: 1925–1933
Ji C, Boyd C, Slaymaker D, Okinaka Y, Takeuchi Y, Midland SL, Sims JJ, Herman E and Keen N (1998) Characterization of a 34-kDa soybean binding protein for the syringolide elicitors. Proc Natl Acad Sci USA 95: 3306–3311
Jirage D, Tootle TL, Reuber TL, Frost LN, Feys BJ, Parker JE, Ausubel FM and Glazebrook J (1999) Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling. Proc Natl Acad Sci USA 96: 13583–13588
Johal GS and Briggs SP (1992) Reductase activity encoded by the HM1 disease resistance gene in maize. Science 258: 985–987
Jones DA and Jones JDG (1996) The roles of leucine-rich repeat proteins in plant defences. Adv Bot Res Inc Adv Plant Pathol 24: 89–167
Jones DA, Thomas CM, Hammond-Kosack KE, Balint-Kurti PJ and Jones JDG (1994) Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science 266: 789–793
Jones JDG (1994) Plant pathology. Paranoid plants have their genes examined. Curr Biol 4: 749–751
Jones JDG (1997) Plant disease resistance-a kinase with keen eyes. Nature 385: 397–398
Joosten MHAJ and De Wit PJGM (1999) The tomato-Cladosporium fulvum interaction: a versatile experimental system to study plant-pathogen interactions. Annu Rev Phytopathol 37: 335–367
Joosten MHAJ, Vogelsang R, Cozijnsen TJ, Verberne MC and De Wit PJGM (1997) The biotrophic fungus Cladosporium fulvum circumvents Cf-4-mediated resistance by producing unstable AVR4 elicitors. Plant Cell 9: 367–379
Kataoka T, Broek D and Wigler M (1985) DNA sequence and characterization of the S. cerevisiae gene encoding adenylate cyclase. Cell 43: 493–505
Kearney B and Staskawicz BJ (1990) Widespread distribution and fitness contribution of Xanthomonas campestris avirulence gene avrBs2. Nature 246: 385–386
Knogge W (1996) Fungal infection of plants. Plant Cell 8: 1711–1722
Kobe B and Deisenhofer J (1993) Crystal structure of porcine ribonuclease inhibitor, a protein with leucine-rich repeats. Nature 366: 751–756
Kobe B and Deisenhofer J (1994) The leucine-rich repeat: a versatile binding motif. Trends Biochem Sci 19: 415–421
Kooman-Gersmann M (1998) The Avr9 elicitor peptide of Cladosporium fulvum; Molecular aspects of recognition. PhD thesis Phytopathology, Wageningen University, Wageningen.
Kooman-Gersmann M, Honée G, Bonnema G and De Wit PJGM (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: 929–938
Kumar S and Colussi PA (1999) Prodomains-adaptors-oligomerization: the pursuit of caspase activation in apoptosis. Trends Biochem Sci 24: 1–4
Lagudah ES, Moullet O and Appels R (1997) Map-based cloning of a gene sequence encoding a nucleotide-binding domain and a leucine-rich region at the Cre3 nematode resistance locus of wheat. Genome 40: 659–665
Lahaye T, Hartmann S, Topsch S, Freialdenhoven A, Yano M and Schulze-Lefert P (1998) High-resolution genetic and physical mapping of the Rar1 locus in barley. Theor Appl Genet 97: 526–534
Landschulz WH, Johnson PF and McKnight SL (1988) The leucine zipper: a hypothetical structure common to a new class of DNA binding proteins. Science 240: 1759–1764
Laugé R (1999) Extracellular proteins of the tomato pathogen Cladosporium fulvum: role in pathogenicity and avirulence, PhD thesis Phytopathology, Wageningen University, Wageningen.
Laugé R and De Wit PJGM (1998) Fungal avirulence genes: structure and possible functions. Fungal Genet Biol 24: 285–297
Laugé R, Joosten MHAJ, Van Den Ackerveken GFJM, Van Den Broek HWJ and De Wit PJGM (1997) The in planta-produced extracellular proteins ECP1 and ECP2 of Cladosporium fulvum are virulence factors. Mol Plant-Microbe Interact 10: 735–744
Lawrence GJ, Finnegan EJ, Ayliffe MA and Ellis JG (1995) The L6 gene for flax rust resistance is related to the Arabidopsis bacterial resistance gene RPS2 and the tobacco viral resistance gene N. Plant Cell 7: 1195–1206
Lemaitre B, Nicolas E, Michaut L, Reichhart JM and Hoffmann JA (1996) The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86: 973–983
McDowell JM, Dhandaydham M, Long TA, Aarts MGM, Goff S, Holub EB and Dangl JL (1998) Intragenic recombination and diversifying selection contribute to the evolution of downy mildew resistance at the RPP8 locus of Arabidopsis. Plant Cell 10: 1861–1874
Meyers BC, Shen KA, Rohani P, Gaut BS and Michelmore RW (1998) Receptor-like genes in the major resistance locus of lettuce are subject to divergent selection. Plant Cell 10: 1833–1846
Michelmore RW and Meyers BC (1998) Clusters of resistance genes in plants evolve by divergent selection and a birth-anddeath process. Genome Res 8: 1113–1130
Milligan SB, Bodeau J, Yaghoobi J, Kaloshian I, Zabel P and Williamson VM (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: 1307–1319
Mindrinos M, Katagiri F, Yu GL and Ausubel FM (1994) The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell 78: 1089–1099
Moyle WR, Campbell RK, Rao SN, Ayad NG, Bernard MP, Han Y and Wang Y (1995) Model of human chorionic gonadotropin and lutropin receptor interaction that explains signal transduction of the glycoprotein hormones. J Biol Chem 270: 20020–20031
Nürnberger T, Wirtz W, Nennstiel D, Hahlbrock K, Jabs T, Zimmermann S and Scheel D (1997) Signal perception and intracellular signal transduction in plant pathogen defense. J Recept Sign Trans Res 17: 127–136
Olivain C and Alabouvette C (1999) Process of tomato root colonization by a pathogenic strain of Fusarium oxysporum f.sp. lycopersici in comparison with a non-pathogenic strain. New Phytol 141: 497–510
Ori N, Eshed Y, Paran I, Presting g, Aviv D, Tanksley S, Zamir D and Fluhr R (1997) The I2C family from the wilt disease resistance locus I2 belongs to the nucleotide binding, leucinerich repeat superfamily of plant resistance genes. Plant Cell 9: 521–532
Osbourn AE (1996) Preformed antimicrobial compounds and plant defense against fungal attack. Plant Cell 8: 1821–1831
Parker JE, Coleman MJ, Szabo V, Frost LN, Schmidt R, Van Der Biezen EA, Moores T, Dean C, Daniels MJ and Jones JDG (1997) The Arabidopsis downy mildew resistance gene Rpp5 shares similarity to the Toll and Interleukin-1 receptors with N and L6. Plant Cell 9: 879–894
Parniske M and Jones JDG (1999) Recombination between diverged clusters of the tomato Cf-9 plant disease resistance gene family. Proc Natl Acad Sci USA 96: 5850–5855
Parniske M, Hammond-Kosack KE, Golstein C, Thomas CM Jones DA, Harrison K, Wulff BBH and Jones JDG (1997) Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomato. Cell 91: 821–832
Parniske M, Wulff BBH, Bonnema G, Thomas CM, Jones DA and Jones JDG (1999) Homologues of the Cf-9 disease resistance gene (Hcr9s) are present at multiple loci on the short arm of tomato chromosome 1. Mol Plant-Microbe Interact 12: 93–102
Rohe M, Gierlich A, Hermann H, Hahn M, Schmidt B, Rosahl S and Knogge W (1995) The race-specific elicitor, NIP1, from the barley pathogen, Rhynchosporium secalis, determines avirulence on host plants of the Rrs1 resistance genotype. EMBO J 14: 4168–4177
Romeis T, Piedras P, Zhang SQ, Klessig DF, Hirt H and Jones JDG (1999) Rapid Avr9-and Cf9-dependent activation of MAP kinases in tobacco cell cultures and leaves: convergence of resistance gene, elicitor, wound, and salicylate responses. Plant Cell 11: 273–287
Rossi M, Goggin FL, Milligan SB, Kaloshian I, Ullman DE and Williamson VM (1998) The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proc Natl Acad Sci USA 95: 9750–9754
Ryals JA, Neuenschwander UH, Willits MG, Molina A, Steiner HY and Hunt MD (1996) Systemic acquired resistance. Plant Cell 8: 1809–1819
Ryals J, Weymann K, Lawton K, Friedrich L, Ellis D, Steiner HY, Johnson J, Delaney TP, Jesse T, Vos P and Uknes S (1997) The Arabidopsis NIM1 protein shows homology to the mammalian transcription factor inhibitor I?B. Plant Cell 9: 425–439
Ryerson DE and Heath MC (1996) Cleavage of nuclear DNA into oligonucleosomal fragments during cell death induced by fungal infection or by abiotic treatments. Plant Cell 8: 393–402
Salmeron JM, Oldroyd GED, Rommens CMT, Scofield SR, Kim HS, Lavelle DT, Dahlbeck D and Staskawicz BJ (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: 123–133
Schopfer CR, Nasrallah ME and Nasrallah JB (1999) The male determinant of self-incompatibility in Brassica. Science 286: 1697–1700
Schulze-Lefert P (1999) Molecular control of resistance to powdery mildewin barley. 9th International Congress on Molecular Plant-Microbe Interactions, Amsterdam
Scofield SR, Tobias CM, Rathjen JP, Chang JH, Lavelle DT, Michelmore RW and Staskawicz BJ (1996) Molecular basis of gene-for-gene specificity in bacterial speck disease of tomato. Science 274: 2063–2065
Shah J, Tsui F and Klessig DF (1997) Characterization of a salicylic acid-insensitive mutant (sai1) of Arabidopsis thaliana, identified in a selective screen utilizing the SA-inducible expression of the tms2 gene. Mol Plant-Microbe Interact 10: 69–78
Shirasu K, Lahaye T, Tan MW, Zhou FS, Azevedo C and Schulze-Lefert P (1999) A novel class of eukaryotic zinc-binding proteins is required for disease resistance signaling in barley and development in C. elegans. Cell 99: 355–366
Simons G, Groenendijk J, Wijbrandi J, Reijans M, Groenen J, Diergaarde P, Van der Lee T, Bleeker M, Onstenk J, De Both M, Haring M, Mes J, Cornelissen B, Zabeau M and Vos P (1998) Dissection of the fusarium I2 gene cluster in tomato reveals six homologs and one active gene copy. Plant Cell 10: 1055–1068
Sims JE, Acres RB, Grubin CE, McMahan CJ, Wignall JM, March CJ and Dower SK (1989) Cloning the interleukin 1 receptor from human T cells. Proc Natl Acad Sci USA 86: 8946–8950
Somssich IE and Hahlbrock K (1998) Pathogen defence in plants-a paradigm of biological complexity. Trends Pl Sci 3: 87–90
Song WY, Wang GL, Chen LL, Kim HS, Pi LY, Holsten T, Gardner J, Wang B, Zhai WX, Zhu LH, Fauquet C and Ronald P (1995) A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270: 1804–1806
Stiekema WJ, Van der Vossen EAG, Sandbrink H, Peters S, Rouppe van der Voort J, Kanyuka K, Bendahmane A, Bakker J and Klein-Lankhorst RM (1999) Two paralogous genes of the Gpa2 resistance locus confer both virus and nematode resistance to potato. 9th International Congress on Molecular Plant-Microbe Interactions, Amsterdam. In: De Wit PJGM, Bisseling T and Stiekema WJ (eds) Biology of Plant-Microbe Interactions, Vol 2 (pp 428–432) 0–9654625–1-X
Stone JM, Trotochaud AE, Walker JC and Clark SE (1998) Control of meristem development by CLAVATA1 receptor kinase and kinase-associated protein phosphatase interactions. Pl Phys 117: 1217–1225
Tai TH, Dahlbeck D, Clark ET, Gajiwala P, Pasion R, Whalen MC, Stall RE and Staskawicz BJ (1999) Expression of the Bs2 pepper gene confers resistance to bacterial spot disease in tomato. Proc Natl Acad Sci USA 96: 14153–14158
Takken FLW, Schipper D, Nijkamp HJJ and Hille J (1998) Identification and Ds-tagged isolation of a new gene at the Cf-4 locus of tomato involved in disease resistance to Cladosporium fulvum race 5. Plant J 14: 401–411
Tang XY, Frederick RD, Zhou JM, Halterman DA, Jia YL and Martin GB (1996) Initiation of plant disease resistance by physical interaction of Avrpto and Pto kinase. Science 274: 2060–2063
Tang XY, Xie MT, Kim YJ, Zhou JM, Klessig DF and Martin GB (1999) Overexpression of Pto activates defense responses and confers broad resistance. Plant Cell 11: 15–29
Thomas CM, Jones DA, ParniskeM, Harrison K, Balint-Kurti PJ, Hatzixanthis K and Jones JDG (1997) Characterization 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: 2209–2224
Thomas CM, Dixon MS, Parniske M, Golstein C and Jones JDG (1998) Genetic and molecular analysis of tomato Cf genes for resistance to Cladosporium fulvum. Phil Trans R Soc Lond B 353(1374): 1413–1424
Thomma BPHJ, Eggermont K, Penninckx IAMA, Mauch Mani B, Vogelsang R, Cammue BPA and Broekaert WF (1998) Separate jasmonate-dependent and salicylate-dependent defenseresponse pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc Natl Acad Sci USA 95: 15107–15111
Traut TW (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
Trowsdale J (1993) Genomic structure and function in the MHC. Trends Genet 9: 117–122
Valent B (1999) Molecular characterization of resistance gene/avirulence gene interactions in the rice blast system. 9th International Congress on Molecular Plant-Microbe Interactions, Amsterdam
Van den Hooven HM, Appelman AWJ, Zey T, De Wit PJGM and Vervoort J (1999) Folding and conformational analysis of AVR9 peptide elicitors of the fungal tomato pathogen Cladosporium fulvum. Eur J Biochem 264: 9–18
Van der Biezen EA and Jones JDG (1998) The NB-ARC domain: a novel signalling motif shared by plant resistance gene products and regulators of cell death in animals. Curr Biol 8: 226–227
Van der Biezen EA and Jones JDG (1999) Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem Sci 23: 454–456
Vivian A and Gibbon MJ (1997) Avirulence genes in plant-pathogenic bacteria-signals or weapons. Microbiology 143: 693–704
Vos P, Simons G, Jesse T, Wijbrandi J, Heinen L, Hogers R, Frijters A, Groenendijk J, Diergaarde P, Reijans M, Fierens Onstenk J, De Both M, Peleman J, Liharska T, Hontelez J and Zabeau M (1998) The tomato Mi-1 gene confers resistance to both root-knot nematodes and potato aphids. Nature Biotech 16: 1365–1369
Wang GL, Ruan DL, Song WY, Sideris S, Chen LL, Pi LY, Zhang SP, Zhang Z, Fauquet C, Gaut BS, Whalen MC and Ronald PC (1998) Xa21D encodes a receptor-like molecule with a leucine-rich repeat domain that determines race-specific recognition and is subject to adaptive evolution. Plant Cell 10: 765–779
Warren RF, Merritt PM, Holub E and Innes RW (1999) Identification of three putative signal transduction genes involved in R gene-specified disease resistance in Arabidopsis. Genetics 152: 401–412
Whitham S, Dinesh-Kumar SP, 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: 1101–1115
Williams RW, Wilson JM and Meyerowitz EM (1997) Apossible role for kinase-associated protein phosphatase in the Arabidopsis CLAVATA1 signaling pathway. Proc Natl Acad Sci USA 94: 10467–10472
Wolter M, Hollricher K, Salamini F and Schulze-Lefert P (1993) The mlo resistance alleles to powdery mildew infection in barley trigger a developmentally controlled defence mimic phenotype. Mol Gen Genet 239: 122–128
Yang Y, Shah J and Klessig DF (1997) Signal perception and transduction in plant defense responses. Gene Develop 11: 1621–1639
Yoshimura S, Yamanouchi U, Katayose Y, Toki S, Wang ZX, 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: 1663–1668
Zhang YL, Fan WH, Kinkema M, Li X and Dong XN (1999) Interaction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of the PR-1 gene. Proc Natl Acad Sci USA 96: 6523–6528
Zhou JM, Loh YT, Bressan RA and Martin GB (1995) The tomato gene Pti1 encodes a serine/threonine kinase that is phosphorylated by Pto and is involved in the hypersensitive response. Cell 83: 925–935
Zhou J, Tang X and Martin GB (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: 3207–3218
Zhu Q, Dröge-Laser W, Dixon RA and Lamb C (1996) Transcriptional activation of plant defense genes. Curr Opin Gen Dev 6: 624–630
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Takken, F.L., Joosten, M.H. Plant Resistance Genes: Their Structure, Function and Evolution. European Journal of Plant Pathology 106, 699–713 (2000). https://doi.org/10.1023/A:1026571130477
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DOI: https://doi.org/10.1023/A:1026571130477