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Pathogenesis by fungi and by parasitic plants: Similarities and differences

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Abstract

The processes by which fungi and parasitic plants infect their plant host are compared. The steps considered are: location of the host by the pathogen, the concept of the haustorium, attachment of the pathogen to the host, mechanism of penetration into the host, responses of the host to infection by fungi and by parasitic plants, and the suppression of the host response by the pathogen. Although superficially similarities between fungal infection and infection by parasitic plants exist, the underlying mechanisms appear to be different and only in the penetration step are similar strategies used, including the use of lytic enzymes. These differences are important when seeking ways of combating the parasitic plants. The strategies used against the parasitic plants must be different from those used to combat fungal infections and should not be based only on analogies with host resistance to fungal pathogens.

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References

  1. Albert, M., Werner, M., Proksch, P., Fry, S.C. and Kaldenhoff, R. (2004) The cell wall-modifying xyloglucan endotransglycosylase/hydrolaseLeXTH1 is expressed during the defence reaction of tomato against the plant parasiteCuscuta reflexa.Plant Biol. 6:402–407.

    Article  PubMed  CAS  Google Scholar 

  2. Alexopolous, C.J. and Mimms, C.W. (1979) Introductory Mycology. 3rd ed. Wiley, New York, NY.

    Google Scholar 

  3. Andary, C. (1994) Chemotaxonomial study of the genusOrobanche. Proc. Third Int. Workshop on Orobanche and Related Striga Research (Amsterdam, the Netherlands), pp. 121–124.

  4. Antonova, T.S. and ter Borg, S.J. (1996) The role of peroxidase in the resistance of sunflower againstOrobanche cumana in Russia.Weed Res. 36:113–121.

    Article  CAS  Google Scholar 

  5. Bar Nun, N., Ben-Hod, G., Lavi, E. and Mayer, A.M. (1996) Purification of pectin methyl esterase fromOrobanche aegyptiaca.Phytochemistry 41:403–406.

    Article  Google Scholar 

  6. Bar Nun, N. and Mayer, A.M. (1999) Culture of pectin methyl esterase and polyphenoloxidase inCuscuta campestris.Phytochemistry 50:719–727.

    Article  Google Scholar 

  7. Bar Nun, N., Mor, A. and Mayer, A.M. (1999) A cofactor requirement for polygalacturonase fromCuscuta campestris.Phytochemistry 52:1217–1221.

    Article  Google Scholar 

  8. Ben-Hod, G., Bar Nun, N., Tzaban, S. and Mayer, A.M. (1997) Inhibitors of polygalacturonase in calli ofOrobanche aegyptiaca.Phytochemistry 45:1115–1121.

    Article  PubMed  CAS  Google Scholar 

  9. Ben-Hod, G., Losner, D., Joel, D.M. and Mayer, A.M. (1991) Infection of tomato roots using calli of broomrape.Physiol. Plant. 83:413–416.

    Article  Google Scholar 

  10. Ben-Hod, G., Losner, D., Joel, D.M. and Mayer, A.M. (1993) Pectin methyl esterase in callii and germinating seeds ofOrobanche aegyptiaca.Phytochemistry 32:1399–1442.

    Article  CAS  Google Scholar 

  11. Borsics, T. and Lados, M. (2002) Dodder infection induces the expression of a pathogenesis-related gene familyPR-10 in alfalfa.J. Exp. Bot. 53:1831–1832.

    Article  PubMed  CAS  Google Scholar 

  12. Boukar, O., Kong, L., Singh, B.B., Murdock, L and Ohm, H.W. (2004) AFLP and AFLP derived SCAR markers associated withStriga gesnerioides resistance in cowpea.Crop Sci. 44:1259–1264.

    CAS  Google Scholar 

  13. Bushmann, H. and Sauerborn, J. (2002) Induced resistance in sunflower againstOrobanche cumana. Proc. IOBC/WRPS Study Group on Induced Resistance in Plants against Insects and Diseases (Wageningen, the Netherlands, 2001).

  14. Carlile, A.J., Bindschedler, L.V., Bailey, A.M., Bowyer, P., Clarkson, J.M. and Cooper, R.M. (2000) Characterization of SNP1, a cell wall-degrading trypsin, produced during infection byStagonospora nodorum.Mol. Plant-Microbe Interact. 13:538–550.

    Article  PubMed  CAS  Google Scholar 

  15. Castillejo, M.A., Amiour, N., Dumas-Gaudot, E., Rubiales, D. and Jorrin, J.V. (2004) A proteomic approach to studying plant responses to crenate broomrape (Orobanche crenata) in pea (Pisum sativum).Phytochemistry 65:1817–1828.

    Article  CAS  Google Scholar 

  16. Christensen, N.M., Dörr, I., Hansen, M., van der Kooij, T.A.W. and Schulz, A. (2003) Development ofCuscuta species on a partially incompatible host: induction of xylem transfer cells.Protoplasma 220:133–142.

    Article  Google Scholar 

  17. Cubero, J.I., Moreno, M.T., Rubiales, D. and Sillero, J. (1999) Resistance toOrobanche; the state of the art.Congresos y Jornadas 51/99 (Cordova, Spain).

  18. Delavault, P., Simier, P., Thoiron, S., Veronesi, C., Fer, A. and Thalouarn, P. (2002) The isolation of mannose-6-phosphate reductase cDNA, changes in enzyme activity and mannitol content in broomrape (Orobanche ramosa) parasitic on tomato roots.Physiol. Plant. 115:48–55.

    Article  PubMed  CAS  Google Scholar 

  19. Dörr, I. (1990) Sieve elements in haustoria of parasitic angiosperms.in: Behnke, H.-D. and Sjolund, R.D. [Eds.] Sieve Elements. Comparative Structure, Induction and Development. Springer-Verlag, Berlin, Germany. pp. 239–256.

    Google Scholar 

  20. Dörr, I. (1996) New results on interspecific bridges between parasites and their hosts.Congresos y Jornadas 36/96 (Cordova, Spain), pp. 196–201.

  21. Dörr, I. and Kollmann, R. (1976) Strukturelle Grundlagen des Parasitismus beiOrobanche III. Die Differenzierung des xylemanschlusses beiO. crenata.Protoplasma 89:233–249.

    Article  Google Scholar 

  22. Dörr, I. and Kollmann, R. (1995) Symplasmic sieve element continuity betweenOrobanche and its host.Bot. Acta 108:47–55.

    Google Scholar 

  23. Dos Santos, C.V., Delavault, P., Letousey, P. and Thalouarn, P. (2003) Identification of suppression subtractive hybridization and expression analysis ofArabidopsis thaliana putative defence genes duringOrobanche ramosa infection.Physiol. Mol. Plant Pathol. 62:297–303.

    Article  CAS  Google Scholar 

  24. Dow, J.M., Clarke, B.R., Milligan, D.E., Tang, J.L. and Daniels, M.J. (1990) Extracellular proteases fromXanthomonas campestris pathovarcampestris, the black rot pathogen.Appl. Environ. Microbiol. 56:2994–2998.

    PubMed  CAS  Google Scholar 

  25. Eizenberg, H., Plakhine, D., Hershenhorn, J., Kleifeld, Y. and Rubin, B. (2003) Resistance of broomrape (Orobanche spp.) in sunflower (Helianthus annuus L.) is temperature dependent.J. Exp. Bot. 54:1305–1311.

    Article  PubMed  CAS  Google Scholar 

  26. Fahn, A. (1990) Plant Anatomy. 4th ed. Pergamon Press, Oxford, UK.

    Google Scholar 

  27. Francis, S.A., Dewey, F.M. and Gurr, S.J. (1996) The role of cutinase in germling development and infection byErysiphe graminis f.sp.hordei.Physiol. Mol. Plant Pathol. 49:201–211.

    Article  CAS  Google Scholar 

  28. Gedalovich, E., Kuijt, J. and Carpita, N.C. (1988) Chemical composition of viscin, an adhesive involved in dispersal of the parasitePhoradendron californicum (Viscaceae).Physiol. Mol. Plant Pathol. 32:61–76.

    Article  CAS  Google Scholar 

  29. Gethi, J.G. and Smith, M.E. (2004) Genetic responses of single crosses of maize toStriga hermonthica (Del.) Benth. andStriga asiatica (L.) Kuntze.Crop Sci. 44:2068–2077.

    Google Scholar 

  30. Gonzalez-Verdejo, C.I., Moreno-Yanguela, M.T., Cubero, J.I. and DiPietro, A. (2004) Cloning and analysis of a peroxidase gene expressed during early infection stages of the parasitic plantOrobanche ramosa.Cost-849 Meeting (Nitra, Slovakia).

  31. Griffitts, A.A., Cramer, C.A. and Westwood, J.H. (2004) Host gene expression in response to Egyptian broomrape (Orobanche aegyptiaca).Weed Sci. 52:697–703.

    Article  CAS  Google Scholar 

  32. Gurney, A.L., Grimanelli, D., Kanampiu, F., Hoisington, D., Scholes, J.D. and Press, M.C. (2003) Novel sources of resistance toStriga hermonthica inTripsacum dactyloides, a wild relative of maize.New Phytol. 160:557–568.

    Article  Google Scholar 

  33. Heide-Jorgensen, H.S. and Kuit, J. (1993) Epidermal derivatives as xylem elements and transfer cells: a study of the host-parasite interface in two species ofTriphysaria (Scrophulariaceae).Protoplasma 174:173–183.

    Article  Google Scholar 

  34. Heide-Jorgensen, H.S. and Kuit, J. (1995) The haustorium of the root parasiteTriphysaria (Scrophulariaceae) with special reference to xylem bridge ultrastructure.Am. J. Bot. 82:782–797.

    Article  Google Scholar 

  35. Hoch, H.C. and Staples, R.C. (1987) Structural and chemical changes among the rust fungi during appressorium development.Annu. Rev. Phytopathol. 25:231–247.

    Article  Google Scholar 

  36. Isaac, S. (1992) Fungal — Plant Interactions. Chapman and Hall, London, UK.

    Google Scholar 

  37. Jennings, D.B., Ehrenshaft, M., Pharr, D.M. and Williamson, J.D. (1998) Roles for mannitol and mannitol dehydrogenase in active oxygen-mediated plant defense.Proc. Natl. Acad. Sci. 95:15129–15133.

    Article  PubMed  CAS  Google Scholar 

  38. Joel, D.M. and Losner-Goshen, D. (1994) The attachment organ of the parasitic angiospermsOrobanche cumana andO. aegyptiaca and its development.Can. J. Bot. 72:564–574.

    Article  Google Scholar 

  39. Joel, D.M., Losner-Goshen, D., Goldman-Guez, T. and Portnoy, V.H. (1998) The haustorium ofOrobanche. Proc. 4 th Int. Workshop on Orobanche (Albena, Bulgaria), pp. 101–106.

  40. Joel, D.M. and Portnoy, V.H. (1998) The angiospermous root parasiteOrobanche L. (Orobanchaceae) induces a pathogenesis related (PR) gene in susceptible tobacco roots.Ann. Bot. 81:779–781.

    Article  Google Scholar 

  41. Kolattukudy, P.E. (1985) Enzymatic penetration of the plant cuticle by fungal pathogens.Annu. Rev. Phytopathol. 23:223–250.

    Article  CAS  Google Scholar 

  42. Köller, W., Yao, C., Trial, F. and Parker, D.M. (1995) Role of cutinases in the invasion of plants.Can. J. Bot. 73 (Suppl. 1):S1109-S1118.

    Article  Google Scholar 

  43. Koskela, T., Puustinen, S., Salonen, V. and Mutikainen, P. (2002) Resistance and tolerance in a host plant — holoparasitic plant interaction: genetic variations and costs.Evolution 56:899–908.

    PubMed  Google Scholar 

  44. Kuijt, J. (1969) The Biology of Parasitic Flowering Plants. University of California Press, Berkeley, CA, USA.

    Google Scholar 

  45. Labrousse, P., Arnaud, M.C., Serieys, H., Berville, A. and Thalouarn, P. (2001) Several mechanisms are involved in resistance ofHelianthus toOrobanche cumana Wallr.Ann. Bot. 88:859–868.

    Article  Google Scholar 

  46. Lane, J.A., Bailey, J.A., Butler, R.C. and Terry, P.J. (1993) Resistance of cowpea (Vigna unguiculata) (L.) Walp.] toStriga gesnerioides (Willd.) Vatke, a parasitic angiosperm.New Phytol. 125:405–412.

    Article  Google Scholar 

  47. Lev-Yadoun, S. (2001) Intrusive growth — the plant analogue of dendrite and axon growth in animals.New Phytol. 150:508–512.

    Article  Google Scholar 

  48. Löffler, C., Sahm, A., Wray, V., Czygan, F-C. and Proksch, P. (1996) Soluble phenolic constituents fromCuscuta reflexa andCuscuta platyloba.Biochem. Syst. Ecol. 23:121–128.

    Article  Google Scholar 

  49. Losner-Goshen, D., Joel, D.M., Mayer, A.M. and Steffens, J.C. (1991) Surface characteristics and internal structure of theOrobanche seedlings.Proc. 5 th Int. Symposium on Parasitic Weeds (Nairobi, Kenya), pp. 356–360.

  50. Losner-Goshen, D., Portnoy, V.H., Mayer, A.M. and Joel, D.M. (1998) Pectolytic activity by the haustorium of the parasitic plantOrobanche L. (Orobanchaceae) in host roots.Ann. Bot. 81:319–326.

    Article  CAS  Google Scholar 

  51. Lucas, J.A. (1998) Plant Pathology and Plant Pathogens. 3rd ed. Blackwell Science, Oxford, UK.

    Google Scholar 

  52. Matvienko, M., Torres, M.J. and Yoder, J.I. (2001) Transcriptional responses in the hemiparasiteTryphysaria versicolor to host plant signals.Plant Physiol. 127:272–282.

    Article  PubMed  CAS  Google Scholar 

  53. Mayer, A.M., Staples, R.C. and Gil-ad, N.L. (2001) Mechanism of survival of necrotrophic fungal plant pathogens in hosts expressing the hypersensitive response.Phytochemistry 58:33–41.

    Article  PubMed  CAS  Google Scholar 

  54. Mohamed, A., Ellicot, A., Housley, T.L. and Ejeta, G. (2003) Hypersensitive response toStriga infection inSorghum.Crop Sci. 43:1320–1324.

    Google Scholar 

  55. Mohavedi, S. and Heale, J.B. (1990) The roles of aspartic proteases and endopectin lyase enzymes in the primary stages of infection and pathogenesis of various tissues by different isolates ofB. cinerea.Physiol. Mol. Plant Pathol. 36:303–324.

    Article  Google Scholar 

  56. Ochocka, J.R. and Piotrowski, A. (2002) Biologically active compounds from European mistletoe (Viscum album L.).Can J. Plant Pathol. 24:21–28.

    CAS  Google Scholar 

  57. Orru, S., Scaloni, A., Giannattasio, M., Urech, K., Pucci, P. and Schaller, G. (1997) Aminoacid sequence, S-S bridge arrangement and distribution in plant tissues of thionins fromViscum album.Biol. Chem. 378:989–996.

    Article  PubMed  CAS  Google Scholar 

  58. Palmer, A.G., Gao, R., Maresh, J., Erbil, W.K. and Lynn, D.G. (2004) Chemical biology of multi-host/pathogen interactions: chemical perception and metabolic complementation.Annu. Rev. Plant Pathol. 42:439–464.

    CAS  Google Scholar 

  59. Parker, C. and Riches, C.R. (1993) Parasitic Weeds of the World. CAB International, Wallingford, UK.

    Google Scholar 

  60. Pérez-de-Luque, A., Rubiales, D., Cubero, J.I., Press, M.C., Scholes, J., Yoneyama, K.et al. (2005) Interaction betweenOrobanche crenata and its host legumes: Unsuccessful haustorial penetration and necrosis of the developing parasite.Ann. Bot. 95:935–942.

    Article  PubMed  Google Scholar 

  61. Pérez-Vich, B., Akhtouch, B., Knapp, S.J., Leon, A.J., Velasco, L., Fernandez-Martinez, J.M.et al. (2004) Quantitative trait loci for broomrape (Orobanche cumana Wallr.) resistance in sunflower.Theor. Appl. Genet. 109:92–102.

    Article  PubMed  CAS  Google Scholar 

  62. Press, M.C. and Graves, D. (1995) Parasitic Plants. Chapman and Hall, London, UK.

    Google Scholar 

  63. Quedraogo, J.T., Tignegre, J-B., Timko, M.P. and Belzile, F.J. (2002) AFLP markers linked to resistance againstStriga gesnerioides race 1 in cowpea (Vigna unguiculata).Genome 45:787–793.

    Article  Google Scholar 

  64. Rank, C., Rasmussen, L.S., Jensen, S.R., Pierce, S., Press, M.C. and Scholes, J.D. (2004) Cytotoxic constituents ofAlectra andStriga species.Weed Res. 44:265–270.

    Article  CAS  Google Scholar 

  65. Reizelman, A., Scheren, M., Nefkens, G.H.L. and Zwaneburg, B. (2000) Synthesis of all the eight stereoisomers of the germination stimulant strigol.Synthesis 1994–1951.

  66. Rich, P.J., Grenier, C. and Ejeta, G. (2004)Striga resistance in the wild relatives of sorghum.Crop Sci. 44:2221–2229.

    Google Scholar 

  67. Riopel, J.L. and Timko, M.P. (1995) Haustorial initiation and differentiation.in: Press, M.C. and Graves, J.D. [Eds.] Parasitic Plants. Chapman and Hall, London, UK. pp. 39–79.

    Google Scholar 

  68. Román, B., Torres, A.M., Rubiales, D., Cubero, J.L. and Satovic, Z. (2002) Mapping of quantitative trait loci controlling broomrape (Orobanche crenata Forsk.) resistance in faba beans (Vicia faba L.).Genome 45:1057–1063.

    Article  PubMed  Google Scholar 

  69. Rousset, A., Simier, P. and Fer, A. (2003) The characterization of simple in vitro cultures ofStriga hermonthica suitable for metabolic studies.Plant Biol. 5:265–273.

    Article  CAS  Google Scholar 

  70. Rubiales, D. (2003) Parasitic plants, wild relatives and the nature of resistance.New Phytol. 160:459–461.

    Article  Google Scholar 

  71. Rubiales, D., Pérez-de-Luque, A., Sillero, J.C., Román, B.M., Kharrat, M., Khalil, S.et al. (2005) Screening techniques and sources of resistance against parasitic weeds in grain legumes.Euphytica (in press).

  72. Sachs, T. (1991) Pattern Formation in Plant Tissues. Cambridge University Press, Cambridge, UK.

    Google Scholar 

  73. Shomer-Ilan, A. (1992) Enzymes with pectinolytic and cellulolytic activity are excreted by the haustorium ofOrobanche aegyptiaca.Phytoparasitica 20:343 (abstr.).

    Google Scholar 

  74. Shomer-Ilan, A. (1993) Germinating seeds of the root parasiteOrobanche aegyptiaca Pers. excrete enzymes with carbohydrase activity.Symbiosis 15:61–70.

    CAS  Google Scholar 

  75. Shomer-Ilan, A. (1999) Proteolytic activity of germinatingOrobanche aegyptiaca seeds controls the degrading level of its own excreted pectinase and cellulase.Phytoparasitica 27:111 (abstr.).

    Google Scholar 

  76. Slavov, S., van Onckelen, H., Batchvarova, R., Atanassov, A. and Prinsen, E. (2004) IAA production during germination ofOrobanche spp. seeds.J. Plant Physiol. 161:847–853.

    Article  PubMed  CAS  Google Scholar 

  77. Staples, R.C. and Mayer, A.M. (2003) Suppression of host resistance by fungal plant pathogens.Isr. J. Plant Sci. 51:173–184.

    Article  CAS  Google Scholar 

  78. Strange, R.N. (2003) Introduction to Plant Pathology. John Wiley and Sons, Chichester, UK.

    Google Scholar 

  79. Teryokhin, E.S. (1997) Weed Broomrapes. Aufstieg-Verlag, Munich, Germany.

    Google Scholar 

  80. Tian, M., Huitema, E., da Cunha, L., Torto-Alalibo, T. and Kamoun, S. (2004) A Kazal-like extracellular serine protease inhibitor fromPhytophthora infestans targets the tomato-related protease P69B.J. Biol. Chem. 279:26370–26377.

    Article  PubMed  CAS  Google Scholar 

  81. Tomilov, A., Tomilova, N. and Yoder, I. (2004)In vitro haustorium development in roots and root cultures of the hemiparasitic plantTriphysaria versicolor.Plant Cell Tissue Organ Cult. 77:257–265.

    Article  Google Scholar 

  82. Valderrama, M.R., Roman, B., Satovic, Z., Rubiales, D., Cubero, J.I. and Torres, A.M. (2004) Locating quantitative trait loci associated withOrobanche crenata resistance in pea.Weed Res. 44:323–328.

    Article  CAS  Google Scholar 

  83. Van Kan, J.A.L., van ’t Klooster, J.W., Dees, D.C.T., Wagemakers, C.A.M. and van der Vlugt-Bergmans, C.J.B. (1997) Cutinase A ofBotrytis cinerea is expressed, but not essential, during the penetration of gerbera and tomato.Mol. Plant-Microbe Interact. 10:30–38.

    Article  PubMed  Google Scholar 

  84. Vaughn, K.C. (2002) Attachment of the parasitic weed dodder to the host.Protoplasma 219:227–237.

    Article  PubMed  CAS  Google Scholar 

  85. Vaughn, K.C. (2003) Dodder hyphae invade the host: a structural and immunocytochemical characterization.Protoplasma 220:189–200.

    Article  PubMed  CAS  Google Scholar 

  86. Veronesi, C. and Thalouarn, P. (2001) Virulence variability among differentOrobanche cumana Walls. races.Proc. 7 th Int. Parasitic Weed Symposium (Nantes, France), p. 245.

  87. Werner, M., Uehlein, N., Proksch, P. and Kaldenhoff, R. (2001) Characterization of two tomato aquaporins and expression during the incompatibility interaction of tomato with the plant parasiteCuscuta reflexa.Planta 213:550–555.

    Article  PubMed  CAS  Google Scholar 

  88. Westwood, J.H., Yu, X., Foy, C.L. and Cramer, C.L. (1998) Expression of a defense-related 3-hydroxy-3-methylglutaryl CoA reductase gene in response to parasitization byOrobanche spp.Mol. Plant-Microbe Interact. 11:530–536.

    Article  PubMed  CAS  Google Scholar 

  89. Zhou, W.J., Yoneyama, K., Takeuchi, Y., Iso, S., Rungmekarat, S., Chae, S.H.et al. (2004)In vitro infection of host roots by differentiated calli of the parasitic plantOrobanche.J. Exp. Bot. 55:899–907.

    Article  PubMed  CAS  Google Scholar 

  90. Zwanenburg, B. and Reizelman, A. (2001) En route to the isolation and characterization of the strigolactone receptor using biotin labelled strigolactone analogues.Proc. 7 th Int. Parasitic Weed Symposium (Nantes, France), pp. 102–105.

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    A. M. Mayer

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Mayer, A.M. Pathogenesis by fungi and by parasitic plants: Similarities and differences. Phytoparasitica 34, 3–16 (2006). https://doi.org/10.1007/BF02981333

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