Threats to global food security from emerging fungal and oomycete crop pathogens

Subjects

Abstract

Emerging fungal and oomycete pathogens infect staple calorie crops and economically important commodity crops, thereby posing a significant risk to global food security. Our current agricultural systems — with emphasis on intensive monoculture practices — and globalized markets drive the emergence and spread of new pathogens and problematic traits, such as fungicide resistance. Climate change further promotes the emergence of pathogens on new crops and in new places. Here we review the factors affecting the introduction and spread of pathogens and current disease control strategies, illustrating these with the historic example of the Irish potato famine and contemporary examples of soybean rust, wheat blast and blotch, banana wilt and cassava root rot. Our Review looks to the future, summarizing what we see as the main challenges and knowledge gaps, and highlighting the direction that research must take to face the challenge of emerging crop pathogens.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: Anthropogenic effects that impact the disease triangle.
Fig. 2: Spread of F. oxysporum f. sp. cubense TR4 throughout global banana-growing regions.
Fig. 3: National changes in cropping diversity.
Fig. 4: Parameterizing the disease triangle in evolutionary time.

Change history

  • 06 July 2020

    An amendment to this paper has been published and can be accessed via a link at the top of the paper.

References

  1. 1.

    Anderson, P. K., Cunningham, A. A., Patel, N. G., Morales, F. J., Epstein, P. R. & Daszak, P. Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends Ecol. Evol. 19, 535–544 (2004).

    PubMed  Google Scholar 

  2. 2.

    Fisher, M. C. et al. Emerging fungal threats to animal, plant and ecosystem health. Nature 484, 186 (2012).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  3. 3.

    Fones, H. N., Fisher, M. C. & Gurr, S. J. Emerging fungal threats to plants and animals challenge agriculture and ecosystem resilience. Microbiol. Spec. https://doi.org/10.1128/microbiolspec.FUNK-0027-2016 (2017).

  4. 4.

    Bebber, D. P., Ramotowski, M. A. & Gurr, S. J. Crop pests and pathogens move polewards in a warming world. Nat. Clim. Change 3, 985–988 (2013).

    ADS  Google Scholar 

  5. 5.

    Fones, H. N. & Gurr, S. J. NOXious gases and the unpredictability of emerging plant pathogens under climate change. BMC Biol. 15, 36 (2017).

    PubMed  PubMed Central  Google Scholar 

  6. 6.

    Manning, W. J. & Tiedemann, A. V. Climate change: potential effects of increased atmospheric carbon dioxide (CO2), ozone (O3), and ultraviolet-B (UV-B) radiation on plant diseases. Environ. Pollut. 88, 219–245 (1995).

    CAS  PubMed  Google Scholar 

  7. 7.

    Ahmed, S., de Labrouhe, D. T. & Delmotte, F. Emerging virulence arising from hybridisation facilitated by multiple introductions of the sunflower downy mildew pathogen Plasmopara halstedii. Fungal Genet. Biol. 49, 847–855 (2012).

    CAS  PubMed  Google Scholar 

  8. 8.

    Stukenbrock, E. H. Evolution, selection and isolation: a genomic view of speciation in fungal plant pathogens. New Phytol. 199, 895–907 (2013).

    PubMed  Google Scholar 

  9. 9.

    Meentemeyer, R. K., Haas, S. E. & Václavík, T. Landscape epidemiology of emerging infectious diseases in natural and human-altered ecosystems. Ann. Rev. Phytopathol 50, 379–402 (2012).

    CAS  Google Scholar 

  10. 10.

    Turner, R. S. After the famine: plant pathology, Phytophthora infestans and the late blight of potatoes, 1845–1960. Hist. Stud. Phys. Biol. Sci. 34, 341–370 (2005).

    Google Scholar 

  11. 11.

    Fry, W. Phytophthora infestans: the plant (and R gene) destroyer. Molec. Plant Pathol 9, 385–402 (2008).

    Google Scholar 

  12. 12.

    Ristaino, J. B., Groves, C. T. & Parra, G. R. PCR amplification of the Irish potato famine pathogen from historic specimens. Nature 411, 695–697 (2001).

    ADS  CAS  PubMed  Google Scholar 

  13. 13.

    Ristaino, J. B. Tracking historic migrations of the Irish potato famine pathogen, Phytophthora infestans. Microbes Infect. 4, 1369–1377 (2002).

    PubMed  Google Scholar 

  14. 14.

    Yoshida, K. et al. The rise and fall of the Phytophthora infestans lineage that triggered the Irish potato famine. eLife 2, e00731 (2013).

    PubMed  PubMed Central  Google Scholar 

  15. 15.

    Goodwin, S. B., Cohen, B. A. & Fry, W. E. Panglobal distribution of a single clonal lineage of the Irish potato famine fungus. Proc. Natl Acad. Sci. USA 91, 11591–11595 (1994).

    ADS  CAS  PubMed  Google Scholar 

  16. 16.

    Fry, W. E. et al. Five reasons to consider Phytophthora infestans a reemerging pathogen. Phytopathol. 105, 966–981 (2015).

  17. 17.

    Goodwin, S. B., Sujkowski, L. S. & Fry, W. E. Rapid evolution of pathogenicity within clonal lineages of the potato late blight disease fungus. Phytopathol 85, 669–676 (1995).

    Google Scholar 

  18. 18.

    Drenth, A., Janssen, E. M. & Govers, F. Formation and survival of oospores of Phytophthora infestans under natural conditions. Plant Pathol. 44, 86–94 (1995).

    Google Scholar 

  19. 19.

    Andersson, B., Sandstrom, M. & Stromberg, A. Indications of soil borne inoculum of Phytophthora infestans. Potato Res. 41, 305–310 (1998).

    Google Scholar 

  20. 20.

    Fischer, T., Byerlee, D. & Edmeades, G. Crop Yields and Global Food Security (ACIAR, 2014).

  21. 21.

    The State of Food and Agriculture No. 37 (FAO, 2006).

  22. 22.

    FAOSTAT (FAO, 2016); http://www.fao.org/faostat/en/#data

  23. 23.

    Cassidy, E. S., West, P. C., Gerber, J. S. & Foley, J. A. Redefining agricultural yields: from tonnes to people nourished per hectare. Environ. Res. Lett. 8, 034015 (2013).

    ADS  Google Scholar 

  24. 24.

    Burles, D. Dimensions of Need: An Atlas of Food and Agriculture (FAO, 1995).

  25. 25.

    Bancroft, J. Report of the board appointed to enquire into the cause of disease affecting livestock and plants. Votes Proc. 3, 1011–1038 (1876).

    Google Scholar 

  26. 26.

    Ploetz, R. C. Panama disease: a classic and destructive disease of banana. Plant Health Prog. https://doi.org/10.1094/PHP-2000-1204-01-HM (2000).

  27. 27.

    Hippolyte, I. et al. Foundation characteristics of edible Musa triploids revealed from allelic distribution of SSR markers. Ann. Bot. 109, 937–951 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. 28.

    Ordonez., N. et al. Worse comes to worst: bananas and Panama disease – when plant and pathogen clones meet. PLoS Pathog. 11, e1005197 (2015).

    PubMed  PubMed Central  Google Scholar 

  29. 29.

    Galvis, S. Colombia confirms that dreaded fungus has hit its banana plantations. Science https://doi.org/10.1126/science.aaz1033 (2019).

    Article  Google Scholar 

  30. 30.

    Rajaram, S. Norman Borlaug: the man I worked with and knew. Ann. Rev. Phytopathol. 49, 17–30 (2011).

    CAS  Google Scholar 

  31. 31.

    Weiner, J. Applying plant ecological knowledge to increase agricultural sustainability. J. Ecol. 105, 865–870 (2017).

    Google Scholar 

  32. 32.

    Evenson, R. E. & Gollin, D. Assessing the impact of the Green Revolution, 1960 to 2000. Science 300, 758–762 (2003).

  33. 33.

    Trewavas, A. Malthus foiled again and again. Nature 418, 668–670 (2002).

    ADS  CAS  PubMed  Google Scholar 

  34. 34.

    Tilman, D., Cassman, K. G., Matson, P. A., Naylor, R. & Polasky, S. Agricultural sustainability and intensive production practices. Nature 418, 671–677 (2002).

    ADS  CAS  PubMed  Google Scholar 

  35. 35.

    Fones, H. & Gurr, S. The impact of Septoria tritici blotch disease on wheat: an EU perspective. Fungal Genet. Biol. 79, 3–7 (2015).

    PubMed  PubMed Central  Google Scholar 

  36. 36.

    Linde, C. C., Zhan, J. & McDonald, B. A. Population structure of Mycosphaerella graminicola: from lesions to continents. Phytopathology 92, 946–955 (2002).

    CAS  PubMed  Google Scholar 

  37. 37.

    McDonald, B. A. & Stukenbrock, E. H. Rapid emergence of pathogens in agro-ecosystems: global threats to agricultural sustainability and food security. Phil. Trans. Royal Soc. B 371, 20160026 (2016).

    Google Scholar 

  38. 38.

    Zhan, J., Pettway, R. E. & McDonald, B. A. The global genetic structure of the wheat pathogen Mycosphaerella graminicola is characterized by high nuclear diversity, low mitochondrial diversity, regular recombination, and gene flow. Fungal Genet. Biol. 38, 286–297 (2003).

    CAS  PubMed  Google Scholar 

  39. 39.

    Möller, M. & Stukenbrock, E. H. Evolution and genome architecture in fungal plant pathogens. Nat. Rev. Microbiol. 15, 756–771 (2017).

    PubMed  Google Scholar 

  40. 40.

    Plissonneau, C., Stürchler, A. & Croll, D. The evolution of orphan regions in genomes of a fungal pathogen of wheat. mBio 7, e01231-16 (2016).

    PubMed  PubMed Central  Google Scholar 

  41. 41.

    Stukenbrock, E. H. et al. The making of a new pathogen: insights from comparative population genomics of the domesticated wheat pathogen Mycosphaerella graminicola and its wild sister species. Genome Res. 21, 2157–2166 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  42. 42.

    Croll, D., Zala, M. & McDonald, B. A. Breakage-fusion-bridge cycles and large insertions contribute to the rapid evolution of accessory chromosomes in a fungal pathogen. PLoS Genet. 9, e1003567 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  43. 43.

    Wittenberg, A. H. et al. Meiosis drives extraordinary genome plasticity in the haploid fungal plant pathogen Mycosphaerella graminicola. PLoS One 4, e5863 (2009).

    ADS  PubMed  PubMed Central  Google Scholar 

  44. 44.

    Fones, H. N., Eyles, C. J., Kay, W., Cowper, J. & Gurr, S. J. A role for random, humidity-dependent epiphytic growth prior to invasion of wheat by Zymoseptoria tritici. Fungal Genet. Biol. 106, 51–60 (2017).

    PubMed  PubMed Central  Google Scholar 

  45. 45.

    Suffert, F., Sache, I. & Lannou, C. Early stages of Septoria tritici blotch epidemics of winter wheat: build-up, overseasoning, and release of primary inoculum. Plant Pathol. 60, 166–177 (2011).

    Google Scholar 

  46. 46.

    Suffert, F., Ravigné, V. & Sache, I. Seasonal changes drive short-term selection for fitness traits in the wheat pathogen Zymoseptoria tritici. Appl. Environ. Microbiol. 81, 6367–6379 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  47. 47.

    van den Berg, F., Paveley, N. D. & van den Bosch, F. Dose and number of applications that maximize fungicide effective life exemplified by Zymoseptoria tritici on wheat – a model analysis. Plant Pathol. 65, 1380–1389 (2016).

    PubMed  PubMed Central  Google Scholar 

  48. 48.

    Torriani, S. F. et al. Zymoseptoria tritici: a major threat to wheat production, integrated approaches to control. Fungal Genet. Biol. 79, 8–12 (2015).

    PubMed  Google Scholar 

  49. 49.

    Li, X. et al. The uniqueness of the soybean rust pathosystem: an improved understanding of the risk in different regions of the world. Plant Dis. 94, 796–806 (2010).

    CAS  PubMed  Google Scholar 

  50. 50.

    Rosa, C. R. E., Spehar, C. R. & Liu, J. Q. Asian soybean rust resistance: an overview. J. Plant Pathol. Microbiol. https://doi.org/10.4172/2157-7471.1000307 (2015).

  51. 51.

    Childs, S. P., Buck, J. W. & Li, Z. Breeding soybeans with resistance to soybean rust (Phakopsora pachyrhizi). Plant Breeding 137, 250–261 (2018).

    CAS  Google Scholar 

  52. 52.

    Islam, M. T. et al. Emergence of wheat blast in Bangladesh was caused by a South American lineage of Magnaporthe oryzae. BMC Biol. 14, 84 (2016).

    PubMed  PubMed Central  Google Scholar 

  53. 53.

    Valent, B. et al. Pyricularia graminis-tritici is not the correct species name for the wheat blast fungus: response to Ceresini et al. Molec. Plant. Pathol. 20, 173–179 (2019).

  54. 54.

    Skamnioti, P. & Gurr, S. J. Against the grain: safeguarding rice from rice blast disease. Trends Biotech. 27, 141–150 (2009).

    CAS  Google Scholar 

  55. 55.

    Stukenbrock, E. H. & McDonald, B. A. The origins of plant pathogens in agro-ecosystems. Annu. Rev. Phytopathol. 46, 75–100 (2008).

    CAS  PubMed  Google Scholar 

  56. 56.

    Ceresini, P. C. et al. Wheat blast: from its origins in South America to its emergence as a global threat. Molec. Plant Pathol. 20, 155–172 (2019).

  57. 57.

    DÁvila, L. S., De Filippi, M. C. C. & Café-Filho, A. C. Both MAT1–1 and MAT 1–2 idiomorphs present in rice blast populations (Magnaporthe oryzae) collected in rice fields in northern Brazil. New Dis. Rep. 40, 3 (2019).

  58. 58.

    Prabhu, A. S., Filippi, M. C., Silva, G. B., Lobo, V. L. S. & Morais, O. P. in Advances in Genetics, Genomics and Control of Rice Blast Disease (eds Wang, G.-L. & Valent, B.) 257–266 (Springer, 2009).

  59. 59.

    Inoue, Y. et al. Evolution of the wheat blast fungus through functional losses in a host specificity determinant. Science 357, 80–83 (2017).

    ADS  CAS  PubMed  Google Scholar 

  60. 60.

    Castroagudin, V. et al. The wheat blast pathogen Pyricularia graminis-tritici has complex origins and a disease cycle spanning multiple grass hosts. Preprint at https://www.biorxiv.org/content/10.1101/203455v1 (2017).

  61. 61.

    Mottaleb, K. A. et al. Threat of wheat blast to South Asia’s food security: an ex-ante analysis. PLoS One 13, e0197555 (2018).

    PubMed  PubMed Central  Google Scholar 

  62. 62.

    Brasier, C. M. & Kirk, S. A. Rapid emergence of hybrids between the two subspecies of Ophiostoma novo-ulmi with a high level of pathogenic fitness. Plant Pathol. 59, 186–199 (2010).

    CAS  Google Scholar 

  63. 63.

    Chavez, V. A., Parnell, S. & van den Bosch, F. V. D. Designing strategies for epidemic control in a tree nursery: the case of ash dieback in the UK. Forests 6, 4135–4145 (2015).

    Google Scholar 

  64. 64.

    Heuch, J. What lessons need to be learnt from the outbreak of ash dieback disease, Chalara fraxinea in the United Kingdom? Arboricult. J. 36, 32–44 (2014).

    Google Scholar 

  65. 65.

    Living Ash Project Survey (Living Ash Project); https://livingashproject.org.uk/survey

  66. 66.

    Skovsgaard, J. P. et al. Silvicultural strategies for Fraxinus excelsior in response to dieback caused by Hymenoscyphus fraxineus. For. Intl J. For. Res. 90, 455–472 (2017).

  67. 67.

    Managing Ash Dieback Case Studies (Royal Forestry Society, Forestry Commission, 2019).

  68. 68.

    Kamoun, S., Talbot, N. J. & Islam, M. T. Plant health emergencies demand open science: tackling a cereal killer on the run. PLoS Biol. 17, e3000302 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  69. 69.

    Raffaele, S. & Kamoun, S. Genome evolution in filamentous plant pathogens: why bigger can be better. Nat. Rev. Microbiol. 10, 417–430 (2012).

    CAS  PubMed  Google Scholar 

  70. 70.

    Guo, H., Li, C. P., Shi, T., Fan, C. J. & Huang, G. X. First report of Phytophthora palmivora causing root rot of cassava in China. Plant Dis. 96, 1072–1072 (2012).

    CAS  PubMed  Google Scholar 

  71. 71.

    Lebot, V. Tropical Root and Tuber Crops: Cassava, Sweet Potato, Yams and Aroids Vol. 17 (CABI, 2009).

  72. 72.

    Reddy, P. P. Plant Protection in Tropical Root and Tuber Crops (Springer, 2015).

  73. 73.

    Álvarez, E., Llano, G. & Mejía, J. F. Cassava Diseases (CIAT, 2012).

  74. 74.

    Johnson, I. & Palaniswami, A. Phytophthora tuber rot of cassava - a new record in India. J. Mycol. Plant Pathol. 29, 323–332 (1999).

    Google Scholar 

  75. 75.

    Maizatul-Suriza, M., Dickinson, M. & Idris, A. S. Molecular characterization of Phytophthora palmivora responsible for bud rot disease of oil palm in Colombia. World. J. Microbiol. Biotech. 35, 44 (2019).

    Google Scholar 

  76. 76.

    Torres, G. A., Sarria, G. A., Martinez, G., Varon, F., Drenth, A. & Guest, D. I. Bud rot caused by Phytophthora palmivora: a destructive emerging disease of oil palm. Phytopathol 106, 320–329 (2016).

    CAS  Google Scholar 

  77. 77.

    Kaur, S., Dhillon, G. S., Brar, S. K., Vallad, G. E., Chand, R. & Chauhan, V. B. Emerging phytopathogen Macrophomina phaseolina: biology, economic importance and current diagnostic trends. Crit. Rev. Microbiol. 38, 136–151 (2012).

    CAS  PubMed  Google Scholar 

  78. 78.

    Msikita, W., James, B., Wilkinson, H. T. & Juba, J. H. First report of Macrophomina phaseolina causing pre-harvest cassava root rot in Benin and Nigeria. Plant Dis. 82, 1402–1402 (1998).

    CAS  PubMed  Google Scholar 

  79. 79.

    de Queiroz Brito, A. C. et al. First report of Macrophomina pseudophaseolina causing stem dry rot in cassava in Brazil. J. Plant Pathol. 1, 1 (2019).

  80. 80.

    Ploetz, R. C. Fusarium wilt of banana. Phytopathol 105, 1512–1521 (2015).

    Google Scholar 

  81. 81.

    Tropical Race 4: Distribution (Promusa); http://www.promusa.org/tiki-index.php?page=Tropical%20race%204%20-%20TR4#Distribution

  82. 82.

    Buddenhagen, I. Understanding strain diversity in Fusarium oxysporum f. sp. cubense and history of introduction of ‘Tropical Race 4’ to better manage banana production. Acta Horticult 828, 193–204 (2009).

    Google Scholar 

  83. 83.

    Davis, R. I., Moore, N. Y., Bentley, S., Gunua, T. G. & Rahamma, S. Further records of Fusarium oxysporum f. sp. cubense from New Guinea. Austral. Plant Pathol. 29, 224 (2000).

    Google Scholar 

  84. 84.

    Qi, Y. X., Zhang, X., Pu, J. J., Xie, Y. X., Zhang, H. Q. & Huang, S. L. Race 4 identification of Fusarium oxysporum f. sp. cubense from Cavendish cultivars in Hainan province, China. Austral. Plant Dis. 3, 46–47 (2008).

    Google Scholar 

  85. 85.

    Ploetz, R. et al. Tropical race 4 of Panama disease in the Middle East. Phytoparasitica 43, 283–293 (2015).

    Google Scholar 

  86. 86.

    Syed, R. N. et al. First report of panama wilt disease of banana caused by Fusarium oxysporum f. sp. cubense in Pakistan. J. Plant Pathol. 1, 213 (2015).

    Google Scholar 

  87. 87.

    Zheng, S. J., García-Bastidas, F. A., Li, X., Zeng, L. & Bai, T. New geographical insights of the latest expansion of Fusarium oxysporum f.sp. cubense tropical race 4 into the Greater Mekong subregion. Front. Plant Sci. 9, 457 (2018).

    PubMed  PubMed Central  Google Scholar 

  88. 88.

    O’Neill, W. T. et al. Detection of Fusarium oxysporum f. sp. cubense tropical race 4 strain in northern Queensland. Austral. Plant Dis. 11, 33 (2016).

    Google Scholar 

  89. 89.

    Maymon, M. et al. First report of Fusarium oxysporum f. sp. cubense tropical race 4 causing Fusarium wilt of Cavendish bananas in Israel. Plant Dis. 59, 348 (2018).

    Google Scholar 

  90. 90.

    Damodaran, T. et al. First report of Fusarium wilt in banana caused by Fusarium oxysporum f. sp. cubense tropical race 4 in India. Plant Dis. 103, 367 (2018).

    Google Scholar 

  91. 91.

    Coleman, J. J., Wasmann, C. C., Usami, T., White, G. J. & Temporini, E. D. Characterization of the gene encoding Pisatin Demethylase (FoPDA 1) in Fusarium oxysporum. Mol. Plant Microbe Interact. 24, 1482–1491 (2011).

    CAS  PubMed  Google Scholar 

  92. 92.

    Wylder, B., Biddle, M., King, K., Baden, R. & Webber, J. Evidence from mortality dating of Fraxinus excelsior indicates ash dieback (Hymenoscyphus fraxineus) was active in England in 2004–2005. For. Int. J. For. Res 91, 434–443 (2018).

    Google Scholar 

  93. 93.

    Bebber, D. P., Field, E., Gui, H., Mortimer, P., Holmes, T. & Gurr, S. J. Many unreported crop pests and pathogens are probably already present. Glob. Change Biol. 25, 2703–2713 (2019).

    ADS  Google Scholar 

  94. 94.

    Islam, M. T., Kim, K. H. & Choi, J. Wheat blast in Bangladesh: the current situation and future impacts. Plant Pathol. J. 35, 1 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  95. 95.

    Lowder, S. K., Skoet, J. & Raney, T. The number, size, and distribution of farms, smallholder farms, and family farms worldwide. World Dev. 87, 16–29 (2016).

    Google Scholar 

  96. 96.

    Ricciardi, V., Ramankutty, N., Mehrabi, Z., Jarvis, L. & Chookolingo, B. How much of the world’s food do smallholders produce? Global Food Secur. 17, 64–72 (2018).

    Google Scholar 

  97. 97.

    Khoury, C. K. et al. Increasing homogeneity in global food supplies and the implications for food security. Proc. Natl Acad. Sci. USA 111, 4001–4006 (2014).

    ADS  CAS  PubMed  Google Scholar 

  98. 98.

    Bentham, J. et al. Multidimensional characterization of global food supply from 1961 to 2013. Nat. Food 1, 70–75 (2020).

  99. 99.

    Schneider, R. W. et al. First report of soybean rust caused by Phakopsora pachyrhizi in the continental United States. Plant Dis. 89, 774–774 (2005).

    CAS  PubMed  Google Scholar 

  100. 100.

    Slaminko, T. L., Miles, M. R., Frederick, R. D., Bonde, M. R. & Hartman, G. L. New legume hosts of Phakopsora pachyrhizi based on greenhouse evaluations. Plant Dis. 92, 767–771 (2008).

    CAS  PubMed  Google Scholar 

  101. 101.

    Del Cid, C., Krugner, R., Zeilinger, A. R., Daugherty, M. P. & Almeida, R. P. Plant water stress and vector feeding preference mediate transmission efficiency of a plant pathogen. Environ. Entomol 47, 1471–1478 (2018).

    PubMed  Google Scholar 

  102. 102.

    Agrios, G. N. Plant Pathology (Academic Press, 2005).

  103. 103.

    Scholthof, K. B. G. The disease triangle: pathogens, the environment and society. Nat. Rev. Microbiol. 5, 152–156 (2007).

    CAS  PubMed  Google Scholar 

  104. 104.

    Chaloner, T. M., Fones, H. N., Varma, V., Bebber, D. P. & Gurr, S. J. A new mechanistic model of weather-dependent Septoria tritici blotch disease risk. Phil. Trans. Roy. Soc. B 374, 20180266 (2019).

    Google Scholar 

  105. 105.

    Zhernakova, A. et al. Population-based metagenomics analysis reveals markers for gut microbiome composition and diversity. Science 352, 565–569 (2016).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  106. 106.

    Holmes, E. C., Dudas, G., Rambaut, A. & Andersen, K. G. The evolution of Ebola virus: unsights from the 2013–2016 epidemic. Nature 538, 193–200 (2016).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  107. 107.

    Chaloner, T. M., Gurr, S. J. & Bebber, D. P. Geometry and evolution of the ecological niche in plant-associated microbes. Nat. Commun. (in the press).

  108. 108.

    Shaw, M. Effects of temperature, leaf wetness and cultivar on the latent period of Mycosphaerella graminicola on winter wheat. Plant Pathol. 39, 255–268 (1990).

    Google Scholar 

  109. 109.

    Bernard, F. The Development of a Foliar Fungal Pathogen Does React to Temperature, but to which Temperature? PhD thesis, AgroParisTech (2012).

  110. 110.

    Bernard, Frédéric, Sache, I., Suffert, F. & Chelle, M. The development of a foliar fungal pathogen does react to leaf temperature! New Phytol. 198, 232–240 (2013).

    PubMed  Google Scholar 

  111. 111.

    Boixel, A. L., Delestre, G., Legeay, J., Chelle, M. & Suffert, F. Phenotyping thermal responses of yeasts and yeast-like microorganisms at the individual and population levels: proof-of-concept, development and application of an experimental framework to a plant pathogen. Microbial Ecol. 78, 42–56 (2019).

    Google Scholar 

  112. 112.

    Schlenker, W. & Roberts, M. J. Nonlinear temperature effects indicate severe damages to US crop yields under climate change. Proc. Natl Acad. Sci. USA 106, 15594–15598 (2009).

    ADS  CAS  PubMed  Google Scholar 

  113. 113.

    Bebber, D. P., Castillo, Á. D. & Gurr, S. J. Modelling coffee leaf rust risk in Colombia with climate reanalysis data. Phil. Trans. R. Soc. B 371, 20150458 (2016).

    PubMed  Google Scholar 

  114. 114.

    Lewis, C. M. et al. Potential for re-emergence of wheat stem rust in the United Kingdom. Comm. Biol. 1, 13 (2018).

    Google Scholar 

  115. 115.

    Croll, D. & McDonald, B. A. The genetic basis of local adaptation for pathogenic fungi in agricultural ecosystems. Molec. Ecol. 26, 2027–2040 (2017).

    CAS  Google Scholar 

  116. 116.

    Lovell, D. J., Hunter, T., Powers, S. J., Parker, S. R. & van den Bosch, F. Effect of temperature on latent period of septoria leaf blotch on winter wheat under outdoor conditions. Plant Pathol. 53, 170–181 (2004).

    Google Scholar 

  117. 117.

    Suffert, F. & Thompson, R. N. Some reasons why the latent period should not always be considered constant over the course of a plant disease epidemic. Plant Pathol. 67, 1831–1840 (2018).

    Google Scholar 

  118. 118.

    Möller, M., Habig, M., Freitag, M. & Stukenbrock, E. H. Extraordinary genome instability and widespread chromosome rearrangements during vegetative growth. Genetics 210, 517–529 (2018).

    PubMed  PubMed Central  Google Scholar 

  119. 119.

    IPCC Climate Change 2014: Synthesis Report (eds Core Writing Team, Pachauri, R. K. & Meyer L. A.) (IPCC, 2014).

  120. 120.

    Bayles, R., Flath, K., Hovmøller, M. & de Vallavieille-Pope, C. Breakdown of the Yr17 resistance to yellow rust of wheat in northern Europe. Agronomie. 20, 805–811 (2000).

    Google Scholar 

  121. 121.

    He, D. C., Zhan, J. S. & Xie, L. H. Problems, challenges and future of plant disease management: from an ecological point of view. J. Integrat. Agricult. 15, 705–715 (2016).

    Google Scholar 

  122. 122.

    Lee, H. A. et al. Current understandings of plant nonhost resistance. Molec. Plant Microbe Interact. 30, 5–15 (2017).

  123. 123.

    Jones, J. D. & Dangl, J. L. The plant immune system. Nature 444, 323 (2006).

    ADS  CAS  Google Scholar 

  124. 124.

    Gurr, S. J. & Rushton, P. J. Compatibility and disease and incompatibility and defence in plant–pathogen interactions. Trends Biotechnol. 6, 275–282 (2005).

    Google Scholar 

  125. 125.

    McDowell, J. M. & Woffenden, B. J. Plant disease resistance genes: recent insights and potential applications. Trends Biotechnol. 21, 178–183 (2003).

    CAS  PubMed  Google Scholar 

  126. 126.

    Ashkani, S. et al. Molecular breeding strategy and challenges towards improvement of blast disease resistance in rice crop. Front. Plant Sci. 6, 886 (2015).

    PubMed  PubMed Central  Google Scholar 

  127. 127.

    Brown, J. K. Durable resistance of crops to disease: a Darwinian perspective. Ann. Rev. Phytopathol 53, 513–539 (2015).

    CAS  Google Scholar 

  128. 128.

    Fuchs, M. Pyramiding resistance-conferring gene sequences in crops. Curr. Op. Virol. 26, 36–42 (2017).

  129. 129.

    Singh, R. P. et al. The emergence of Ug99 races of the stem rust fungus is a threat to world wheat production. Annu. Rev. Phytopathol. 49, 465–481 (2011).

    CAS  PubMed  Google Scholar 

  130. 130.

    Singh, R. P., Huerta-Espino, J. & William, H. M. Genetics and breeding for durable resistance to leaf and stripe rusts in wheat. Turk. J. Agric. Forest. 29, 121–127 (2005).

    CAS  Google Scholar 

  131. 131.

    Rehman, M. U. et al. Adult plant resistance to stem rust (Puccinia graminis f. sp. tritici) in Pakistani advanced lines and wheat varieties. Austral. J. Crop Sci 12, 1633–1639 (2018).

    CAS  Google Scholar 

  132. 132.

    Garrett, K. A. et al. Resistance genes in global crop breeding networks. Phytopathol. 107, 1268–1278 (2017).

    CAS  Google Scholar 

  133. 133.

    Byerlee, D. & Dubin, H. J. Crop improvement in the CGIAR as a global success story of open access and international collaboration. Internat. J. Comm 4, 452–480 (2009).

    Google Scholar 

  134. 134.

    Global Fungicides Market Research Report (Globe Newswire, 2018).

  135. 135.

    Oliver, R. P. & Hewitt, H. G. Fungicides in Crop Protection (CABI, 2014).

  136. 136.

    Fisher, M. C., Hawkins, N. J., Sanglard, D. & Gurr, S. J. Worldwide emergence of resistance to antifungal drugs challenges human health and food security. Science 360, 739–742 (2018).

    CAS  PubMed  Google Scholar 

  137. 137.

    Steinberg, G. et al. A lipophilic cation protects crops against fungal pathogens by multiple modes of action. Nat. Commun. 11, 1608 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  138. 138.

    McDougall, P. Evolution of the Crop Protection Industry Since 1960 (Informa, 2019).

  139. 139.

    Bosch, F. V. D., Oliver, R., van den Berg, F. & Paveley, N. Governing principles can guide fungicide-resistance management tactics. Ann. Rev. Phytopathol. 52, 175–195 (2018).

  140. 140.

    Elderfield, J. A., Lopez-Ruiz, F. J., van den Bosch, F. & Cunniffe, N. J. Using epidemiological principles to explain fungicide resistance management tactics: Why do mixtures outperform alternations? Phytopathol. 108, 803–817 (2018).

    CAS  Google Scholar 

  141. 141.

    EU votes to withdraw chlorothalonil. AgriTradeNews (29 March 2019).

Download references

Acknowledgements

S.J.G. is a CIFAR Fellow in the Fungal Kingdom: Opportunities and Threats programme. This work was funded in part by GFS/BBSRC grant no. BB/N020847/1 (awarded to D.B., S.G. and G.S.) and BBSRC grant no. BB/PO18335 (awarded to G.S. and S.G.) and BBSRC doctoral studentship BB/M009122/1 to T.C.

Author information

Affiliations

Authors

Contributions

H.F. wrote the paper with S.G. H.F. made Figs. 1, 3 and 4 and Tables 1 and 2; G.S. made Fig. 2. D.B. carried out data analyses. W.K., T.C., D.B. and G.S. contributed to the writing of the paper. All authors proofread and approved the submitted work.

Corresponding authors

Correspondence to Helen N. Fones or Sarah J. Gurr.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Fones, H.N., Bebber, D.P., Chaloner, T.M. et al. Threats to global food security from emerging fungal and oomycete crop pathogens. Nat Food 1, 332–342 (2020). https://doi.org/10.1038/s43016-020-0075-0

Download citation

Further reading