Skip to main content
SpringerLink
Log in

Molecular basis of specificity in host/fungus interactions

  • Mini Review
  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

Fungal phytopathogens have evolved efficient mechanisms that enable them to exploit the plant nutrient reservoir for the purpose of growth and propagation. These are counteracted by the plants to arrest fungal development. Two general principles control the specificity of host/fungus interactions. In several cases, the interplay between fungus-produced toxins and either plant toxin targets or detoxification mechanisms determine the outcome of the interaction. An analogous principle appears to be operative in the opposite direction; deposition by plants of fungitoxic compounds that can be detoxified by pathogenic fungi. Presumably of more general importance is the recognition-based plant defense system. The ensuing resistance is frequently controlled by single genes in both interacting organisms. Originally observed in many crop plants at the sub-species level, it has recently also been described in wild plants and at the species level. The structures of disease resistance genes cloned to date from different plants allow the conclusion that the plant protective system against pathogens is based on a general principle that appears to be as effective as the animal disease protection system.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Balint-Kurti PJ, Dixon MS, Jones DA, Norcott KA and Jones JDG (1994) RFLP linkage analysis of theCf-4 andCf-9 genes for resistance toCladosporium fulvum in tomato. Theoretical and Applied Genetics 88: 691–700

    Google Scholar 

  • Balint-Kurti PJ, Jones DA and Jones JDG (1995) Integration of the classical and RFLP linkage maps of the short arm of tomato chromosome 1. Theoretical and Applied Genetics 90: 17–26

    Google Scholar 

  • Bangham AD and Horne RW (1962) Action of saponin on biological membranes. Nature 196: 952–953

    PubMed  Google Scholar 

  • Bent AF, Kunkel BN, Dahlbeck D, Brown KL, Schmidt R, Giraudet J, Leung J and Staskawicz BJ (1994)RPS2 ofArabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. Science 265: 1856–1860

    PubMed  Google Scholar 

  • Bonnet P, Lacourt I, Venard P and Ricci P (1994) Diversity in pathogenicity to tobacco and in elicitin production among isolates ofPhytophthora parasitica. Journal of Phytopathology 141: 25–37

    Google Scholar 

  • Bowyer P, Clarke BR, Lunness P, Daniels MJ and Osbourn AE (1995) Host range of a plant pathogenic fungus determined by a saponin detoxifying enzyme. Science 267: 371–374

    PubMed  Google Scholar 

  • Brosch G, Ransom R, Lechner T, Walton JD and Loidl P (1995) Inhibition of maize histone deacetylases by HC toxin, the host-selective ofCochliobolus carbonum. Plant Cell 7: 1941–1950

    PubMed  Google Scholar 

  • Bushnell WR and Rowell JB (1981) Suppressors of defense reactions: a model for roles in specificity. Phytopathology 71: 1012–1014

    Google Scholar 

  • CÔté F and Hahn MG (1994) Oligosaccharins: Structures and signal transduction. Plant Molecular Biology 26: 1379–1411

    PubMed  Google Scholar 

  • De Wit PJGM (1995) Fungal avirulence genes and plant resistance genes: Unravelling the molecular basis of gene-for-gene interactions. In: Andrews JH and Tommerup IC (eds) Advances in Botanical Research, Vol. 12 (pp. 147–185) Academic Press, London

    Google Scholar 

  • Dickinson M, Jones DA and Jones JDG (1993) Close linkage between Cf-2/Cf-5 andMi resistance loci in tomato. Molecular Plant-Microbe Interactions 6: 341–347

    PubMed  Google Scholar 

  • Dixon MS, Jones DA, Keddie JS, Thomas CM and Harrison K, Jones JDG (1996) The tomatoCf-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins. Cell 84: 451–459

    PubMed  Google Scholar 

  • Ebel J and Cosio EG (1994) Elicitors of plant defense responses. International Review of Cytology 148: 1–36

    Google Scholar 

  • Ebel J and Scheel D (1996) Signals in host-parasite interactions. In: Carroll GC and Tudzinsky P (eds) The Mycota. Vol. VI. Plant Relationships. Spring-Verlag, Berlin (In press)

    Google Scholar 

  • Flor HH (1955) Host-parasite interactions in flax rust — its genetics and other implications. Phytopathology 45: 680–685

    Google Scholar 

  • Flor HH (1971) Current status of the gene-for-gene concept. Annual Review of Phytopathology 9: 275–296

    Google Scholar 

  • Grant MR, Godiard L, Straube E, Ashfield T, Lewald J, Sattler A, Innes RW and Dangl JL (1995) Structure of theArabidopsis RPM1 gene enabling dual specificity disease resistance. Science 269: 843–846

    PubMed  Google Scholar 

  • Hahn M, Jüngling S and Knogge W (1993) Cultivar-specific elicitation of barley defense reactions by the phytotoxic peptide NIP1 fromRhynchosporium secalis. Molecular Plant-Microbe Interactions 6: 745–754

    PubMed  Google Scholar 

  • Hashimoto C, Hudson K and Anderson KV (1988) TheToll gene ofDrosophila, required for dorsal-ventral embryonic polarity, appears to encode a transmembrane protein. Cell 52: 269–279

    PubMed  Google Scholar 

  • Heath MC (1981) A generalized concept of host-parasite specificity. Phytopathology 71: 1121–1123

    Google Scholar 

  • Heath MC (1982) The absence of active defense mechanisms in compatible host-pathogen interactions. In: Wood RKS (ed) Active Defense Mechanisms in Plants (pp. 143–156) Plenum Press, New York, London

    Google Scholar 

  • Heath MC (1991) The role of gene-for-gene interactions in the determination of host species specificity. Phytopathology 81: 127–130

    Google Scholar 

  • Heath MC (1994) Current concepts of the determinants of plant-fungal specificity. In: Kohmoto K and Yoder OC (eds) Host-Specific Toxins: Biosynthesis, Receptor and Molecular Biology (pp. 3–21) Faculty of Agriculture, Tottori University

  • Heguy A, Baldari CT, Macchia G, Telford JL and Melli M (1992) Amino acids conserved in interleukin-1 receptors (IL-1Rs) and theDrosophila Toll protein are essential for IL-1R signal transduction. Journal of Biological Chemistry 267: 2605–2609

    PubMed  Google Scholar 

  • Honée G and Nürnberger T (1995) Molecular genetics of fungal plant pathogens and signal perception and transduction in plant-fungus interactions. European Journal of Plant Pathology 101: 579–583

    Google Scholar 

  • Honée G, Van den Ackerveken GFJM, Van den Broek HWJ, Cozijinsen TJ, Joosten MHAJ, Kooman-Gersmann M, Vervoort J, Vogelsang R, Vossen P, Wubben JP and De Wit PJGM (1994) Molecular characterization of the interaction between the fungal pathogenCladosporium fulvum and tomato. Euphytica 79: 219–225

    Google Scholar 

  • Johal GS and Briggs SP (1992) Reductase activity encoded by theHM1 disease resistance gene in maize. Science 258: 985–987

    PubMed  Google Scholar 

  • Jones DA, Thomas CM, Hammond-Kosack KE, Balint-Kurti PJ and Jones JDG (1994) Isolation of the tomatoCf-9 gene for resistance toCladosporium fulvum by transposon tagging. Science 266: 789–793

    PubMed  Google Scholar 

  • Joosten MHAJ, Cozijnsen AJ and De Wit PJGM (1994) Host resistance to a fungal tomato pathogen lost by a single base-pair change in an avirulence gene. Nature 367: 384–387

    PubMed  Google Scholar 

  • Kamoun S, Klucher KM, Coffey MD and Tyler BM (1993a) A gene encoding a host-specific elicitor protein ofPhytophthora parasitica. Molecular Plant-Microbe Interactions 6: 573–581

    PubMed  Google Scholar 

  • Kamoun S, Young M, Förster H, Coffey MD and Tyler BM (1994) Potential role of elicitins in the interaction betweenPhytophthora species and tobacco. Applied and Environmental Microbiology 60: 1593–1598

    Google Scholar 

  • Kamoun S, Young M, Glascock CB and Tyler BM (1993b) Extra-cellular protein elicitors fromPhytophthora: Host-specificity and induction of resistance to bacterial and fungal pathogens. Molecular Plant-Microbe Interactions 6: 15–25

    Google Scholar 

  • Kang S, Sweigard JA and Valent B (1995) ThePWL host specificity gene family in the blast fungusMagnaporthe grisea. Molecular Plant-Microbe Interaction 8: 939–948

    Google Scholar 

  • Keen NT (1986) Pathogenic strategies of fungi. In: Lugtenberg B (ed) Recognition in Microbe-Plant Symbiotic and Pathogenic Interactions. Vol. H4 (pp. 171–188) Springer-Verlag, Berlin

    Google Scholar 

  • Keen NT (1990) Gene-for-gene complementarity in plant-pathogen interactions. Annual Review Genetics 24: 447–463

    Google Scholar 

  • Kim S-D, Knoche HW and Dunkle LD (1987) Essentiality of the ketone function for toxicity of the host-selective toxin produced byHelminthosporium carbonum. Physiological and Molecular Plant Pathology 30: 433–440

    Google Scholar 

  • Knogge W (1991) Plant resistance genes for fungal pathogens — Physiological models and identification in cereal crops. Zeitschrift für Naturforschung 46c: 969–981

    Google Scholar 

  • Knogge W (1996) Elicitors and suppressors of the resistance response. In: Heitefu\ R, Hoppe HH and Hartleb H (eds) Resistance of Crop Plants Against Fungi. Fischer-Verlag, Jena (In press)

    Google Scholar 

  • Kobe B and Deisenhofer J (1994) The leucine-rich repeat: A versatile binding motif. Trends in Biochemical Sciences 19: 415–421

    PubMed  Google Scholar 

  • Kombrink E and Somssich IE (1995) Defense responses of plants to pathogens. In: Andrews JH and Tommerup IC (eds) Advances in Botanical Research. Vol. 21 (pp. 1–34) Academic Press, London

    Google Scholar 

  • Kooman-Gersmann M, Honée G, Bonnema G and De Wit PJGM (1996) A high affinity binding site for the AVR9 peptide elicitor ofCladosporium fulvum is present on plasma membranes of tomato and other solanaceous plants. Plant Cell 8: 929–939

    PubMed  Google Scholar 

  • Lawrence GJ, Finnegan EJ, Ayliffe MA and Ellis JG (1995) TheL6 gene for flax rust resistance is related to theArabidopsis bacterial resistance geneRPS2 and the tobacco viral resistance geneN. Plant Cell 7: 1195–1206

    PubMed  Google Scholar 

  • Lehnackers H and Knogge W (1990) Cytological studies on the infection of barley cultivars with known resistance genotypes byRhynchosporium secalis. Canadian Journal of Botany 68: 1953–1961

    Google Scholar 

  • Marmeisse R, Van den Ackerveken GFJM, Goosen T, De Wit PJGM and Van den Broek HWJ (1993) Disruption of the avirulence geneavr9 in two races of the tomato pathogenCladosporium fulvum causes virulence on tomato genotypes with the complementary resistance geneCf9. Molecular Plant-Microbe Interactions 6: 412–417

    Google Scholar 

  • Martin GB, Brommonschenkel SH, Chunwongse J, Frary A, Ganal MW, Spivey R, Wu T, Earle ED and Tanksley SD (1993) Mapbased cloning of a protein kinase gene conferring resistance in tomato. Science 262: 1432–1436

    PubMed  Google Scholar 

  • Meeley RB, Johal GS, Briggs SP and Walton JD (1992) A biochemical phenotype for a disease resistance gene of maize. Plant Cell 4: 71–77

    PubMed  Google Scholar 

  • Meeley RB and Walton JD (1991) Enzymatic detoxification of HC-toxin, the host-selective cyclic peptide fromCochliobolus carbonum. Plant Physiology 97: 1080–1086

    Google Scholar 

  • Meeley RB and Walton JD (1993) Molecular biology and biochemistry ofHm1, a maize gene for fungal resistance. In: Nester EW and Verma DPS (eds) Advances in Molecular Genetics of Plant-Microbe Interactions. Vol. 2 (pp. 463–476) Kluwer Academic Press, Dordrecht

    Google Scholar 

  • Mindrinos M, Katagiri F, Yu G-L and Ausubel FM (1994) TheA. thaliana disease resistance geneRPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell 78: 1089–1099

    PubMed  Google Scholar 

  • Oku H, Shiraishi T, Ouchi S and Ishiura M (1980) A new determinant of pathogenicity in plant disease. Naturwissenschaften 67: 310

    Google Scholar 

  • Osbourn A, Bowyer P, Lunness P, Clarke B and Daniels M (1995) Fungal pathogens of oat roots and tomato leaves employ closely related enzymes to detoxify different host plant saponins. Molecular Plant-Microbe Interactions 8: 971–978

    PubMed  Google Scholar 

  • Panaccione DG, Scott-Craig JS, Pocard J-A and Walton JD (1992) A cyclic peptide synthetase gene required for pathogenicity of the fungusCochliobolus carbonum. Proceedings of the National Academy of Sciences USA 89: 6590–6594

    Google Scholar 

  • Parker JE, Hahlbrock K and Scheel D (1988) Different cell-wall components fromPhytophthora megasperma f.sp.iaglycinea elicit phytoalexin production in soybean and parsley. Planta 176: 75–82

    Google Scholar 

  • Pernollet JC, Sallantin M, Sallé-Tourne M and Huet JC (1993) Elicitin isoforms from sevenPhytophthora species: Comparison of their physico-chemical properties and toxicity to tobacco and other plant species. Physiological and Molecular Plant Pathology 42: 53–67

    Google Scholar 

  • Ricci P, Bonnet P, Huet JC, Sallantin M, Beauvais-Cante F, Bruneteau M, Billard V, Michel G and Pernollet JC (1989) Structure and activity of proteins from pathogenic fungiPhytophthora eliciting necrosis and acquired resistance in tobacco. European Journal of Biochemistry 183: 555–563

    PubMed  Google Scholar 

  • Ricci P, Panabieres F, Bonnet P, Maia N, Ponchet M, Devergne JC, Marais A, Cardin L, Milat ML and Blein JP (1993) Proteinaceous elicitors of plant defense responses. In: Fritig B and Legrands M (eds) Mechanisms of Plant Defense Response (pp. 121–135) Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • 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 theRrs1 resistance genotype. EMBO Journal 14: 4168–4177

    PubMed  Google Scholar 

  • Sandrock RW, DellaPenna D and VanEtten H (1995) Purification and characterization ofΒ 2-tomatinase, an enzyme involved in the degradation ofα-tomatine and isolation of the gene encodingΒ 2-tomatinase fromSeptoria lycopersici. Molecular Plant-Microbe Interactions 8: 960–970

    PubMed  Google Scholar 

  • Scott-Craig JS, Panaccione DG, Pocard JA and Walton JD (1992) The cyclic peptide synthetase catalyzing HC-toxin production in the filamentous fungusCochliobolus carbonum is encoded by a 15.7 kilobase open reading frame. Journal of Biological Chemistry 267: 26044–26049

    PubMed  Google Scholar 

  • Shiraishi T, Araki M, Yoshioka H, Kobayashi I, Yamada T, Ichinose Y, Kunoh H and Oku H (1991) Inhibition of ATPase activity in pea plasma membranesin situ by a suppressor from a pea pathogen,Mycosphaerella pinodes. Plant Cell Physiology 32: 1067–1075

    Google Scholar 

  • Shiraishi T, Oku H, Yamashita M and Ouchi S (1978) Elicitor and suppressor of pisatin induction in spore germination fluid of pea pathogen,Mycosphaerella pinodes. Annals of the Phytopathological Society Japan 44: 659–665

    Google Scholar 

  • Shiraishi T, Saitoh K, Kim HM, Kato T, Tahara M, Oku H, Yamada T and Ichinose Y (1992) Two suppressors, supprescins A and B, secreted by a pea pathogen,Mycosphaerella pinodes. Plant Cell Physiology 33: 663–667

    Google Scholar 

  • Sims JE, Acres B, Grubin CE, McMahan CJ, Wignall JM, March CJ and Dower SK (1989) Cloning the interleukin-1 receptor from human T cells. Proceedings of the National Academy of Sciences USA 86: 8946–8950

    Google Scholar 

  • 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 kinase-like protein encoded by the rice disease resistance gene,Xa21. Science 270: 1804–1806

    PubMed  Google Scholar 

  • Staskawicz BJ, Ausubel FM, Baker BJ, Ellis JG and Jones JDG (1995) Molecular genetics of plant disease resistance. Science 268: 661–667

    PubMed  Google Scholar 

  • Sweigard JA, Carroll AM, Kang S, Farrall L, Chumley FG and Valent B (1995) Identification, cloning and characterization ofPWL2, a gene for host-species specificity in the rice blast fungus. Plant Cell 7: 1221–1233

    PubMed  Google Scholar 

  • Valent B and Chumley FG (1991) Molecular genetic analysis of the rice blast fungus,Magnaporthe grisea. Annual Review of Phytopathology 29: 443–467

    Google Scholar 

  • Valent B and Chunley FG (1994) Avirulence genes and mechanisms of genetic instability in the rice blast fungus. In: Zeigler R, Teng PS and Leong S (eds) Rice Blast Disease (pp. 111–134) CAB International, Wallingford

    Google Scholar 

  • Van den Ackerveken GF, Vossen P and De Wit PJGM (1993) The AVR9 race-specific elicitor ofCladosporium fulvum is processed by endogenous and plant proteases. Plant Physiology 103: 91–96

    PubMed  Google Scholar 

  • Van den Ackerveken GFJM, Van Kan JAL and De Wit PJGM (1992) Molecular analysis of the avirulence geneavr9 of the fungal tomato pathogenCladosporium fulvum fully supports the gene-for-gene hypothesis. Plant Journal 2: 359–366

    PubMed  Google Scholar 

  • Van Kan JAL, Van den Ackerveken GFJM and De Wit PJGM (1991) Cloning and characterization of cDNA of avirulence geneavr9 of the fungal pathogenCladosporium fulvum, causal agent of tomato leaf mold. Molecular Plant-Microbe Interactions 4: 52–59

    PubMed  Google Scholar 

  • VanEtten H, Funnell-Baerg D, Wasmann C and McCluskey K (1994a) Location of pathogenicity genes on dispensable chromosomes inNectria haematococca MPVI. Antonie van Leeuwenhoek 65: 263–267

    PubMed  Google Scholar 

  • VanEtten HD, Mansfield JW, Bailey JA and Farmer EE (1994b) Two classes of plant antibiotics: phytoalexins versus “phytoanticipins”. Plant Cell 6: 1191–1192

    PubMed  Google Scholar 

  • Walton JD, Ahn J-H, Akimitsu K, Pitkin JW and Ransom R (1994a) Leaf-spot disease of maize: chemistry, biochemistry, and molecular biology of a host-selective cyclic peptide. In: Daniels MJ, Downie JA and Osbourn AE (eds) Advances in Molecular Genetics of Plant-Microbe Interactions. Vol. 3 (pp. 231–237) Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Walton JD, Akimitsu K, Ahn J-H and Pitkin JW (1994b) Towards an understanding of theTOX2 gene ofCochliobolus carbonum. In: Kohmoto K and Yoder OC (eds) Host-Specific Toxin: Biosynthesis, Receptor and Molecular Biology (pp. 227–237) Faculty of Agriculture, Tottori University

  • Wallon JD and Panaccione DG (1993) Host-selective toxins and disease specificity: Perspectives and progress. Annual Review of Phytopathology 31: 275–303

    Google Scholar 

  • Wevelsiep L, Kogel K-H and Knogge W (1991) Purification and characterization of peptides fromRhynchosporium secalis inducing necrosis in barley. Physiological and Molecular Plant Pathology 39: 471–482

    Google Scholar 

  • Wevelsiep L, Rüpping E and Knogge W (1993) Stimulation of barley plasmalemma H+-ATPase by phytotoxic peptides from the fungal pathogenRhynchosporium secalis. Plant Physiology 101: 297–301

    PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Yu LM (1995) Elicitins fromPhytophthora and basic resistance in tobacco. Proceedings of the National Academy of Sciences USA 92: 4088–4094

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biochemistry, Max-Planck-Institut für Züchtungsforschung, Carl-von-Linné-Weg 10, D-50829, Köln, Germany

    Wolfgang Knogge

Authors
  1. Wolfgang Knogge
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Knogge, W. Molecular basis of specificity in host/fungus interactions. Eur J Plant Pathol 102, 807–816 (1996). https://doi.org/10.1007/BF01877049

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01877049

Key words

Search

Navigation