European Journal of Plant Pathology

, Volume 153, Issue 3, pp 695–713 | Cite as

Functional groups of plant pathogens in agroecosystems: a review

  • Damián VegaEmail author
  • Marcela E. Gally
  • Ana M. Romero
  • Santiago L. Poggio


The concept of functional groups (set of species having similar physiological, ecological or life-history traits) has been largely used for plants, microorganisms, nematodes or insects in agroecosystems. However, this concept has been rarely applied to describe assemblages of plant pathogens. Yet, classification systems in plant pathology resemble this functional approach, as they address different disease processes or life history traits. In this review, we discuss advantages and drawbacks of current classification systems in relation to their application to the ecological management of crop diseases. Then, we propose to reorganize one of the classical plant-pathogen systems in a dichotomous key of functional groups obtained by combining two life-history traits: dispersal and survival strategies. The six functional groups proposed here are soil inhabitants; soil survivors; debris-seed-borne; air-borne; seed-borne, and vector-borne pathogens. We applied these groups to characterize pathogens of two major crops, wheat and tomato, grown in temperate climate regions. Our contribution intends to provide a comprehensive conceptual framework for the design of crop disease management strategies based on ecological principles, as well as to facilitate the interpretation of the occurrence of epidemics in response to the agricultural practices applied in real-world agroecosystems.


Agroecology Crop diseases Cropping systems design Ecological disease management 



This article is part of the Doctoral Thesis of D. Vega, developed at the Doctoral Program in Agroecology, University of Antioquia (Medellin, Colombia), which is held in association with the Sociedad Científica Latinoamericana de Agroecología (SOCLA). S. L. Poggio is member of CONICET (Consejo Nacional de Investigaciones Científicas y Técnicas), the National Scientific and Technical Research Council of Argentina.


This article has been supported by grants from UBACyT (20020130100501BA, 2014–2017).

Compliance with ethical standards

Conflict of interest

Damián Vega declares that he has no conflict of interest. Marcela E. Gally declares that she has no conflict of interest. Ana María Romero declares that she has no conflict of interest. Santiago L. Poggio declares that he has no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.


  1. Abdala Roberts, L., Mooney, K. A., Quijano-Medina, T., Campos Navarrete, M. J., González Moreno, A., & Parra Tabla, V. (2015). Comparison of tree genotypic diversity and species diversity effects on different guilds of insect herbivores. Oikos, 124(11), 1527–1535.Google Scholar
  2. Agrios, G. N. (1969). Plant pathology. New York: Academic Press.Google Scholar
  3. Agrios, G. N. (2005). Plant Pathology. Fifth edition (p. 922). Elsevier academic press.Google Scholar
  4. Alfano, J. R., & Collmer, A. (2004). Type III secretion system effector proteins: Double agents in bacterial disease and plant defense. Annual Review of Phytopathology, 42, 385–414.Google Scholar
  5. Altieri, M. A. (1987). Agroecology: The scientific basis of alternative agriculture. Westview Press.Google Scholar
  6. Bannon, F. J., & Cooke, B. M. (1998). Studies on dispersal of Septoria tritici pycnidiospores in wheat–clover intercrops. Plant Pathology, 47(1), 49–56.Google Scholar
  7. Berkelmans, R., Ferris, H., Tenuta, M., and van Bruggen, A.H.C. (2003). Effects of long-term crop management on higher trophic levels of nematodes than plant parasitic nematodes disappear after 1 year of uniform management. Applied Soil Ecology. 23: 223–235.Google Scholar
  8. Bockus, W. W. (1983). Effects of fall infection by Gaeumannomyces graminis var. tritici and triadimenol seed treatment on severity of take-all in winter wheat. Phytopathology, 73(4), 540–543.Google Scholar
  9. Bockus, W.W., Bowden, R.L., Hunger, R.M., Morrill, W.L., Murray, T.D. & Smiley, R.W. (ed) (2010) Compendium of wheat diseases and pests, Third Edition.Google Scholar
  10. De Boer, S.H. (1982) Survival of phytopathogenic bacteria in soil. Chapter 12. In: Mount, M.S., Lacy, G.H. (ed) Phytopathogenic prokaryotes, Vol.1. pp 285–302.Google Scholar
  11. Boudreau, M. A. (2013). Diseases in intercropping systems. Annual Review of Phytopathology, 51, 499–519.Google Scholar
  12. Brown, J. (1997). Survival and dispersal of plant parasites: general concepts. In J. F. Brown & H. J. Ogle (Eds.), Plant pathogens and plant diseases (pp. 195–231). Armidale: APPS.Google Scholar
  13. Cardina, J., Webster, T. M., Herms, C. P., & Regnier, E. E. (1999). Development of weed IPM: Levels of integration for weed management. Journal of Crop Production, 2(1), 239–267.Google Scholar
  14. Chaboussou, F. (1980). Plantes malades des pesticides: bases nouvelles d'une prevention contre maladies et parasites. Debard, 304 pp.Google Scholar
  15. Clark, D. P., Dunlap, P., Madigan, M., & Martinko, J. (2009). Brock biology of microorganisms.Google Scholar
  16. Gaumann, E. (1946). Types of defensive reactions in plants. Phytopathology, 36(8), 624–633.Google Scholar
  17. Gilligan, C. A. (2002). An epidemiological framework for disease management. Advances in Botanical Research, 38, 1–64.Google Scholar
  18. Gómez-Rodrıguez, O., Zavaleta-Mejıa, E., Gonzalez-Hernandez, V. A., Livera-Munoz, M., & Cárdenas-Soriano, E. (2003). Allelopathy and microclimatic modification of intercropping with marigold on tomato early blight disease development. Field Crops Research, 83(1), 27–34.Google Scholar
  19. Grose, M. J., Parker, C. A., & Sivasithamparam, K. (1984). Growth of Gaeumannomyces graminis var. tritici in soil: Effects of temperature and water potential. Soil Biology and Biochemistry, 16(3), 211–216.Google Scholar
  20. Gubbins, S., Gilligan, C. A., & Kleczkowski, A. (2000). Population dynamics of plant–parasite interactions: Thresholds for invasion. Theoretical Population Biology, 57, 219–233.Google Scholar
  21. Hiddink, G.A., Termorshuizen, A.J. & van Bruggen, A.H.C. (2009). Mixed cropping and suppression of soilborne diseases, a review. In: E. Lichtfouse (ed.), Genetic engineering, Biofertilisation, soil quality and organic farming, Sust. Agric. Rev. 4: 119–146.Google Scholar
  22. Irwin, M. E., Ruesink, W. G., Isard, S. A., & Kampmeier, G. E. (2000). Mitigating epidemics caused by non-persistently transmitted aphid-borne viruses: The role of the pliant environment. Virus Research, 71(1), 185–211.Google Scholar
  23. Jones, J.B., Zitter, T.A., Momol, T.M. & Miller, S.A. (ed) (2014) Compendium of Tomato Diseases and Pests, second edition. ISBN 978–0–89054-424-2. pp 176.Google Scholar
  24. Keesing, F., Holt, R. D., & Ostfeld, R. S. (2006). Effects of species diversity on disease risk. Ecology Letters, 9, 485–498.Google Scholar
  25. Kendall, D. A., Chinn, N. E., Smith, B. D., Tidboald, C., Winstone, L., & Western, N. M. (1991). Effects of straw disposal and tillage on spread of barley yellow dwarf virus in winter barley. Annals of Applied Biology, 119(2), 359–364.Google Scholar
  26. Knops, J. M. H., Tilman, D., Haddad, N. M., Naeem, S., Mitchell, C. E., Haarstad, J., Ritchie, M. E., Howe, K. M., Reich, P. B., Siemann, E., & Groth, J. (1999). Effects of plant species richness on invasión dynamics, disease outbreaks, insect abundances and diversity. Ecology Letters, 2, 286–293.Google Scholar
  27. Lavorel, S., & Garnier, É. (2002). Predicting changes in community composition and ecosystem functioning from plant traits: Revisiting the holy grail. Functional Ecology, 16(5), 545–556.Google Scholar
  28. Leoni, C., Rossing, W. A. H., & van Bruggen, A. H. C. (2015). Crop rotation. Chapter 4.2 in: Finckh, M., van Bruggen, a.H.C. and Tamm, L. (eds.) Plant Diseases and their Management in Organic Agriculture. APS press, St (pp. 127–140). Minnesota: Paul.Google Scholar
  29. Letourneau, D., & van Bruggen, A. H. C. (2006). Crop Protection. Ch 4. In P. Kristiansen, A. Taji, & J. Reganold (Eds.), Organic Agriculture: A Global Perspective (pp. 93–121). CSIRO.Google Scholar
  30. Lewis, D. H. (1972). Concepts in fungal nutrition and the origin of biotrophy. Biological Reviews, 48(2), 261–277.Google Scholar
  31. Lockwood, J. L. (1988). Evolution of concepts associated with soilborne plant pathogens. Annual Review of Phytopathology, 26(1), 93–121.Google Scholar
  32. Luttrell, E. S. (1974). Parasitism of fungi on vascular plants. Mycologia, 66(1), 1–15.Google Scholar
  33. Martin, A. R., & Isaac, M. E. (2018). Functional traits in agroecology: Advancing description and prediction in agroecosystems. Journal of Applied Ecology, 55(1), 5–11.Google Scholar
  34. McDonald, B. A., & Linde, C. (2002). Pathogen population genetics, evolutionary potential, and durable resistance. Annual Review of Phytopathology, 40(1), 349–379.Google Scholar
  35. McNew, G. L. (1960). The nature, origin, and evolution of parasitism. VI. The effects of environment on different classes of parasitism. B. the effects of mineral nutrition. Plant Pathology, 2, 48–52.Google Scholar
  36. Médiène, S., Morison, M. V., Sarthou, J. P., Tourdonnet, S., Gosme, M., Bertrand, M., Estrade, J. R., Aubertot, J. N., Rusch, A., Motisi, N., Pelosi, C., & Doré, T. (2011). Agroecosystem management and biotic interactions: A review. Agronomy for Sustainable Development, 31, 491–514.Google Scholar
  37. Mitchel, C. A., Tilman, D., & Groth, J. V. (2002). Effects of grass-land species diversity, abundance, and composition on foliar fungal diseases. Ecology, 83, 1713–1726.Google Scholar
  38. Moonen, A. C., & Bàrberi, P. (2008). Functional biodiversity: An agroecosystem approach. Agriculture, Ecosystems & Environment., 127(1–2), 7–21.Google Scholar
  39. Moule, G. Chapter 9 (1988). In: Halley, R. J., Soffe, R. J. (ed). Primrose McConnell’s The Agricultural Notebook. 18 th edition. Butterworths & co. publishers ltd. pp 269–287.Google Scholar
  40. Mundt, C. C. (2002). Use of multiline cultivars and cultivar mixtures for disease management. Annual Review of Phytopathology, 40(1), 381–410.Google Scholar
  41. Nicholls C.I. & Altieri, A.M. (2008). Suelos saludables, plantas saludables: la evidencia agroecológica. LEISA. Revista de Agroecología, 24(2), 6–8.Google Scholar
  42. Noble, M., De Temple, J., & Neergaard, P. (1958). An annotated list of seed-borne diseases.Google Scholar
  43. Oliver, R. P., & Ipcho, S. V. S. (2004). Arabidopsis pathology breathes new life into the necrotrophs-vs.-biotrophs classification of fungal pathogens. Molecular Plant Pathology, 5(4), 347–352.Google Scholar
  44. Perfect, S. E., & Green, J. R. (2001). Infection structures of biotrophic and hemibiotrophic fungal plant pathogens. Molecular Plant Pathology, 2(2), 101–108.Google Scholar
  45. Perfecto, I., Vandermeer, J., & Wright, A. (2009). Nature’s matrix: linking agriculture, conservation and food sovereignty (pp. 272). London: Routledge.Google Scholar
  46. Phatak, H. C. (1974). Seed-borne plant viruses-identification and diagnosis in seed health testing. Seed Science and Technology, 2(3).Google Scholar
  47. Poggio, S. L., Chaneton, E. J., & Ghersa, C. M. (2013). The arable plant diversity of intensively managed farmland: Effects of field position and crop type at local and landscape scales. Agriculture, Ecosystems & Environment, 166, 55–64.Google Scholar
  48. Power, A. G., & Mitchel, C. E. (2004). Pathogen spillover in disease epidemics. The American Naturalist, 164, S69–S89.Google Scholar
  49. Ratnadass, A., Fernandes, P., Avelino, J., y Habib, R. (2012). Plant species diversity for sustainable management of crop pests and diseases in agroecosystems: A review. Agronomy for Sustainable Development, 32(1), 273–303.Google Scholar
  50. Reeleder, R. D. (2003). Fungal plant pathogens and soil biodiversity. Canadian Journal of Soil Science, 83, 331–336.Google Scholar
  51. Rekah, Y., Shtienberg, D., & Katan, J. (2001). Population Dynamics of Fusarium Oxysporum f. Sp. Radicis-lycopersici in Relation to the Onset of Fusarium Crown and Root Rot of Tomato. European Journal of Plant Pathology, 107, 367.Google Scholar
  52. Schroth, M. N., Weinhold, A. R., McCain, A. H., Hildebrand, D. C., & Ross, N. (1971). Biology and control of agrobacterium tumefaciens. University of Calif.Google Scholar
  53. Sharma, O. P., & Bambawale, O. M. (2008). Integrated management of key diseases of cotton and rice. In A. Ciancio & K. G. Mukerji (Eds.), Integrated Management of Diseases Caused by Fungi, Phytoplasma and Bacteria (pp. 271–302). Springer Netherlands.Google Scholar
  54. Shennan, C. (2008). Biotic interactions, ecological knowledge and agriculture. Philosophical Transactions of the Royal Society of London. B: Biological Sciences, 363(1492), 717–739.Google Scholar
  55. Sutton, J. C., & Vyn, T. J. (1990). Crop sequences and tillage practices in relation to diseases of winter wheat in Ontario. Canadian Journal of Plant Pathology, 12, 358–368.Google Scholar
  56. Termorshuizen, A. J., & Jeger, M. J. (2009). Strategies of soilborne plant pathogenic fungi in relation to disease suppression. Fungal Ecology, 1, 108–114.Google Scholar
  57. Thaler, J. S., Owen, B., & Higgins, V. J. (2004). The role of the jasmonate response in plant susceptibility to diverse pathogens with a range of lifestyles. Plant Physiology, 135, 530–538.Google Scholar
  58. Tresh, J. M. (1982). Cropping practices and virus spread. Annual Review of Phytopathology, 20, 193–218.Google Scholar
  59. van Bruggen, A. H. C. (1995). Plant disease severity in high-input compared to reduced input and organic farming systems. Plant Disease., 79(10), 976–984.Google Scholar
  60. van Bruggen, A. H. C., & Finckh, M. (2016). Plant diseases and management approaches in organic farming systems. Annual Review of Phytopathology, 54, 25–54.Google Scholar
  61. van Bruggen, A. H. C., & Semenov, A. M. (2015). Soil health and soilborne diseases in organic agriculture. Chapter 3.2. In M. Finckh, A. H. C. van Bruggen, & L. Tamm (Eds.), Plant Diseases and their Management in Organic Agriculture (pp. 67–89). St. Paul, Minnesota: APS press.Google Scholar
  62. van Bruggen, A. H., Gamliel, A., & Finckh, M. R. (2016). Plant disease management in organic farming systems. Pest Management Science, 72(1), 30–44.Google Scholar
  63. Vatovec, C., Jordan, N., & Huerd, S. (2005). Responsiveness of certain agronomic weed species to arbuscular mycorrhizal fungi. Renewable Agriculture and Food Systems, 20(3), 181–189.Google Scholar
  64. Vega, D., & Romero, A. M. (2016). Survival of Clavibacter michiganensis subsp. michiganensis in tomato debris under greenhouse conditions. Plant Pathology, 65, 545–550.Google Scholar
  65. Vizvary, M. A., & Warren, H. L. (1982). Survival of Colletotrichum graminicola in soil. Phytopathology, 72(5), 522–525.Google Scholar
  66. Waggoner, P. E., Green, J. S. A., & Smith, F. B. (1983). The aerial dispersal of the pathogens of plant disease [and discussion]. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 302(1111), 451–462.Google Scholar
  67. Weller, D. M., Raaijmakers, J. M., Gardener, B. B. M., & Thomashow, L. S. (2002). Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annual Review of Phytopathology, 40(1), 309–348.Google Scholar
  68. West, J. S., Townsend, J. A., Stevens, M., & Fitt, B. D. L. (2012). Comparative biology of different plant pathogens to estimate effects of climate change on crop diseases in Europe. European Journal of Plant Pathology, 133, 315–331.Google Scholar
  69. Wilhelm, S. (1951). Is verticillium albo-atrum a soil invader or a soil inhabitant. Phytopathology, 41(10), 944–945.Google Scholar
  70. Wood, S. A., Karp, D. S., DeClerck, F., Kremen, C., Naeem, S., & Palm, C. A. (2015). Functional traits in agriculture: Agrobiodiversity and ecosystem services. Trends in Ecology & Evolution, 30(9), 531–539.Google Scholar
  71. Zanin, G., Otto, S., Riello, L., & Borin, M. (1997). Ecological interpretation of weed flora dynamics under different tillage systems. Agriculture, Ecosystems & Environment, 66(3), 177–188.Google Scholar
  72. Zhu, Y., Chen, H., Fan, J., Wang, Y., Li, Y., Chen, J., Fan, J., Yang, S., Hu, L., Leung, H., Mew, T. W., Teng, P. S., Wang, Z., & Mundt, C. C. (2000). Genetic diversity and disease control in rice. Nature, 406, 718–722.Google Scholar

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© Koninklijke Nederlandse Planteziektenkundige Vereniging 2018

Authors and Affiliations

  1. 1.Universidad de Buenos Aires. Facultad de Agronomía. Departamento de Producción Vegetal. Cátedra de Fitopatología.Buenos AiresArgentina
  2. 2.Universidad de Buenos Aires. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Ecología (IFEVA). Facultad de Agronomía. Departamento de Producción Vegetal. Cátedra de Producción Vegetal.Buenos AiresArgentina

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