1932

Abstract

Innovations in aerobiological and epidemiological modeling are enabling the development of powerful techniques to infer connectivity networks for transboundary pathogens in ways that were not previously possible. The innovations are supported by improved access to historical and near real-time highly resolved weather data, multi-country disease surveillance data, and enhanced computing power. Using wheat rusts as an exemplar, we introduce a flexible modeling framework to identify characteristic pathways for long-distance spore dispersal within countries and beyond national borders. We show how the models are used for near real-time early warning systems to support smallholder farmers in East Africa and South Asia. Wheat rust pathogens are ideal exemplars because they continue to pose threats to food security, especially in regions of the world where resources for control are limited. The risks are exacerbated by the rapid appearance and spread of new pathogenic strains, prodigious spore production, and long-distance dispersal for transboundary and pandemic spread.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-phyto-121423-041956
2024-09-09
2024-12-11
Loading full text...

Full text loading...

/deliver/fulltext/phyto/62/1/annurev-phyto-121423-041956.html?itemId=/content/journals/10.1146/annurev-phyto-121423-041956&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Ali S, Gladieux P, Leconte M, Gautier A, Justesen AF, et al. 2014.. Origin, migration routes and worldwide population genetic structure of the wheat yellow rust pathogen Puccinia striiformis f. sp. tritici. . PLOS Pathog. 10:(1):e1003903
    [Crossref] [Google Scholar]
  2. 2.
    Allen-Sader C, Thurston W, Meyer M, Nure E, Bacha N, et al. 2019.. An early warning system to predict and mitigate wheat rust diseases in Ethiopia. . Environ. Res. Lett. 14:(11):115004 2. Details components for early warning system for stem and stripe rust.
    [Crossref] [Google Scholar]
  3. 3.
    Aylor DE. 1986.. A framework for examining inter-regional aerial transport of fungal spores. . Agric. For. Meteorol. 38:(4):26388
    [Crossref] [Google Scholar]
  4. 4.
    Aylor DE. 1987.. Deposition gradients of urediniospores of Puccinia recondita near a source. . Phytopathology 77:(10):144248
    [Crossref] [Google Scholar]
  5. 5.
    Aylor DE. 1990.. The role of intermittent wind in the dispersal of fungal pathogens. . Annu. Rev. Phytopathol. 28::7392
    [Crossref] [Google Scholar]
  6. 6.
    Aylor DE. 2003.. Spread of plant disease on a continental scale: role of aerial dispersal of pathogens. . Ecology 84:(8):198997 6. Integrates long distance dispersal of pathogens with green wave of crop growth to model continental spread.
    [Crossref] [Google Scholar]
  7. 7.
    Aylor DE. 2017.. Aerial Dispersal of Pollen and Spores. St. Paul, MN:: APS Press
    [Google Scholar]
  8. 8.
    Bauer P, Thorpe A, Brunet G. 2015.. The quiet revolution of numerical weather prediction. . Nature 525:(7567):4755
    [Crossref] [Google Scholar]
  9. 9.
    Beddow JM, Hurley TM, Kriticos DJ, Pardey PG. 2013.. Measuring the Global Occurrence and Probabilistic Consequences of Wheat Stem Rust. St. Paul, MN:: HarvestChoice
    [Google Scholar]
  10. 10.
    Beddow JM, Pardey PG, Chai Y, Hurley TM, Kriticos DJ, et al. 2015.. Research investment implications of shifts in the global geography of wheat stripe rust. . Nat. Plants 1:(10):15132
    [Crossref] [Google Scholar]
  11. 11.
    Bentley AR, Donovan J, Sonder K, Baudron F, Lewis JM, et al. 2022.. Near- to long-term measures to stabilize global wheat supplies and food security. . Nat. Food 3:(7):48386
    [Crossref] [Google Scholar]
  12. 12.
    Bhavani S, Singh RP, Hodson DP, Huerta-Espino J, Randhawa MS. 2022.. Wheat rusts: current status, prospects of genetic control and integrated approaches to enhance resistance durability. . In Wheat Improvement: Food Security in a Changing Climate, ed. MP Reynolds, H-J Braun , pp. 12541. Cham, Switz:.: Springer
    [Google Scholar]
  13. 13.
    Blasch G, Alemayehu Y, Rodrigues F. 2023.. The potential of UAV and very high-resolution satellite imagery for yellow and stem rust detection and phenotyping in Ethiopia. . Sci. Rep. 13::16768
    [Crossref] [Google Scholar]
  14. 14.
    Bradshaw CD, Thurston W, Hodson D, Mona T, Smith JW, et al. 2022.. Irrigation can create new green bridges that promote rapid intercontinental spread of the wheat stem rust pathogen. . Environ. Res. Lett. 17:(11):114025 14. Shows how irrigation can provide green bridges for spread of rust into and out of East Africa.
    [Crossref] [Google Scholar]
  15. 15.
    Brodsky H, Calderón R, Hamilton DS, Li L, Miles A, et al. 2023.. Assessing long-distance atmospheric transport of soilborne plant pathogens. . Environ. Res. Lett. 18:(10):104021
    [Crossref] [Google Scholar]
  16. 16.
    Brown JKM, Hovmøller MS. 2002.. Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. . Science 297:(5581):53741 16. Comprehensive review of long-distance dispersal of plant pathogens.
    [Crossref] [Google Scholar]
  17. 17.
    Burgin LE, Gloster J, Sanders C, Mellor PS, Gubbins S, Carpenter S. 2013.. Investigating incursions of bluetongue virus using a model of long-distance Culicoides biting midge dispersal. . Transbound. Emerg. Dis. 60:(3):26372
    [Crossref] [Google Scholar]
  18. 18.
    Bushnell WR, Roelfs AP, eds. 1985.. The Cereal Rusts, Vol. II. Diseases, Distribution, Epidemiology, and Control. Orlando, FL:: Academic
    [Google Scholar]
  19. 19.
    Conway G. 2012.. One Billion Hungry: Can We Feed the World? New York:: Cornell Univ. Press
    [Google Scholar]
  20. 20.
    Cressman K. 2001.. Desert locust guidelines: 2. Survey. Rep. , FAO, Rome:. https://www.fao.org/ag/locusts/common/ecg/347_en_DLG2e.pdf
    [Google Scholar]
  21. 21.
    Cressman K. 2016.. Desert locust. . In Biological and Environmental Hazards, Risks, and Disasters, ed. JF Shroder, R Sivanpillai , pp. 87105. Boston:: Academic
    [Google Scholar]
  22. 22.
    de Vallavieille-Pope C, Huber L, Leconte M, Bethenod O. 2002.. Preinoculation effects of light quantity on infection efficiency of Puccinia striiformis and P. triticina on wheat seedlings. . Phytopathology 92:(12):130814
    [Crossref] [Google Scholar]
  23. 23.
    de Vallavieille-Pope Huber L, Leconte M, Goyeau H. 1995.. Comparative effects of temperature and interrupted wet periods on germination, penetration, and infection of Puccinia recondita f. sp. tritici and P. striiformis on wheat seedlings. . Phytopathology 85:(4):40915
    [Crossref] [Google Scholar]
  24. 24.
    De Wolf ED, Isard SA. 2007.. Disease cycle approach to plant disease prediction. . Annu. Rev. Phytopathol. 45::20320
    [Crossref] [Google Scholar]
  25. 25.
    Dillon Weston WAR. 1929.. Observations on the bacterial and fungus flora of the upper air. . Trans. Br. Mycol. Soc. 14:(1–2):11117
    [Crossref] [Google Scholar]
  26. 26.
    Draxler R, Arnold D, Chino M, Galmarini S, Hort M, et al. 2015.. World Meteorological Organization's model simulations of the radionuclide dispersion and deposition from the Fukushima Daiichi nuclear power plant accident. . J. Environ. Radioact. 139::17284
    [Crossref] [Google Scholar]
  27. 27.
    Draxler R, Stunder B, Rolph G, Stein A, Taylor A, et al. 2022.. HYSPLIT user's guide. NOAA Air Resourc. Lab. , College Park, MD:. https://www.arl.noaa.gov/documents/reports/hysplit_user_guide.pdf
    [Google Scholar]
  28. 28.
    Dubin HJ, Brennan JP. 2009.. Combating stem and leaf rust of wheat: historical perspective, impacts, and lessons learned. IFPRI Discuss. Pap. , Washington, DC:. https://ebrary.ifpri.org/utils/getfile/collection/p15738coll2/id/17034/filename/17035.pdf
    [Google Scholar]
  29. 29.
    Dybiec B, Kleczkowski A, Gilligan CA. 2004.. Controlling disease spread on networks with incomplete knowledge. . Phys. Rev. E 70:(6):066145
    [Crossref] [Google Scholar]
  30. 30.
    Dybiec B, Kleczkowski A, Gilligan CA. 2009.. Modelling control of epidemics spreading by long-range interactions. . J. R. Soc. Interface 6:(39):94150
    [Crossref] [Google Scholar]
  31. 31.
    FAO. 2022.. Agricultural production statistics 2000–2021. FAOSTAT Anal. Brief Ser. 60 , FAO, Rome:. https://www.fao.org/3/cc3751en/cc3751en.pdf
    [Google Scholar]
  32. 32.
    FAO. 2023.. The State of Food Security and Nutrition in the World 2023: Urbanization, Agrifood Systems Transformation and Healthy Diets Across the Rural-Urban Continuum. Rome:: FAO
    [Google Scholar]
  33. 33.
    Fernandes JMC, Nicolau M, Pavan W, Hölbig CA, Karrei M, et al. 2017.. A weather-based model for predicting early season inoculum build-up and spike infection by the wheat blast pathogen. . Trop. Plant Pathol. 42:(3):23037
    [Crossref] [Google Scholar]
  34. 34.
    Figueroa M, Hammond-Kosack KE, Solomon PS. 2018.. A review of wheat diseases: a field perspective. . Mol. Plant Pathol. 19:(6):152336
    [Crossref] [Google Scholar]
  35. 35.
    Garrett KA, Alcalá-Briseño RI, Andersen KF, Buddenhagen CE, Choudhury RA, et al. 2018.. Network analysis: a systems framework to address grand challenges in plant pathology. . Annu. Rev. Phytopathol. 56::55980
    [Crossref] [Google Scholar]
  36. 36.
    Gilligan CA. 2008.. Sustainable agriculture and plant diseases: an epidemiological perspective. . Philos. Trans. R. Soc. Lond. B 363:(1492):74159
    [Crossref] [Google Scholar]
  37. 37.
    Gilligan CA, van den Bosch F. 2008.. Epidemiological models for invasion and persistence of pathogens. . Annu. Rev. Phytopathol. 46::385418
    [Crossref] [Google Scholar]
  38. 38.
    Gregory PH. 1945.. The dispersion of air-borne spores. . Trans. Br. Mycol. Soc. 28:(1–2):2672
    [Crossref] [Google Scholar]
  39. 39.
    Gregory PH. 1973.. The Microbiology of the Atmosphere. London:: Leonard Hill Books. , 2nd ed..
    [Google Scholar]
  40. 40.
    Hei NB, Tsegaab T, Getaneh W, Girma T, Obsa C, et al. 2020.. First report of Puccinia graminis f. sp. tritici race TTKTT in Ethiopia. . Plant Dis. 104:(3):982
    [Crossref] [Google Scholar]
  41. 41.
    Hirst JM, Stedman OJ, Hurst GW. 1967.. Long-distance spore transport: vertical sections of spore clouds over the sea. . Microbiology 48:(3):35777
    [Google Scholar]
  42. 42.
    Hodson DP. 2011.. Shifting boundaries: challenges for rust monitoring. . Euphytica 179:(1):93104
    [Crossref] [Google Scholar]
  43. 43.
    Hodson DP, Cressman K, Nazari K, Park RF, Yahyaoui A. 2009.. The global cereal rust monitoring system. . In Proceedings of Oral Papers and Posters 2009 Technical Workshop, BGRI, . 3546. Veracruz, Mex.:: CIMMYT
    [Google Scholar]
  44. 44.
    Int. Food Policy Res. Inst. 2019.. Global spatially-disaggregated crop production statistics data for 2010 version 2.0. Harv. Dataverse, Cambridge, MA:. https://dataverse.harvard.edu/dataset.xhtml?persistentId=doi:10.7910/DVN/PRFF8V
    [Google Scholar]
  45. 45.
    Isard SA, Barnes CW, Hambleton S, Ariatti A, Russo JM, et al. 2011.. Predicting soybean rust incursions into the North American continental interior using crop monitoring, spore trapping, and aerobiological modeling. . Plant Dis. 95:(11):134657
    [Crossref] [Google Scholar]
  46. 46.
    Isard SA, Dufault NS, Miles MR, Hartman GL, Russo JM, et al. 2006.. The effect of solar irradiance on the mortality of Phakopsora pachyrhizi urediniospores. . Plant Dis. 90:(7):94145
    [Crossref] [Google Scholar]
  47. 47.
    Isard SA, Gage SH, Comtois P, Russo JM. 2005.. Principles of the atmospheric pathway for invasive species applied to soybean rust. . BioScience 55:(10):85161
    [Crossref] [Google Scholar]
  48. 48.
    Isard SA, Russo JM, Ariatti A. 2007.. The integrated aerobiology modeling system applied to the spread of soybean rust into the Ohio River valley during September 2006. . Aerobiologia 23:(4):27182
    [Crossref] [Google Scholar]
  49. 49.
    Jeger MJ, Pautasso M, Holdenrieder O, Shaw MW. 2007.. Modelling disease spread and control in networks: implications for plant sciences. . New Phytol. 174:(2):27997
    [Crossref] [Google Scholar]
  50. 50.
    Jones A, Thomson D, Hort M, Devenish B. 2007.. The U.K. Met Office's next-generation atmospheric dispersion model, NAME III. . In Air Pollution Modeling and its Application XVII, pp. 58089. Boston, MA:: Springer
    [Google Scholar]
  51. 51.
    Kislev ME. 1982.. Stem rust of wheat 3300 years old found in Israel. . Science 216::99394
    [Crossref] [Google Scholar]
  52. 52.
    Lin JC. 2012.. Lagrangian modeling of the atmosphere: an introduction. . In Lagrangian Modeling of the Atmosphere, ed. JC Lin, D Brunner, C Gerbig, A Stohl, A Luhar, P Webley , pp. 111. Washington, DC:: Am. Geophys. Union
    [Google Scholar]
  53. 53.
    Maddison AC, Manners JG. 1973.. Lethal effects of artificial ultraviolet radiation on cereal rust uredospores. . Trans. Br. Mycol. Soc. 60:(3):47194
    [Crossref] [Google Scholar]
  54. 54.
    Meyer M, Bacha N, Tesfaye T, Alemayehu Y, Abera E, et al. 2021.. Wheat rust epidemics damage Ethiopian wheat production: a decade of field disease surveillance reveals national-scale trends in past outbreaks. . PLOS ONE 16:(2):e0245697
    [Crossref] [Google Scholar]
  55. 55.
    Meyer M, Burgin L, Hort MC, Hodson DP, Gilligan CA. 2017.. Large-scale atmospheric dispersal simulations identify likely airborne incursion routes of wheat stem rust into Ethiopia. . Phytopathology 107:(10):117586 55. Analyzes forward and backward projections of transboundary spore dispersal. Also introduces UV death of spores.
    [Crossref] [Google Scholar]
  56. 56.
    Meyer M, Cox JA, Hitchings MDT, Burgin L, Hort MC, et al. 2017.. Quantifying airborne dispersal routes of pathogens over continents to safeguard global wheat supply. . Nat. Plants 3:(10):78086 56. Analyzes historic data to identify transboundary dispersal routes: detailed supplements on model and risk maps.
    [Crossref] [Google Scholar]
  57. 57.
    Meyer M, Thurston W, Smith JW, Schumacher A, Millington SC, et al. 2023.. Three-dimensional visualization of long-range atmospheric transport of crop pathogens and insect pests. . Atmosphere 14:(6):910
    [Crossref] [Google Scholar]
  58. 58.
    Milus EA, Kristensen K, Hovmøller MS. 2009.. Evidence for increased aggressiveness in a recent widespread strain of Puccinia striiformis f. sp. tritici causing stripe rust of wheat. . Phytopathology 99:(1):8994
    [Crossref] [Google Scholar]
  59. 59.
    Mottaleb KA. 2021.. Wheat rust early warning and advisory system in Ethiopia: impact assessment in two major wheat-growing regional states. Rep. , CIMMYT, Addis Ababa, Ethiop:. https://repository.cimmyt.org/bitstream/handle/10883/21766/64693.pdf?sequence=1&isAllowed=y
    [Google Scholar]
  60. 60.
    Nagarajan S. 2012.. Is Puccinia graminis f. sp. tritici virulence Ug99 a threat to wheat production in the North West Plain Zone of India?. Indian Phytopathol. 65:(3):21926
    [Google Scholar]
  61. 61.
    Nagarajan S, Kogel HJ, Zadoks JC. 2012.. Epidemiology of Puccinia graminis f. sp. tritici-Ug99 in the Rift Valley “flyway” from Uganda-Kenya to Yemen. . Plant Health Prog. 13:(1):31
    [Crossref] [Google Scholar]
  62. 62.
    Nagarajan S, Kogel HJ, Zadoks JC. 2013.. Influence of the Arabian Sea tropical cyclone and the western disturbance on the appearance of Puccinia graminis f. sp. tritici virulence Ug99-TTKSK in Iran in 2007. . Curr. Sci. India 105:(2):16466
    [Google Scholar]
  63. 63.
    Nagarajan S, Kogel K, Zadoks J. 2014.. Epidemiological analysis of the damage potential of Pgt-Ug99 in Central East, North East Africa; Iran and Punjab (India). . Indian Phytopathol. 67:(1):2632 63. Uses meteorological data and cropping knowledge to assess risks of transcontinental spread of rust spores.
    [Google Scholar]
  64. 64.
    Nagarajan S, Singh DV. 1990.. Long-distance dispersion of rust pathogens. . Annu. Rev. Phytopathol. 28::13953
    [Crossref] [Google Scholar]
  65. 65.
    Nagarajan S, Singh H, Joshi LM, Saari EE. 1976.. Meteorological conditions associated with long-distance dissemination and deposition of Puccinia graminis tritici uredospores in India. . Phytopathology 66::198203
    [Crossref] [Google Scholar]
  66. 66.
    Nazari K, Al-Maaroof EM, Kurtulus E, Kavaz H, Hodson D, Ozseven I. 2021.. First report of Ug99 race TTKTT of wheat stem rust (Puccinia graminis f. sp. tritici) in Iraq. . Plant Dis. 105:(9):2719
    [Crossref] [Google Scholar]
  67. 67.
    Neale RB, Gettelman A, Park S, Chen C-C, Lauritzen PH, et al. 2012.. Description of the NCAR community atmosphere model (CAM 5.0). Tech. Rep. , NCAR, Boulder, CO:. https://www2.cesm.ucar.edu/models/cesm2/atmosphere/docs/description/cam5_desc.pdf
    [Google Scholar]
  68. 68.
    Olivera P, Newcomb M, Szabo LJ, Rouse M, Johnson J, et al. 2015.. Phenotypic and genotypic characterization of race TKTTF of Puccinia graminis f. sp. tritici that caused a wheat stem rust epidemic in southern Ethiopia in 2013–14. . Phytopathology 105:(7):91728
    [Crossref] [Google Scholar]
  69. 69.
    Pardey PG, Beddow JM, Kriticos DJ, Hurley TM, Park RF, et al. 2013.. Right-sizing stem-rust research. . Science 340:(6129):14748
    [Crossref] [Google Scholar]
  70. 70.
    Park R, Fetch T, Hodson D, Jin Y, Nazari K, et al. 2011.. International surveillance of wheat rust pathogens: progress and challenges. . Euphytica 179:(1):10917
    [Crossref] [Google Scholar]
  71. 71.
    Patpour M, Hovmøller MS, Justesen AF, Newcomb M, Olivera P, et al. 2016.. Emergence of virulence to SrTmp in the Ug99 race group of wheat stem rust, Puccinia graminis f. sp. tritici, in Africa. . Plant Dis. 100:(2):522
    [Crossref] [Google Scholar]
  72. 72.
    Prank M, Kenaley SC, Bergstrom GC, Acevedo M, Mahowald NM. 2019.. Climate change impacts the spread potential of wheat stem rust, a significant crop disease. . Environ. Res. Lett. 14:(12):124053
    [Crossref] [Google Scholar]
  73. 73.
    Pretorius ZA, Singh RP, Wagoire WW, Payne TS. 2000.. Detection of virulence to wheat stem rust resistance gene Sr31 in Puccinia graminis f. sp. tritici in Uganda. . Plant Dis. 84:(2):203
    [Crossref] [Google Scholar]
  74. 74.
    Pretorius ZA, Visser B, Terefe T, Herselman L, Prins R, et al. 2015.. Races of Puccinia triticina detected on wheat in Zimbabwe, Zambia and Malawi and regional germplasm responses. . Australas. Plant Pathol. 44:(2):21724
    [Crossref] [Google Scholar]
  75. 75.
    Radhakrishnan GV, Cook NM, Bueno-Sancho V, Lewis CM, Persoons A, et al. 2019.. MARPLE, a point-of-care, strain-level disease diagnostics and surveillance tool for complex fungal pathogens. . BMC Biol. 17:(1):65
    [Crossref] [Google Scholar]
  76. 76.
    Radici A, Martinetti D, Bevacqua D. 2022.. Early-detection surveillance for stem rust of wheat: insights from a global epidemic network based on airborne connectivity and host phenology. . Environ. Res. Lett. 17:(6):064045
    [Crossref] [Google Scholar]
  77. 77.
    Radici A, Martinetti D, Bevacqua D. 2023.. Global benefits and domestic costs of a cooperative surveillance strategy to control transboundary crop pathogens. . Plants People Planet 5::92332
    [Crossref] [Google Scholar]
  78. 78.
    Rautenhaus M, Kern M, Schäfler A, Westermann R. 2015.. Three-dimensional visualization of ensemble weather forecasts—Part 1: the visualization tool Met.3D (version 1.0). . Geosci. Model Dev. 8:(7):232953
    [Crossref] [Google Scholar]
  79. 79.
    Retkute R, Thurston W, Cressman K, Gilligan CA. 2023.. A framework for modelling desert locust population dynamics and large-scale dispersal. . bioRxiv 548524. https://doi.org/10.1101/2023.07.11.548524
  80. 80.
    Richard H, Martinetti D, Lercier D, Fouillat Y, Hadi B, et al. 2023.. Computing geographical networks generated by air-mass movement. . GeoHealth 7:(10):e2023GH000885
    [Crossref] [Google Scholar]
  81. 81.
    Roelfs AP. 1985.. Epidemiology in North America. . In The Cereal Rusts, Vol. II. Diseases, Distribution, Epidemiology, and Control, ed. WR Bushnell, AP Roelfs , pp. 40334. Orlando, FL:: Academic
    [Google Scholar]
  82. 82.
    Roelfs AP, Martell LB. 1984.. Uredospore dispersal from a point source within a wheat canopy. . Phytopathology 74::126267
    [Crossref] [Google Scholar]
  83. 83.
    Roelfs AP, Martens JW. 1988.. An international system of nomenclature for Puccinia graminis f. sp. tritici. . Phytopathology 78::52633
    [Crossref] [Google Scholar]
  84. 84.
    Roelfs AP, Singh RP, Saari EE. 1992.. Rust diseases of wheat: concepts and methods of disease management. Rep. , CIMMYT, Veracruz, Mex:. 84. Detailed account of epidemiology and control of wheat rusts with continuing relevance to current challenges.
    [Google Scholar]
  85. 85.
    Rosvall M, Bergstrom CT. 2008.. Maps of random walks on complex networks reveal community structure. . PNAS 105:(4):111823
    [Crossref] [Google Scholar]
  86. 86.
    Rowell JB, Roelfs AP. 1971.. Evidence for an unrecognized source of overwintering wheat stem rust in the United States. . Plant Dis. 66::2057
    [Google Scholar]
  87. 87.
    Savary S, Willocquet L, Pethybridge SJ, Esker P, McRoberts N, Nelson A. 2019.. The global burden of pathogens and pests on major food crops. . Nat. Ecol. Evol. 3:(3):43039
    [Crossref] [Google Scholar]
  88. 88.
    Schmale DG, Ross SD. 2015.. Highways in the sky: scales of atmospheric transport of plant pathogens. . Annu. Rev. Phytopathol. 53::591611
    [Crossref] [Google Scholar]
  89. 89.
    Shaw MW, Pautasso M. 2014.. Networks and plant disease management: concepts and applications. . Annu. Rev. Phytopathol. 52::47793
    [Crossref] [Google Scholar]
  90. 90.
    Singh PK, Gahtyari NC, Roy C, Roy KK, He X, et al. 2021.. Wheat blast: a disease spreading by intercontinental jumps and its management strategies. . Front. Plant Sci. 12::1467
    [Google Scholar]
  91. 91.
    Singh RP, Hodson DP, Huerta-Espino J, Jin Y, Bhavani S, et al. 2011.. The emergence of Ug99 races of the stem rust fungus is a threat to world wheat production. . Annu. Rev. Phytopathol. 49::46581
    [Crossref] [Google Scholar]
  92. 92.
    Singh RP, Hodson DP, Huerta-Espino J, Jin Y, Njau P, et al. 2008.. Will stem rust destroy the world's wheat crop?. Adv. Agron. 98:(8):271309 92. Historically important review of potential impact of the stem rust variant Ug99 on food security.
    [Crossref] [Google Scholar]
  93. 93.
    Singh RP, Hodson DP, Jin Y, Huerta-Espino J, Kinyua MG, et al. 2007.. Current status, likely migration and strategies to mitigate the threat to wheat production from race Ug99 (TTKS) of stem rust pathogen. . CABI Rev. https://doi.org/10.1079/PAVSNNR20061054
    [Google Scholar]
  94. 94.
    Singh RP, Hodson DP, Jin Y, Lagudah ES, Ayliffe MA, et al. 2015.. Emergence and spread of new races of wheat stem rust fungus: continued threat to food security and prospects of genetic control. . Phytopathology 105:(7):87284
    [Crossref] [Google Scholar]
  95. 95.
    Stakman EC. 1934.. Epidemiology of cereal rusts. . In Proceedings of the 5th Pacific Science Congress, pp. 317784. Toronto:: Univ. Toronto Press
    [Google Scholar]
  96. 96.
    Stein AF, Draxler RR, Rolph GD, Stunder BJB, Cohen MD, Ngan F. 2015.. NOAA's HYSPLIT atmospheric transport and dispersion modeling system. . Bull. Am. Meteorol. Soc. 96:(12):205977
    [Crossref] [Google Scholar]
  97. 97.
    Stohl A, Eckhardt S, Forster C, James P, Spichtinger N, Seibert P. 2002.. A replacement for simple back trajectory calculations in the interpretation of atmospheric trace substance measurements. . Atmos. Environ. 36:(29):463548
    [Crossref] [Google Scholar]
  98. 98.
    Tembo B, Mulenga RM, Sichilima S, M'siska KK, Mwale M, et al. 2020.. Detection and characterization of fungus (Magnaporthe oryzae pathotype Triticum) causing wheat blast disease on rain-fed grown wheat (Triticum aestivum L.) in Zambia. . PLOS ONE 15:(9):e0238724
    [Crossref] [Google Scholar]
  99. 99.
    Terefe TG, Visser B, Pretorius ZA. 2016.. Variation in Puccinia graminis f. sp. tritici detected on wheat and triticale in South Africa from 2009 to 2013. . Crop Prot. 86::916
    [Crossref] [Google Scholar]
  100. 100.
    Visser B, Meyer M, Park RF, Gilligan CA, Burgin LE, et al. 2019.. Microsatellite analysis and urediniospore dispersal simulations support the movement of Puccinia graminis f. sp. tritici from southern Africa to Australia. . Phytopathology 109:(1):13344 100. Genetic analysis and atmospheric dispersion modeling infer stem rust dispersion from Africa to Australia.
    [Crossref] [Google Scholar]
  101. 101.
    Walters D, Boutle I, Brooks M, Melvin T, Stratton R, et al. 2017.. The Met Office Unified Model Global Atmosphere 6.0/6.1 and JULES Global Land 6.0/6.1 configurations. . Geosci. Model Dev. 10:(4):1487520
    [Crossref] [Google Scholar]
  102. 102.
    Wang J, Huang Y, Huang L, Dong Y, Huang W, et al. 2023.. Migration risk of fall armyworm (Spodoptera frugiperda) from North Africa to Southern Europe. . Front. Plant Sci. 14::1141470
    [Crossref] [Google Scholar]
  103. 103.
    Webster HN, Thomson DJ, Johnson BT, Heard IPC, Turnbull K, et al. 2012.. Operational prediction of ash concentrations in the distal volcanic cloud from the 2010 Eyjafjallajökull eruption. . J. Geophys. Res. Atmos. 117:(D20):D00U08
    [Crossref] [Google Scholar]
  104. 104.
    Wilson JD, Sawford BL. 1996.. Review of Lagrangian stochastic models for trajectories in the turbulent atmosphere. . Bound.-Lay. Meteorol. 78:(1):191210
    [Crossref] [Google Scholar]
  105. 105.
    Zadoks JC. 1981.. EPIPRE: a disease and pest management system for winter wheat developed in the netherlands. . EPPO Bull. 11:(3):36569
    [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-phyto-121423-041956
Loading
/content/journals/10.1146/annurev-phyto-121423-041956
Loading

Data & Media loading...

Supplemental Materials

Supplemental Materials

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error