Modeling virus coinfection to inform management of maize lethal necrosis in Kenya

Phytopathology

Volumn 107, Issue 10, 2017, Pages 1095-1108

  Hilker, Frank M ^a   Allen, Linda J S ^b   Bokil, Vrushali A ^c   Briggs, Cheryl J ^d   Feng, Zhilan ^e   Garrett, Karen A ^f   Gross, Louis J ^g   Hamelin, Frédéric M ^h   Jeger, Michael J ⁱ   Manore, Carrie A ^j   Power, Alison G ^k   Redinbaugh, Margaret G ^l   Rúa, Megan A ^m   Cunniffe, Nik J ⁿ  

^a UNIVERSITY OF OSNABRÜCK   (Germany)

^b TEXAS TECH UNIVERSITY   (United States)

^c OREGON STATE UNIVERSITY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e PURDUE UNIVERSITY   (United States)

^f UNIVERSITY OF FLORIDA   (United States)

^g UNIVERSITY OF TENNESSEE   (United States)

^h Universite Rennes 1   (France)

ⁱ IMPERIAL COLLEGE LONDON   (United Kingdom)

^j LOS ALAMOS NATIONAL LABORATORY   (United States)

^k Department of Obstetrics Gynecology   (United States)

^l OHIO STATE UNIVERSITY   (United States)

^m WRIGHT STATE UNIVERSITY   (United States)

ⁿ UNIVERSITY OF CAMBRIDGE   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

AGRICULTURE; INSECT CONTROL; ISOLATION AND PURIFICATION; KENYA; MAIZE; MIXED INFECTION; PLANT DISEASE; PLANT SEED; POTYVIRUS; PREVENTION AND CONTROL; STATISTICS AND NUMERICAL DATA; THEORETICAL MODEL; TOMBUSVIRIDAE; VIROLOGY;

AGRICULTURE; COINFECTION; INSECT CONTROL; KENYA; MODELS, THEORETICAL; PLANT DISEASES; POTYVIRUS; SEEDS; TOMBUSVIRIDAE; ZEA MAYS;

EID: 85032615562     PISSN: 0031949X     EISSN: None     Source Type: Journal    
DOI: 10.1094/PHYTO-03-17-0080-FI     Document Type: Article

References (78)

1. Adams, I. P., Harju, V. A., Hodges, T., Hany, U., Skelton, A., Rai, S., Deka, M. K., Smith, J., Rox, A., Uzayisenga, B., Ngaboyisonga, C., Uwumukiza, B., Rutikanga, A., Rutherford, M., Richthis, B., Phiri, N., and Boonham, N. 2014. First report of maize lethal necrosis disease in Rwanda. New Dis. Rep. 29:22.
2. Adams, I. P., Miano, D. W., Kinyua, Z. M., Wangai, A., Kimani, E., Phiri, N., Reeder, R., Harju, V., Glover, R., Hany, U., Souza-Richards, R., Deb Nath, P., Nixon, T. Fox, A., Barnes, A., Smith, J., Skelton, A., Thwaites, R., Munford, R., and Boonham, N. 2013. Use of next-generation sequencing for the identification and characterization of Maize chlorotic mottle virus and Sugarcane mosaic virus causing maize lethal necrosis in Kenya. Plant Pathol. 62:741-749.
3. Allen, L. J. S. 2007. An Introduction to Mathematical Biology. Pearson Education Inc., Upper Saddle River, NJ.
4. Bassanezi, R. B., Montesino, L. H., Gimenes-Fernandes, N., Yamamoto, P. T., De Queiroz, L., Gottwald, T. R., Amorim, L., and Bergamin Filho, A. 2013. Efficacy of area-wide inoculum reduction and vector control on temporal progress of huanglongbing in young sweet orange plantings. Plant Dis. 97:789-796.
5. Bockelman, D. L., Claflin, L. E., and Uyemoto, J. K. 1982. Host range and seed-transmission studies of Maize chlorotic mottle virus in grasses and corn. Plant Dis. 66:216-218.
6. Bond, W. P., and Pirone, T. P. 1970. Evidence for soil transmission of Sugarcane mosaic virus. Phytopathology 60:437-440.
7. Buhnerkempe, M. G., Roberts, M. G., Dobson, A. P., Heesterbeek, H., Hudson, P. J., and Lloyd-Smith, J. O. 2015. Eight challenges in modelling disease ecology in multi-host, multi-agent systems. Epidemics 10:26-30.
8. Cabanas, D., Watanabe, S., Higashi, C. H. V., and Bressan, A. 2013. Dissecting the mode of Maize chlorotic mottle virus transmission (Tombusviridae: Machlomovirus) by Frankliniella williamsi (Thysanoptera: Thripidae). J. Econ. Entomol. 106:16-24.
9. Cunniffe, N. J., Cobb, R. C., Meentemeyer, R. K., Rizzo, D. M., and Gilligan, C. A. 2016. Modeling when, where, and how to manage a forest epidemic, motivated by sudden oak death in California. Proc. Natl. Acad. Sci. USA 113:5640-5645.
10. Cunniffe, N. J., and Gilligan, C. A. 2010. Invasion, persistence and control in models of soil-borne plant pathogens: The effect of host demography. J. R. Soc. Interface 7:439-451.
11. Cunniffe, N. J., and Gilligan, C. A. 2011. A theoretical framework for biological control of soil-borne plant pathogens: Identifying efficient strategies. J. Theor. Biol. 278:32-43.
12. Cunniffe, N. J., Koskella, B., Metcalf, C. J. E., Parnell, S., Gottwald, T. R., and Gilligan, C. A. 2015a. Thirteen challenges in modelling plant disease. Epidemics 10:6-10.
13. Cunniffe, N. J., Laranjeira, F. F., Neri, F. M., DeSimone, R. E., and Gilligan, C. A. 2014. Cost-effective control of plant disease when epidemiological knowledge is incomplete: Modelling Bahia bark scaling of citrus. PLOS Comput. Biol. 10:e1003753.
14. Cunniffe, N. J., Stutt, R. O. J. H., Desimone, R. E., Gottwald, T. R., and Gilligan, C. A. 2015b. Optimising and communicating options for the control of invasive plant disease when there is epidemiological uncertainty. PLOS Comput. Biol. 11:e1004211.
15. Cunniffe, N. J., Stutt, R. O. J. H., van den Bosch, F., and Gilligan, C. A. 2012. Time-dependent infectivity and flexible latent and infectious periods in compartmental models of plant disease. Phytopathology 102:365-380.
16. De Groote, H., Oloo, F., Tongruksawattana, S., and Das, B. 2016. Community-survey based assessment of the geographic distribution and impact of maize lethal necrosis (MLN) disease in Kenya. Crop Prot. 82:30-35.
17. Deng, T.-C., Chou, C.-M., Chen, C.-T., Tsai, C.-H., and Lin, F.-C. 2015. First report of Maize chlorotic mottle virus on sweet corn in Taiwan. Phytopathology 105:956-965.
18. Fargette, D., and Vié, K. 1995. Simulation of the effects of host resistance, reversion, and cutting selection on incidence of African cassava mosaic virus and yield losses in cassava. Phytopathology 85:370-375.
19. Gitonga, K. 2014. Maize lethal necrosis–The growing challenge in Eastern Africa. Online publication. USDA Foreign Agricultural Service Global Agricultural Information Network (GAIN) report. https://gain.fas.usda.gov/Recent%20GAIN%20Publications/Maize%20Lethal%20Necrosis%20-%20The %20growing%20challenge%20in%20Eastern%20Africa%20_Nairobi_Kenya_ 12-10-2014.pdf
20. Goldberg, K.-B., and Brakke, M. K. 1987. Concentration of Maize chlorotic mottle virus increased in mixed infections with maize dwarf mosaic virus, strain B. Phytopathology 77:162-177.
21. Gottwald, T. R., and Graham, J. H. 2014. Citrus diseases with global ramifications including citrus canker and huanglongbing. CAB Rev. Perspect. Agric. Vet. Sci. Nutr. Nat. Resour. 9:1-11.
22. Gowda, M., Das, B., Makumbi, D., Babu, R., Semagn, K., Mahuku, G., Olsen, M. S., Bright, J. M., Beyene, Y., and Prasanna, B. M. 2015. Genome-wide association and genomic prediction of resistance to maize lethal necrosis disease in tropical maize germplasm. Theor. Appl. Genet. 128:1957-1968.
23. Hamelin, F. M., Allen, L. J. S., Prendeville, H. R., Hajimorad, M. R., and Jeger, M. J. 2016a. The evolution of plant virus transmission pathways. J. Theor. Biol. 396:75-89.
24. Hamelin, F. M., Bisson, A., Desprez-Loustau, M. L., Fabre, F., and Mailleret, L. 2016b. Temporal niche differentiation of parasites sharing the same plant host: Oak powdery mildew as a case study. Ecosphere 7:e01517.
25. Hamelin, F. M., Castel, M., Poggi, S., Andrivon, D., and Mailleret, L. 2011. Seasonality and the evolutionary divergence of plant parasites. Ecology 92:2159-2166.
26. Hassan, M., Sahi, G. M., Wakil, W., and Imanat, Y. 2003. Aphid transmission of Sugarcane mosaic virus (SCMV). Pak. J. Agric. Sci. 40:74-76.
27. Hibino, H., Roechan, M., and Sudarisman, S. 1978. Association of two types of virus particles with penyakit habang (tungro disease) of rice in Indonesia. Phytopathology 68:1412-1416.
28. Holt, J., and Chancellor, T. C. B. 1996. Simulation modelling of the spread of rice tungro virus disease: The potential for management by roguing. J. Appl. Ecol. 33:927-936.
29. Holt, J., and Chancellor, T. C. B. 1997. A model of plant virus disease epidemics in asynchronously-planted cropping systems. Plant Pathol. 46:490-501.
30. Hyatt-Twynam, S. R., Parnell, S., Stutt, R. O. J. H., Gottwald, T. R., Gilligan, C. A., and Cunniffe, N. J. 2017. Risk-based management of invading plant disease. New Phytol. 214:1317-1329.
31. Jardine, D. J. 2017. Factsheets: Corn Lethal Necrosis. Online publication. http://www.plantpath.k-state.edu/extension/publications/cornlethalnecrosis.pdf
32. Jeger, M. J., Madden, L. V., and van den Bosch, F. 2009. The effect of transmission route on plant virus epidemic development and disease control. J. Theor. Biol. 258:198-207.
33. Jensen, S. G. 1985. Laboratory transmission of Maize chlorotic mottle virus by three species of corn rootworms. Plant Dis. 69:864-868.
34. Jensen, S. G., Wysong, D. S., Ball, E. M., and Higley, P. M. 1991. Seed transmission of maize chlorotic mottle virus. Plant Dis. 75:497-498.
35. Kang’ethe E. 2011. Situation Analysis: Improving Food Safety in the Maize Value Chain in Kenya. Online publication. College of Agriculture and Veterinary Science, University of Nairobi, Kenya. http://www.fao.org/fileadmin/user_upload/agns/pdf/WORKING_PAPER_AFLATOXIN_ REPORTDJ10thOctober.pdf
36. Kirimi, L. 2012. History of Kenyan Maize Production, Marketing and Policies. Tegemeo Institute of Agricultural Policy and Development, Nairobi, Kenya.
37. Kokkinos, C. D., Clark, C. A., Mcgregor, C. E., and Labonte, D. R. 2006. The effect of sweet potato virus disease and its viral components on gene expression levels in sweetpotato. J. Am. Soc. Hortic. Sci. 131:657-666.
38. Kusia, E. S., and Villinger, I. P. M. 2015. First report of lethal necrosis disease associated with co-infection of finger millet with Maize chlorotic mottle virus and Sugarcane mosaic virus in Kenya. Plant Dis. 99:899-900.
39. Li, L., Wang, X., and Zhou, G. 2007. Analyses of maize embryo invasion by Sugarcane mosaic virus. Plant Sci. 172:131-138.
40. Li, L., Wang, X. F., and Zhou, G. H. 2011. Effects of seed quality on the proportion of seed transmission for Sugarcane mosaic virus in maize. Cereal Res. Commun. 39:257-266.
41. Louie, R. 1980. Sugarcane mosaic virus in Kenya. Plant Dis. 64:944-947.
42. Lukanda, M., Owati, A., Ogunsanya, P., Valimunzigha, K., Katsongo, K., Ndemere, H., and Kumar, P. L. 2016. First report of Maize chlorotic mottle virus infecting maize in the Democratic Republic of the Congo. Crop Prot. 82:30-35.
43. Madden, L. V., Hughes, G., and van den Bosch, F. 2007. The Study of Plant Disease Epidemics. American Phytopathological Society, St. Paul, MN.
44. Madden, L. V., and van den Bosch, F. 2002. A population-dynamic approach to assess the threat of plant pathogens as biological weapons against annual crops. Bioscience 52:65-74.
45. Mahuku, G., Lockhart, B. E., Wanjala, B., Jones, M. W., Kimunye, J. N., Stewart, L. R., Cassone, B. J., Sevgan, S., Nyasani, J. O., Kusia, E., Kumar, P. L., Niblett, C. L., Kiggundu, A., Asea, G., Pappu, H. R., Wangai, A., Prasanna, B. M., and Redinbaugh, M. G. 2015. Maize lethal necrosis (MLN), an emerging threat to maize-based food security in sub-Saharan Africa. Phytopathology 105:956-965.
46. Mailleret, L., Castel, M., Montarry, J., and Hamelin, F. M. 2012. From elaborate to compact seasonal plant epidemic models and back: Is competitive exclusion in the details? Theor. Ecol. 5:311-324.
47. McQuaid, C. F., Sseruwagi, P., Pariyo, A., and van den Bosch, F. 2016. Cassava brown streak disease and the sustainability of a clean seed system. Plant Pathol. 65:299-309.
48. Mezzalama, M., Das, B., and Prasanna, B. M. 2015. MLN pathogen diagnosis, MLN-free seed production and safe exchange to non-endemic countries. Online publication. International Maize and Wheat Improvement Center (CIMMYT). http://repository.cimmyt.org/xmlui/bitstream/handle/10883/4284/56880.pdf?sequence=3
49. Milne, A. E., Bell, J. R., Hutchison, W. D., van den Bosch, F., Mitchell, P. D., Crowder, D., Parnell, S., and Whitmore, A. P. 2015. The effect of farmers’ decisions on pest control with Bt crops: A billion dollar game of strategy. PLOS Comput. Biol. 11:e1004483.
50. Morales, K., Zambrano, J. L., and Stewart, L. R. 2014. Co-infection and disease severity of Ohio Maize dwarf mosaic virus and Maize chlorotic dwarf virus strains. Plant Dis. 98:1661-1665.
51. Moritz, G., Brandt, S., Triapistyn, S., and Subramanian, S. 2013. Identification and information tools for pest thrips in East Africa. Online publication. QAAFI Biological Information Technology, University of Queensland, Australia. http://thripsnet.zoologie.uni-halle.de/key-server-neu/data/03030c05-030b4107-880b-0a0a0702060d/media/Html/index.html
52. Nault, L. R., Styer, W. E., Coffey, M. E., Gordon, D. T., Negi, L. S., and Niblett, C. L. 1978. Transmission of Maize chlorotic mottle virus by chrysomelid beetles. Phytopathology 68:1071-1074.
53. Nelson, S., Brewbaker, J., and Hu, J. 2011. Maize chlorotic mottle. Plant Dis. 79:1-6.
54. Niblett, C. L., and Claflin, L. E. 1978. Corn lethal necrosis—A new virus disease of corn in Kansas. Plant Dis. Rep. 62:15-19.
55. Phillips, N. J., Uyemoto, J. K., and Wilson, D. L. 1982. Maize chlorotic mottle virus and crop rotation: Effect of sorghum on virus incidence. Plant Dis. 66: 376-379.
56. Quito-Avila, D. F., Alvarez, R. A., and Mendoza, A. A. 2016. Occurrence of maize lethal necrosis in Ecuador: A disease without boundaries? Eur. J. Plant Pathol. 146:705-710.
57. Redinbaugh, M. G., and Zambrano, J. L. 2014. Control of virus diseases in maize. Pages 391-429 in: Control of Plant Virus Diseases—Seed-Propagated Crops. Advances in Virus Research, Vol. 90. G. Loebenstein and N. Katis, eds. Academic Press, Cambridge, MA.
58. Reynolds, T. W., Waddington, S. R., Anderson, C. L., Chew, A., True, Z., and Cullen, A. 2015. Environmental impacts and constraints associated with the production of major food crops in Sub-Saharan Africa and South Asia. Food Secur. 7:795-822.
59. Scheets, K. 1998. Maize chlorotic mottle machlomovirus and Wheat streak mosaic rymovirus concentrations increase in the synergistic disease corn lethal necrosis. Virology 242:28-38.
60. Seabloom, E. W., Borer, E. T., Gross, K., Kendig, A. E., Lacroix, C., Mitchell, C. E., Mordecai, E. A., and Power, A. G. 2015. The community ecology of pathogens: Coinfection, coexistence and community composition. Ecol. Lett. 18:401-415.
61. Semagn, K., Beyenea, Y., Babub, R., Nair, S., Gowda, M., Das, B., Tarekegne, A., Mugo, S., Mahuku, G., Worku, M., Warburton, M. L., Olsen, M., and Prasanna, B. M. 2015. Quantitative trait loci mapping and molecular breeding for developing stress resilient maize for sub-Saharan Africa. Crop Sci. 55:1449-1459.
62. Stewart, L. R., Teplier, R., Todd, J. C., Jones, M. W., Cassone, B. J., Wijeratne, S., Wijeratne, A., and Redinbaugh, M. G. 2014. Viruses in maize and johnsongrass in southern Ohio. Phytopathology 104:1360-1369.
63. Susi, H., Barrès, B., Vale, P. F., and Laine, A.-L. 2015. Co-infection alters population dynamics of infectious disease. Nat. Commun. 6: Article 5975. doi:10.1038/ncomms6975
64. Thomas-Sharma, S., Abdurahman, A., Ali, S., Andrade-Piedra, J. L., Bao, S., Charkowski, A. O., Crook, D., Kadian, M., Kromann, P., Struik, P. C., Torrance, L., Garrett, K. A., and Forbes, G. A. 2016. Seed degeneration in potato: The need for an integrated seed health strategy to mitigate the problem in developing countries. Plant Pathol. 65:3-16.
65. Thomas-Sharma, S., Andrade-Piedra, J., Carvajal Yepes, M., Hernandez Nopsa, J. F., Jeger, M. J., Jones, R. A. C., Kromann, P., Legg, J. P., Yuen, J., Forbes, G. A., and Garrett, K. A. 2017. A risk assessment framework for seed degeneration: Informing an integrated seed health strategy for vegetatively propagated crops. Phytopathology 107:1123-1135.
66. Thompson, R. N., Cobb, R. C., Gilligan, C. A., and Cunniffe, N. J. 2016. Management of invading pathogens should be informed by epidemiology rather than administrative boundaries. Ecol. Modell. 324:28-32.
67. Tollenaere, C., Susi, H., and Laine, A.-L. 2016. Evolutionary and epidemiological implications of multiple infection in plants. Trends Plant Sci. 21:80-90.
68. USDA. 2014. Maize Lethal Necrosis—The Growing Challenge in Eastern Africa. Washington, DC.
69. Uyemoto, J. K. 1983. Biology and control of Maize chlorotic mottle virus. Plant Dis. 67:7-10.
70. Uyemoto, J. K., Bockelman, D. L., and Claflin, L. E. 1980. Severe outbreak of corn lethal necrosis disease in Kansas. Plant Dis. 64:99-100.
71. van den Bosch, F., and De Roos, A. M. 1996. The dynamics of infectious diseases in orchards with roguing and replanting as control strategy. J. Math. Biol. 35:129-157.
72. van den Bosch, F., Jeger, M. J., and Gilligan, C. A. 2007. Disease control and its selection for damaging plant virus strains in vegetatively propagated staple food crops; a theoretical assessment. Proc. R. Soc. Lond. B 274:11-18.
73. Wangai, A. W., Redinbaugh, M. G., Kinyua, Z. M., Miano, D. W., Leley, P. K., Kasina, M., Mahuku, G., Scheets, K., and Jeffers, D. 2012. First report of Maize chlorotic mottle virus and maize lethal necrosis in Kenya. Plant Dis. 96:1582.
74. Xia, Z., Zhao, Z., Chen, L., Li, M., Zhou, T., Deng, C., Zhou, Q., and Fan, Z. 2016. Synergistic infection of two viruses MCMV and SCMV increases the accumulations of both MCMV and MCMV-derived siRNAs in maize. Sci. Rep. 6: Article 20520.
75. Xie, L., Zhang, J., Wang, Q., Meng, C., Hong, J., and Zhou, X. 2011. Characterization of Maize chlorotic mottle virus associated with maize lethal necrosis disease in China. J. Phytopathol. 159:191-193.
76. Zhang, X.-S., and Holt, J. 2001. Mathematical models of cross protection in the epidemiology of plant-virus diseases. Phytopathology 91:924-934.
77. Zhang, X.-S., Holt, J., and Colvin, J. 2001. Synergism between plant viruses: A mathematical analysis of the epidemiological implications. Plant Pathol. 50:732-746.
78. Zhao, M., Ho, H., Wu, Y., He, Y., and Li, M. 2014. Western flower thrips (Frankliniella occidentalis) transmits Maize chlorotic mottle virus. J. Phytopathol. 162:532-536.