Microbial Interactions Preventing Fungal Growth on Senescent and Necrotic Aerial Plant Surfaces

  • William F. Pfender


Although there is an extensive literature concerning many aspects of phyllosphere microbial ecology, only a small proportion addresses senescent and necrotic aerial plant tissues. But microbial activity on these surfaces is important, in part because the microflora there can interact with microbes on living plant surfaces (see Köhl and Fokkema, 1994; Fokkema, 1993). Furthermore, a consideration of the environment on senescent or non-living plant surfaces can bring forward, through contrast with the living phyllosphere, general principles of microbial ecology and interactions. In another chapter of this volume, Alan Rayner discusses fungal interactions on bark, a non-living layer of aerial tissue in woody plants. In contrast, this chapter addresses senescent and non-living aerial tissues of herbaceous plants — specifically, the physical and nutritional environment of these surfaces as it affects the microbial community, the microbial interactions that can limit the survival or activity of fungi there, and how these effects are relevant to microbial activity in phyllospheres of living plants.


Wheat Straw Necrotic Tissue Plant Surface Antibiotic Production Microbial Interaction 
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  1. Abawi, G. S. and Grogan, R. G. 1975, Source of primary inoculum and effects of temperature and moisture on infection of beans by Whetzelinia sclerotiorum. Phytopathology 65:300–309.Google Scholar
  2. Adee, E. A. and Pfender, W. F. 1989, The effect of primary inoculum level of Pyrenophora tritici-repentis on tan spot epidemic development in wheat. Phytopathology 79:873–877.Google Scholar
  3. Adee, S. R., Pfender, W. F. and Hartnett, D. C. 1990, Competition between Pyrenophora tritici-repentis and Septoria nodorum in the wheat leaf as measured with de Wit replacement series. Phytopathology 80:1177–1182.Google Scholar
  4. Andrews, J. H. 1992, Biological control in the phyllosphere. Annu. Rev. Phytopathol. 30:603–635.CrossRefPubMedGoogle Scholar
  5. Atlas, R. M. and Bartha, R. 1993, Microbial Ecology: Fundamentals and Applications. USA: Benjamin-Cummings Publishing Co.Google Scholar
  6. Baddeley, M.S. 1971, Biochemical aspects of senescence, pp. 415–429 In: Preece, T.F. and Dickinson, G.H., (eds.) Ecology of Leaf Surface Micro-organisms. London: Academic Press.Google Scholar
  7. Beattie, G.A. and Lindow, S.E. 1994, Epiphytic fitness of phytopathogenic bacteria: Physiological adaptations for growth and survival, pp. 1–27 In: Dangl, J.L., (ed.) Current Topics in Microbiology and Immunology, vol. 129. Heidelberg: Springer-Verlag.Google Scholar
  8. Biles, C. L. and Hill, J. P. 1988, Effect of Trichoderma harzianum on sporulation of Cochliobolus sativus on excised wheat seedling leaves. Phytopathology 78:656–659.Google Scholar
  9. Blakeman, J. P. 1991, Foliar bacterial pathogens: epiphytic growth and interactions on leaves. J. Appl. Bacteriol. Symposium Supplement 70:49S–59S.Google Scholar
  10. Blakeman, J. P. and Brodie, I. D. S. 1977, Competition for nutrients between epiphytic microorganisms and germination of spores of plant pathogens on beetroot leaves. Physiol. Plant Pathol. 10:29–42.CrossRefGoogle Scholar
  11. Boland, G. J. and Inglis, G. D. 1989, Antagonism of white mold (Sclerotinia sclerotiorum) of bean by fungi from bean and rapeseed flowers. Can. J. Bot. 67:1775–1781.Google Scholar
  12. Burrage, S.W. 1976, Aerial microclimate around plant surfaces, pp. 173–184 In: Dickinson, C.H. and Preece, T.F., (eds.) Microbiology of Aerial Plant Surfaces. London: Academic Press.Google Scholar
  13. Chakraborty, B. N., Chakraborty, U. and Basu, K. 1994, Antagonism of Erwinia herbicola towards Leptosphaeria maculans causing blackleg disease of Brassica napus. Letters in Appl. Microbiol. 18:74–76.Google Scholar
  14. Cherif, M. and Benhamou, N. 1990, Cytochemical aspects of chitin breakdown during the parasitic action of a Trichoderma sp. on Fusarium oxysporum f. sp. radicis-lycopersici. Phytopathology 80:1406–1414.Google Scholar
  15. Chernin, L., Ismailov, Z., Haran, S. and Chet, I. 1995, Chitinolytic Enterobacter agglomerans antagonistic to fungal plant pathogens. Appl. Environ. Microbiol. 61(5):1720–1726.PubMedGoogle Scholar
  16. Corbell, N. and Loper, J. E. 1995, A global regulator of secondary metabolite production in Pseudomonas fluorescens strain Pf-5. J. Bacteriol. 177:6230–6236.PubMedGoogle Scholar
  17. Cullen, D. and Andrews, J.H. 1984, Epiphytic microbes as biological control agents, pp. 381–399 In: Kosuge, T. and Nestler, E.W., (eds.) Plant-microbe Interactions. New York: MacMillan Publishing Company.Google Scholar
  18. Di Pietro, A., Lorito, M., Hayes, C. K., Broadway, R. M. and Harman, G. E. 1993, Endochitinase from Gliocladium virens: isolation, characterization, and synergistic antifungal activity in combination with gliotoxin. Phytopathology 83:308–313.CrossRefGoogle Scholar
  19. Dickinson, C. H. 1967, Fungal colonization of Pisum leaves. Can. J. Bot. 45:915Google Scholar
  20. Dik, A. J., Fokkema, N. J. and van Pelt, J. A. 1992, Influence of climatic and nutritional factors on yeast population dynamics in the phyllosphere of wheat. Microb. Ecol. 23:41–52.CrossRefGoogle Scholar
  21. Elad, Y., Köhl, J. and Fokkema, N. J. 1994, Control of infection and sporulation of Botrytis cinerea on bean and tomato by saprophytic yeasts. Phytopathology 84:1193–1200.CrossRefGoogle Scholar
  22. Fernandes, J. M. C., Sutton, J. C. and James, T. D. W. 1991, A sensor for monitoring moisture of wheat residues: Application in ascospore maturation of Pyrenophora tritici-repentis. Plant Dis. 75:1101–1105.CrossRefGoogle Scholar
  23. Fiala, V., Glad, C., Martin, M., Jolivet, E. and Derridj, S. 1990. Occurrence of soluble carbohydrates on the phylloplane of maize (Zea mays L.): variations in relation to leaf heterogeneity and position on the plant. New Phytol. 115:609–615.CrossRefGoogle Scholar
  24. Fokkema, N. J. 1993, Opportunities and problems of control of foliar pathogens with micro-organisms. Pestic. Sci. 37:411–416.CrossRefGoogle Scholar
  25. Haran, S., Schickler, H., Oppenheim, A. and Chet, I. 1995, New components of the chitinolytic system of Trichoderma harzianum. Mycol. Res. 99(4):441–446.Google Scholar
  26. Hengge-Aronis, R. 1993, Survival of hunger and stress: The role of rpoS in early stationary phase gene regulation in E. coli. Cell 72:165–168.PubMedCrossRefGoogle Scholar
  27. Heye, C. C. and Andrews, J. H. 1983, Antagonism of Athelia bombacina and Chaetomium globosum to the apple scab pathogen, Venturia inaequalis. Phytopathology 73:650–654.Google Scholar
  28. Howell, C. R. and Stipanovic, R. D. 1980, Suppression of Pythium ultimum-induced damping-off of cotton seedlings by Pseudomonas fluorescens and its antibiotic, pyoluteorin. Phytopathology 70:712–715.Google Scholar
  29. Hrabak, E. M. and Willis, D. K. 1992, The lemA required for pathogenicity of Pseudomonas syringae pv. syringae on bean is a member of a family of two-component regulators. J. Bacteriol. 174:3011–3020.PubMedGoogle Scholar
  30. Hudson, H. J. 1968, The ecology of fungi on plant remains above the soil. New Phytol. 67:837–874.CrossRefGoogle Scholar
  31. Hudson, H. J., Webster, J. 1958, Succession of fungi on decaying stems of Agropyron repens. Trans. Brit. Mycol. Soc. 41:165–177.Google Scholar
  32. James, T. D. W., Sutton, J. C. and Rowell, P. M. 1984, Monitoring wetness of dead onion leaves in relation to Botrytis leaf blight. Proc. British Crop Protection Conference 2:627–632.Google Scholar
  33. Kempf, H. J. and Wolf, G. 1989, Erwinia herbicola as a biocontrol agent of Fusarium culmorum and Puccinia recondita f. sp. tritici on wheat. Phytopathology 79:990–994.Google Scholar
  34. Kinkel, L. 1991, Fungal community dynamics, pp. 253–270 In: Andrews, J.H. and Hirano, S.S., (eds.) Microbial Ecology of Leaves. New York: Springer-Verlag.Google Scholar
  35. Köhl, J. and Fokkema, N.J. 1994, Fungal interactions on living and necrotic leaves, pp. 321–334 In: Blakeman, J.P. and Williamson, B., (eds.) Ecology of Plant Pathogens., Oxon, UK: CAB International.Google Scholar
  36. Köhl, J., Molhoek, W. M. L., van der Plas, C. H. and Fokkema, N. J. 1995, Suppression of sporulation of Botrytis spp. as a valid biocontrol strategy. Eur. J. Plant Pathol. 101:251–259.CrossRefGoogle Scholar
  37. Köhl, J., Molhoek, W. M. L., van der Plas, C. H. and Fokkema, N. J. 1995, Effect of Ulocladium atrum and other antagonists on sporulation of Botrytis cinerea on dead lily leaves exposed to field conditions. Phytopathology 85:393–401.CrossRefGoogle Scholar
  38. Köhl, J., van der Plas, C. H., Molhoek, W. M. L. and Fokkema, N. J. 1995, Effect of interrupted leaf wetness periods on suppression of sporulation of Botrytis allii and B. cinerea by antagonists on dead onion leaves. Eur. J. Plant Pathol. 101:627–637.CrossRefGoogle Scholar
  39. Kolattukudy, P. E., Rogers, L. M., Li, D., Hwang, C., and Flaishman, M. A. 1995, Surface signalling in pathogenesis. Proc. Nat. Acad. Sci. USA 92:4080–4087.PubMedCrossRefGoogle Scholar
  40. Lorito, M., Di Pietro, A., Hayes, C. K., Woo, S. L. and Harman, G. E. 1993, Antifungal, synergistic interaction between chitinolytic enzymes from Trichoderma harzianum and Enterobacter cloacae. Phytopathology 83:721–728.CrossRefGoogle Scholar
  41. Lorito, M., Hayes, C. K., Di Pietro, A., Woo, S. L. and Harman, G. E. 1994, Purification, characterization, and synergistic activity of a glucan 1,3-ß-glucosidase and an N-Acetyl-ß-Glucosaminidase from Trichoderma harzianum. Phytopathology 84:398–405.CrossRefGoogle Scholar
  42. Magan, N. and Lacey, J. 1984, Effect of water activity, temperature and substrate on interactions between field and storage fungi. Trans. Brit. Mycol. Soc. 82:83–93.CrossRefGoogle Scholar
  43. Mercier, J. and Reeleder, R. D. 1987, Interactions between Sclerotinia sclerotiorum and other fungi on the phylloplane of lettuce. Can. J. Bot. 65:1633–1637.Google Scholar
  44. Morgan, J. V. and Tukey, H. B. 1964, Characterization of leachate from plant foliage. Plant Physiol. 39:590–593.PubMedGoogle Scholar
  45. Nowak-Thompson, B. and Gould, S. J. 1994, Production of 2,4-diacetylphloroglucinol by the biocontrol agent Pseudomonas fluorescens Pf-5. Can. J. Microbiol. 40:1064–1066.CrossRefGoogle Scholar
  46. Peng, G., Sutton, J. C. 1991, Evaluation of microorganisms for biocontrol of Botrytis cinerea in strawberry. Can J. Plant Pathol. 13:247–257.CrossRefGoogle Scholar
  47. Pfender, W. F. 1988, Suppression of ascocarp formation in Pyrenophora tritici-repentis by Limonomyces roseipellis, a basidiomycete from reduced-tillage wheat straw. Phytopathology 78:1254–1258.Google Scholar
  48. Pfender, W. F., King, L. G. and Rabe, J. R. 1991, Use of dual-stain fluorescence microscopy to observe antagonism of Pyrenophora tritici-repentis by Limonomyces roseipellis in wheat straw. Phytopathology 81:109–112.Google Scholar
  49. Pfender, W. F., Kraus, J. and Loper, J. E. 1993, A genomic region from Pseudomonas fluorescens Pf-5 required for pyrrolnitrin production and inhibition of Pyrenophora tritici-repentis in wheat straw. Phytopathology 83:1223–1228.CrossRefGoogle Scholar
  50. Pfender, W. F., Sharma, U. and Zhang, W. 1991, Effect of water potential on microbial antagonism to Pyrenophora tritici-repentis in wheat residue. Mycol. Res. 95:308–314.CrossRefGoogle Scholar
  51. Pfender, W. F. and Wootke, S. L. 1988, Microbial communities of Pyrenophora-infested wheat straw as examined by multivariate analysis. Microb. Ecol. 15:95–113.CrossRefGoogle Scholar
  52. Pfender, W. F., Zhang, W. and Nus, A. 1993, Biological control to reduce inoculum of the tan spot pathogen Pyrenophora tritici-repentis in surface-borne residues of wheat fields. Phytopathology 83:371–375.CrossRefGoogle Scholar
  53. Powelson, R. L. 1960, Initiation of strawberry fruit rot caused by Botrytis cinerea. Phytopathology 50:491–494.Google Scholar
  54. Sarniguet, A., Kraus, J., Henkels, M.D., Muelchen, A.M. and Loper, J.E. 1995, An rpoS homolog affects antibiotic production and biological control activity of Pseudomonas fluorescens Pf-5. Proc. Nat. Acad. Sci. USA 92:12255–12259.PubMedCrossRefGoogle Scholar
  55. Shapira, R., Ordentlich, A., Chet, I. and Oppenheim, A. B. 1989, Control of plant diseases by chitinase expressed from cloned DNA in Escherichia coli. Phytopathology 79:1246–1249.Google Scholar
  56. Silvertown, J.W. 1982, Interactions in mixtures of species, pp. 147–165 In: Silvertown, J.W. Introduction to Plant Population Ecology. New York: Longman.Google Scholar
  57. Sitepu, D. and Wallace, H. R. 1984, Biological control of Sclerotinia sclerotiorum in lettuce by Fusarium lateritium. Aust. J. Exp. Agric. Anim. Husb. 24:272–276.CrossRefGoogle Scholar
  58. Sutton, J. C. 1990, Epidemiology and management of botrytis leaf blight of onion and gray mold of strawberry: a comparative analysis. Can. J. Plant Pathol. 12:100–110.CrossRefGoogle Scholar
  59. Sutton, J. C. and Peng, G. 1993, Biocontrol of Botrytis cinerea in strawberry leaves. Phytopathology 83:615–621.CrossRefGoogle Scholar
  60. Tronsmo, A. 1992, Leaf and blossom epiphytes and endophytes as biological control agents, pp. 43–54 In: Tjamos, E.S. (ed.) Biological Control of Plant Diseases. New York: Plenum Press.Google Scholar
  61. Wicklow, D.T. 1992, Interference competition, pp. 265–274 In: Carroll, G.C. and Wicklow, D.T (eds.) The Fungal Community: Its Organization and Role in the Ecosystem. 2nd ed. New York: Marcel Dekker, vol. 15.Google Scholar
  62. Wilhite, S. E., Lumsden, R. D. and Straney, D. C. 1994, Mutational analysis of gliotoxin production by the biocontrol fungus Gliocladium virens in relation to suppression of Pythium damping-off. Phytopathology 84:816–821.CrossRefGoogle Scholar
  63. Wilson, M., Savka, M. A., Hwang, I., Farrand, K. and Lindow, S. E. 1995, Altered epiphytic colonization of mannityl opine-producing transgenic tobacco plants by a mannityl opine-catabolizing strain of Pseudomonas syringae. Appl. Environ. Microbiol. 61:2151–2158.PubMedGoogle Scholar
  64. Yuen, G. Y., Craig, M. L., Kerr, E. D. and Steadman, J. R. 1994, Influences of antagonist population levels, blossom development stage, and canopy temperature on the inhibition of Sclerotinia sclerotiorum on dry edible bean by Erwinia herbicola. Phytopathology 84:495–501.CrossRefGoogle Scholar
  65. Zhang, W. and Pfender, W. F. 1992, Effect of residue management on wetness duration and ascocarp production by Pyrenophora tritici-repentis in wheat residue. Phytopathology 82:1434–1439.Google Scholar
  66. Zhang, W. and Pfender, W. F. 1993, Effect of wetting-period duration on ascocarp suppression by selected antagonistic fungi in wheat straw infested with Pyrenophora tritici-repentis. Phytopathology 83:1288–1293.CrossRefGoogle Scholar
  67. Zhou, T. and Reeleder, R. D. 1989, Application of Epicoccum purpurascens spores to control white mold of snap bean. Plant Dis. 73:639–642.CrossRefGoogle Scholar
  68. Zhou, T. and Reeleder, R. D. 1991, Colonization of bean flowers by Epicoccum purpurascens. Phytopathology 81:774–778.Google Scholar
  69. Zhou, T., Reeleder, R. D. and Sparace, S. A. 1991, Interactions between Sclerotinia sclerotiorum and Epicoccum purpurascens. Can. J. Bot. 69:2503–2510.Google Scholar

Copyright information

© Plenum Press, New York 1996

Authors and Affiliations

  • William F. Pfender
    • 1
  1. 1.Department of Plant Pathology 4024 Throckmorton Plant Science CenterKansas State UniversityManhattan

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