Functional groups of plant pathogens in agroecosystems: a review

Abstract

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.

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References

  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.

    Article  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.

  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.

    CAS  PubMed  Article  Google Scholar 

  5. Altieri, M. A. (1987). Agroecology: The scientific basis of alternative agriculture. Westview Press.

  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.

    Article  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.

  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.

    Article  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.

  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.

  11. Boudreau, M. A. (2013). Diseases in intercropping systems. Annual Review of Phytopathology, 51, 499–519.

    CAS  PubMed  Article  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.

  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.

  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.

    Article  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.

    Article  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.

    Article  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.

    CAS  PubMed  Article  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.

  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.

    CAS  PubMed  Article  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.

  24. Keesing, F., Holt, R. D., & Ostfeld, R. S. (2006). Effects of species diversity on disease risk. Ecology Letters, 9, 485–498.

    CAS  PubMed  Article  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.

    Article  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.

    Article  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.

    Article  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.

  30. Lewis, D. H. (1972). Concepts in fungal nutrition and the origin of biotrophy. Biological Reviews, 48(2), 261–277.

    Article  Google Scholar 

  31. Lockwood, J. L. (1988). Evolution of concepts associated with soilborne plant pathogens. Annual Review of Phytopathology, 26(1), 93–121.

    Article  Google Scholar 

  32. Luttrell, E. S. (1974). Parasitism of fungi on vascular plants. Mycologia, 66(1), 1–15.

    Article  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.

    Article  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.

    CAS  PubMed  Article  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.

    Article  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.

    Article  Google Scholar 

  38. Moonen, A. C., & Bàrberi, P. (2008). Functional biodiversity: An agroecosystem approach. Agriculture, Ecosystems & Environment., 127(1–2), 7–21.

    Article  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.

  40. Mundt, C. C. (2002). Use of multiline cultivars and cultivar mixtures for disease management. Annual Review of Phytopathology, 40(1), 381–410.

    CAS  PubMed  Article  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.

  42. Noble, M., De Temple, J., & Neergaard, P. (1958). An annotated list of seed-borne diseases.

  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.

    CAS  PubMed  Article  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.

    CAS  PubMed  Article  Google Scholar 

  45. Perfecto, I., Vandermeer, J., & Wright, A. (2009). Nature’s matrix: linking agriculture, conservation and food sovereignty (pp. 272). London: Routledge.

  46. Phatak, H. C. (1974). Seed-borne plant viruses-identification and diagnosis in seed health testing. Seed Science and Technology, 2(3).

  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.

    Article  Google Scholar 

  48. Power, A. G., & Mitchel, C. E. (2004). Pathogen spillover in disease epidemics. The American Naturalist, 164, S69–S89.

    Article  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.

  50. Reeleder, R. D. (2003). Fungal plant pathogens and soil biodiversity. Canadian Journal of Soil Science, 83, 331–336.

    Article  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.

    Article  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.

  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.

  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.

  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.

    Article  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.

    Article  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.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  58. Tresh, J. M. (1982). Cropping practices and virus spread. Annual Review of Phytopathology, 20, 193–218.

    Article  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.

    Article  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.

    PubMed  Article  CAS  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.

    PubMed  Article  CAS  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.

    Article  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.

    Article  Google Scholar 

  65. Vizvary, M. A., & Warren, H. L. (1982). Survival of Colletotrichum graminicola in soil. Phytopathology, 72(5), 522–525.

    Article  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.

    Article  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.

    CAS  PubMed  Article  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.

    Article  Google Scholar 

  69. Wilhelm, S. (1951). Is verticillium albo-atrum a soil invader or a soil inhabitant. Phytopathology, 41(10), 944–945.

  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.

    Article  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.

    Article  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.

    CAS  PubMed  Article  Google Scholar 

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Acknowledgements

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.

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

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Correspondence to Damián Vega.

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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.

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Vega, D., Gally, M.E., Romero, A.M. et al. Functional groups of plant pathogens in agroecosystems: a review. Eur J Plant Pathol 153, 695–713 (2019). https://doi.org/10.1007/s10658-018-01616-8

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Keywords

  • Agroecology
  • Crop diseases
  • Cropping systems design
  • Ecological disease management