Phytophthora infestans: New Tools (and Old Ones) Lead to New Understanding and Precision Management

Annual Review of Phytopathology

Volumn 54, Issue , 2016, Pages 529-547

  Fry, William E ^a  

^a Department of Molecular Biology and Genetics   (United States)

Author keywords

Field; Gene expression; Genotype; Late blight; Migration; Phenotype; Population

Indexed keywords

GENETICS; GROWTH, DEVELOPMENT AND AGING; MEXICO; MICROBIOLOGY; PHYSIOLOGY; PHYTOPHTHORA INFESTANS; PLANT DISEASE; POTATO; TOMATO;

LYCOPERSICON ESCULENTUM; MEXICO; PHYTOPHTHORA INFESTANS; PLANT DISEASES; SOLANUM TUBEROSUM;

EID: 84981312032     PISSN: 00664286     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev-phyto-080615-095951     Document Type: Article

References (88)

1. Anderson JB, Kohn LM. 1995. Clonality in soilborne, plant-pathogenic fungi. Annu. Rev. Phytopathol. 33:369-91
2. Andrade-Piedra J, Hijmans RJ, Forbes GA, Fry WE, Nelson RJ. 2005. Simulation of potato late blight in the Andes. I: Modification and parameterization of the LATEBLIGHT model. Phytopathology 95:1191-99
3. Araus JL, Cairns JE. 2014. Field high-throughput phenotyping: the new crop breeding frontier. Trends Plant Sci. 19:52-61
4. Barber D. 2009. You say tomato, I say agricultural disaster. New York Times, August 9
5. Bourke A. 1993. "The Visitation of God?" The Potato and the Great Irish Famine. Dublin, Irel.: Lilliput Press
6. Brurberg MB, Elameen A, Le VH, Nærstad R, Hermansen A, et al. 2011. Genetic analysis of Phytophthora infestans populations in the Nordic European countries reveals high genetic variability. Fungal Biol. 115:335-42
7. Cai G, Restrepo S, Myers K, Zuluaga AP, Danies G, et al. 2013. Gene profiling in partially resistant and susceptible near-isogenic tomatoes in response to late blight in the field. Mol. Plant Pathol. 14(2):171-84
8. Carter DA, Archer SA, Buck KW, Shaw DS, Shattock RC. 1990. Restriction fragment polymorphisms of mitochondrial DNA of Phytophthora infestans. Mycol. Res. 94:1123-28
9. Champouret N, Bouwmeester K, Rietman H, van der Lee T, Maliepaard C, et al. 2009. Phytophthora infestans isolates lacking class I ipiO variants are virulent on Rpi-blb1 potato. Mol. Plant-Microbe Interact. 22:1535-45
10. Childers R, Danies G, Myers K, Fei Z, Small IM, Fry WE. 2014. Acquired resistance to mefenoxam in sensitive isolates of Phytophthora infestans. Phytopathology 105:342-49
11. Chowdappa P, Kumar NBJ, Madhura S, Kumar MSP, Myers KL, et al. 2013. Emergence of 13-A2 blue lineage of Phytophthora infestans was responsible for severe outbreaks of late blight on tomato in south-west India. J. Phytopathol. 161:49-58
12. Chowdappa P, Kumar NBJ, Madhura S, Kumar MSP, Myers KL, et al. 2015. Severe outbreaks of late blight on potato and tomato in South India caused by recent changes in the Phytophthora infestans population. Plant Pathol. 64:191-99
13. Cobb JN, DeClerck G, Greenberg A, Clark R, McCouch S. 2013. Next-generation phenotyping: requirements and strategies for enhancing our understanding of genotype-phenotype relationships and its relevance to crop improvement. Theor. Appl. Genet. 126:867-87
14. Cooke DEL, Cano LM, Raffaele S, Bain RA, Cooke LR, et al. 2012. Genome analyses of an aggressive and invasive lineage of the Irish potato famine pathogen. PLOS Pathog. 8:e1002940
15. Crosier W. 1934. Studies in the biology of Phytophthora infestans (Mont.) de Bary. PhD Thesis, Cornell Univ., Ithaca, N.Y.
16. Danies G, Myers K, Mideros M, Restrepo S, Martin FN, et al. 2014. An ephemeral sexual population of Phytophthora infestans in the northeastern United States and Canada. PLOS ONE 9(12):e116354
17. Danies G, Small IM, Myers K, Childers R, Fry WE. 2013. Phenotypic characterization of recent clonal lineages of Phytophthora infestans in the United States. Plant Dis. 97:873-81
18. Dao J. 1995. Worst blight since Ireland's is chilling potato farmers. New York Times, July 30
19. Dong S, Stam R, Cano LM, Song J, Sklenar J, et al. 2014. Effector specialization in a lineage of the Irish potato famine pathogen. Science 343:552-55
20. Durrant W, Rowland O, Piedras P, Hammond-Kosack K, Jones J. 2000. cDNA-AFLP reveals a striking overlap in race-specific resistance and wound response gene expression profiles. Plant Cell 12:963-77
21. Elshire R, Glaubitz J, Sun Q, Poland J, Kawamoto K, et al. 2011. A robust, simple genotyping-bysequencing (GBS) approach for high diversity species. PLOS ONE 6:e19379
22. Eshed Y, Zamir D. 1995. An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield-associated QTL. Genetics 141:1147-62
23. Ewing EE, Simko I, Smart CD, Bonierbale MW, Mizubuti ESG, et al. 2000. Genetic mapping from field tests of qualitative and quantitative resistance to Phytophthora infestans in a population derived from Solanum tuberosum and Solanum berthaultii. Mol. Breed. 6:25-36
24. Fay JC, Fry WE. 1997. Effects of hot and cold temperatures on the survival of oospores produced by United States strains of Phytophthora infestans. Am. Potato J. 74:315-23
25. Fry WE. 1975. Integrated effects of polygenic resistance and a protective fungicide on development of potato late blight. Phytopathology 65:908-11
26. Fry WE. 2008. Phytophthora infestans, the crop (and R gene) destroyer. Mol. Plant Pathol. 9:385-402
27. Fry WE, Apple AE, Bruhn JA. 1983. Evaluation of potato late blight forecasts modified to incorporate host resistance and fungicide weathering. Phytopathology 73:1054-59
28. Fry WE, Birch PRJ, Judelson HS, Grünwald NJ, Danies G, et al. 2015. Five reasons to consider Phytophthora infestans a reemerging pathogen. Phytopathology 105:966-81
29. Fry WE, Bruck RI, Mundt CC. 1979. Retardation of potato late blight epidemics by fungicides with eradicant and protectant properties. Plant Dis. Rep. 63:970-74
30. Fry WE, Goodwin SB. 1995. Recent migrations of Phytophthora infestans. In Phytophthora infestans 150, ed. LJ Dowley, E Bannon, LR Cooke, T Keane, E O'Sullivan, pp. 89-95. Dublin, Irel.: Boole Press
31. Fry WE, Goodwin SB. 1997. Re-emergence of potato and tomato late blight in the United States. Plant Dis. 81:1349-57
32. Fry WE, Goodwin SB. 1997. Resurgence of the Irish potato famine fungus. Bioscience 47:363-71
33. Fry WE, Goodwin SB, Matuszak JM, Spielman LJ, Milgroom MG, Drenth A. 1992. Population genetics and intercontinental migrations of Phytophthora infestans. Annu. Rev. Phytopathol. 30:107-29
34. Fry WE, Grunwald NJ, Cooke DEL, McLeod A, Forbes GA, Cao K. 2009. Population genetics and population diversity of Phytophthora infestans. In Oomycete Genetics and Genomics: Diversity, Interactions and Research Tools, ed. K Lamour, S Kamoun, pp. 139-64. Hoboken, NJ: Wiley-Blackwell
35. Fry WE, McGrath MT, Seaman A, Zitter TA, McLeod A, et al. 2013. The 2009 late blight pandemic in the eastern United States: causes and results. Plant Dis. 97:296-306
36. Gavino PD, Smart CD, Sandrock RW, Miller JS, Hamm PB, et al. 2000. Implications of sexual reproduction for Phytophthora infestans in the United States: generation of an aggressive lineage. Plant Dis. 84:731-35
37. Goodwin SB, Cohen BA, Deahl KL, Fry WE. 1994. Migration from northern Mexico was the probable cause of recent genetic changes in populations of Phytophthora infestans in the United States and Canada. Phytopathology 84:553-58
38. Goodwin SB, Cohen BA, Fry WE. 1994. Panglobal distribution of a single clonal lineage of the Irish potato famine fungus. PNAS 91:11591-95
39. Goodwin SB, Drenth A, Fry WE. 1992. Cloning and genetic analyses of two highly polymorphic, moderately repetitive nuclear DNAs from Phytophthora infestans. Curr. Genet. 22:107-15
40. Goodwin SB, Smart CD, Sandrock RW, Deahl KL, Punja ZK, Fry WE. 1998. Genetic change within populations of Phytophthora infestans in the United States and Canada during 1994 to 1996: role of migration and recombination. Phytopathology 88:939-49
41. Goodwin SB, Sujkowski LS, Fry WE. 1995. Rapid evolution of pathogenicity within clonal lineages of the potato late blight disease fungus. Phytopathology 85:669-76
42. Goodwin SB, Sujkowski LS, Fry WE. 1996. Widespread distribution and probable origin of resistance to metalaxyl in clonal genotypes of Phytophthora infestans in the United States and western Canada. Phytopathology 86:793-800
43. Goss EM, Tabima JF, Cooke DEL, Restrepo S, Fry WE, et al. 2014. The Irish potato famine pathogen Phytophthora infestans originated in central Mexico rather than the Andes. PNAS 111:8791-96
44. Grünwald NJ, Flier WG. 2005. The biology of Phytophthora infestans at its center of origin. Annu. Rev. Phytopathol. 43:171-90
45. Halterman DA, Chen Y, Sopee J, Berduo-Sandoval J, Sanchez-Perez A. 2010. Competition between Phytophthora infestans effectors leads to increased aggressiveness on plants containing broad-spectrum late blight resistance. PLOS ONE 5:e10536
46. Hannukkala AO, Kaukoranta T, Lehtinen A, Rahkonen A. 2007. Late-blight epidemics on potato in Finland, 1933-2002; increased and earlier occurrence of epidemics associated with climate change and lack of rotation. Plant Pathol. 56:167-76
47. Hardwick NV. 2006. Disease forecasting. In The Epidemiology of Plant Diseases, ed. BM Cooke, DG Jones, B Kaye, pp. 239-67. Dordrecht, Neth.: Springer
48. Harrison JG. 1992. Effects of the aerial environment on late blight of potato foliage: a review. Plant Pathol. 41:384-416
49. Helgeson JP, Haberlach GT, Ehlenfeldt MK, Hunt G, Pohlman JD, Austin S. 1993. Sexual progeny of somatic hybrids between potato and Solanum brevidens: potential for use in breeding programs. Am. Potato J. 70:437-52
50. Hohl HR, Iselin K. 1984. Strains of Phytophthora infestans from Switzerland with A2mating type behavior. Trans. Br. Mycol. Soc. 83:529-30
51. Hu C-H, Perez FG, Donahoo R, McLeod A, Myers K, et al. 2012. Recent genotypes of Phytophthora infestans in the eastern United States reveal clonal populations and reappearance of mefenoxam sensitivity. Plant Dis. 96:1323-30
52. Johnson DA, Cummings TF, Hamm PB, Rowe RC, Miller JS, et al. 1997. Potato late blight in the Columbia Basin: an economic analysis of the 1995 epidemic. Plant Dis. 81:103-6
53. Kamoun S, Furzer O, Jones JDG, Judelson HS, Ali GS, et al. 2014. The top 10 oomycete pathogens in molecular plant pathology. Mol. Plant Pathol. 16(4):413-34
54. Kato M, Mizubuti ESG, Goodwin SB, Fry WE. 1997. Sensitivity to protectant fungicides and pathogenic fitness of clonal lineages of Phytophthora infestans in the United States. Phytopathology 87:973-78
55. Krause RA, Massie LB. 1975. Blitecast: a computerized forecast of potato late blight. Plant Dis. Rep. 59:95-98
56. Lambert DH, Currier AI. 1997. Differences in tuber rot development for North American clones of Phytophthora infestans. Am. Potato J. 74:39-43
57. Large EC. 1940. The Advance of the Fungi. New York: Dover Publ. 488 pp.
58. Leary WE. 1993. New fungus blight is threatening potato crops around the world. New York Times, October 24
59. Lees AK, Wattier R, Shaw DS, Sullivan L, Williams NA, Cooke DEL. 2006. Novel microsatellite markers for the analysis of Phytophthora infestans populations. Plant Pathol. 55:311-19
60. Li Y, Cooke DE, Jacobsen E, van der Lee T. 2013. Efficient multiplex simple sequence repeat genotyping of the oomycete plant pathogen Phytophthora infestans. J. Microbiol. Methods 92:316-22
61. Li Y, van der Lee T, Zhu JH, Jin GH, Lan CZ, et al. 2013. Population structure of Phytophthora infestans in China: geographic clusters and presence of the EU genotype Blue-13. Plant Pathol. 62:932-42
62. Liu D, Kashchandra GR, Hasegawa PM, Bressan RA. 1994. Osmotin overexpression in potato delays development of disease symptoms. PNAS 91:1888-92
63. Malcolmson JF. 1969. Races of Phytophthora infestans occurring in Great Britain. Trans. Br. Mycol. Soc. 53:417-23
64. Manosalva PM, Park S-W, Forouhar F, Tong L, Fry WE, Klessig DF. 2010. Methyl esterase 1 (StMES1) is required for systemic acquired resistance in potato. Mol. Plant-Microbe Interact. 23:1151-63
65. Matson MEH, Small IM, Fry WE, Judelson HS. 2015. Metalaxyl resistance in Phytophthora infestans: assessing role of RPA190 gene and diversity within clonal lineages. Phytopathology 105:1594-600
66. Mayton H, Smart CD, Moravec BC, Mizubuti ESG, Muldoon AE, Fry WE. 2000. Oospore survival and pathogenicity of single oospore recombinant progeny from a cross involving the US-8 and US-17 lineages of Phytophthora infestans. Plant Dis. 84:1190-96
67. Melhus IE. 1915. Germination and infection with the fungus of the late blight of potato (Phytophthora infestans). Agric. Exp. Stn. Res. Bull. 37, Univ. Wis., Madison, WI
68. Mizubuti ESG, Aylor DE, Fry WE. 2000. Survival of Phytophthora infestans sporangia exposed to solar radiation. Phytopathology 90:78-84
69. Niederhauser JS. 1991. Phytophthora infestans: the Mexican connection. In Phytophthora, ed. JA Lucas, RC Shattock, DS Shaw, LR Cooke, pp. 25-45. Cambridge: Cambridge Univ. Press
70. Pieterse CMJ, van West P, Verbakel HM, Brasse PWHM, van den Berg-Velthuis GCM, Govers F. 1994. Structure and genomic organization of the ipiB and ipiO gene clusters of Phytophthora infestans. Gene 138:67-77
71. Pule BB, Meitz JC, Thompson AH, Linde CC, Fry WE, et al. 2013. Phytophthora infestans populations in central, eastern and southern African countries consist of twomajor clonal lineages. Plant Pathol. 62:154-65
72. Runno-Paurson E, Fry WE, Myers KL, Koppel M, Mänd M. 2009. Characterisation of Phytophthora infestans isolates collected from potato in Estonia during 2002-2003. Eur. J. Plant Pathol. 124:565-75
73. Runno-Paurson E, Fry WE, Remmel T, Mand M, Myers KL. 2010. Phenotypic and genotypic characterisation of Estonian isolates of Phytophthora infestans in 2004-2007. Eur. J. Plant Pathol. 92:375-84
74. Saville A, Graham K, Grünwald N, Myers K, Fry WE, Ristaino JB. 2015. Fungicide sensitivity of USgenotypes of Phytophthora infestans (Mont.) de Bary to six oomycete-targeted compounds. Plant Dis. 99:659-66
75. Small IM, Joseph L, Fry WE. 2015. Development and implementation of the BlightPro decision support system for potato and tomato late blight management. Comput. Electron. Agric. 115:57-65
76. Small IM, Joseph L, Fry WE. 2015. Evaluation of the BlightPro decision support system for management of potato late blight using computer simulation and field validation. Phytopathology 107:1545-54
77. Smart CD, Tanksley SD, Mayton H, Fry WE. 2007. Resistance to Phytophthora infestans in Lycopersicon pennellii. Plant Dis. 91:1045-49
78. Song J, Bradeen JM, Naess SK, Raasch JA, Wielgus SM, et al. 2003. Gene RB cloned from Solanum bulbocastanum confers broad spectrum resistance to potato late blight. PNAS 100:9128-33
79. Stevens NE. 1933. The dark ages in plant pathology in America: 1830-1870. J. Wash. Acad. Sci. 23:435-46
80. Sujkowski LS, Goodwin SB, Dyer AT, Fry WE. 1994. Increased genotypic diversity via migration and possible occurrence of sexual reproduction of Phytophthora infestans in Poland. Phytopathology 84:201-7
81. Sujkowski LS, Goodwin SB, Fry WE. 1996. Changes in specific virulence in Polish populations of Phytophthora infestans: 1985-1991. Eur. J. Plant Pathol. 102:555-61
82. Tooley PW, Fry WE. 1983. Genetic variation in Phytophthora infestans identified through isozyme analysis. Phytopathology 73:827
83. USDA. 2004. Potatoes - Fall fungicide use, NSF Center for Integrated Pest Management. 2001. Natl. Agric. Stat. Serv.
84. Van der Vossen E, Sikkema A, Hekkert BTL, Gros J, Stevens P, et al. 2003. An ancient R gene from wild potato species Solanum bulbocastanum confers broad spectrum resistance to Phytophthora infestans in cultivated potato and tomato. Plant J. 36:867-82
85. Vleeshouwers VG, Oliver R. 2013. Effectors as tools in disease resistance breeding against biotrophic, hemibiotrophic, and necrotrophic plant pathogens. Mol. Plant-Microbe Interact. 27:196-206
86. Vleeshouwers VGAA, Raffaele S, Vossen JH, Champouret N, Oliva R, et al. 2011. Understanding and exploiting late blight resistance in the age of effectors. Annu. Rev. Phytopathol. 49:507-31
87. Woodham-Smith C. 1962. The Great Hunger. New York: Harper & Row. 510 pp.
88. Yuen JE, Andersson B. 2013. What is the evidence for sexual reproduction of Phytophthora infestans in Europe? Plant Pathol. 62:485-91