Analyses of the population structure in a global collection of Phytophthora nicotianae isolates inferred from mitochondrial and nuclear DNA sequences

Phytopathology

Volumn 103, Issue 6, 2013, Pages 610-622

  Mammella, Marco A ^a   Martin, Frank N ^b   Cacciola, Santa O ^c   Coffey, Michael D ^d   Faedda, Roberto ^c   Schena, Leonardo ^a  

^a UNIVERSITY MEDITERRANEA OF REGGIO CALABRIA   (Italy)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

^c UNIVERSITY OF CATANIA   (Italy)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Intraspecific variability

Indexed keywords

MITOCHONDRIAL DNA;

ARTICLE; GENE EXPRESSION REGULATION; GENETIC MARKER; GENETIC VARIABILITY; GENETICS; HAPLOTYPE; PHYLOGENY; PHYSIOLOGY; PHYTOPHTHORA;

DNA, MITOCHONDRIAL; GENE EXPRESSION REGULATION; GENETIC MARKERS; GENETIC VARIATION; HAPLOTYPES; PHYLOGENY; PHYTOPHTHORA;

EID: 84877936532     PISSN: 0031949X     EISSN: None     Source Type: Journal    
DOI: 10.1094/PHYTO-10-12-0263-R     Document Type: Article

References (65)

1. Abbott, C. L., Gilmore, S. R., Lewis, C. T., Chapados, J. T., Peters, R. D., Platt, H. W., Coffey, M. D., and Lévesque, C. A. 2010. Development of a SNP genetic marker system based on variation in microsatellite flanking regions of Phytophthora infestans. Can. J. Plant Pathol. 32:440-457.
2. Álvarez, L. A., Pérez-Sierra, A., Armengol, J., and García-Jiménez, J. 2007. Characterization of Phytophthora nicotianae isolates causing collar and root rot of lavender and rosemary in Spain. J. Plant Pathol. 89:261-264.
3. Blair, J. E., Coffey, M. D., Park, S-Y., Geiser, D. M., and Kang, S. 2008. A multi-locus phylogeny for Phytophthora utilizing markers derived from complete genome sequences. Fungal Genet. Biol. 45:266-277.
4. Bonnet, P., Maia, N., Tello-Marquina, J., and Venard, P. 1978. Pouvoir pathogène du Phytophthora parasitica (Dastur): Facteurs de variabilité et notion de spécialisation parasitaire. Ann. Phytopathol. 10:15-29.
5. Brumfield, R. T., Beerli, P., Nickerson, D. A., and Edwards, S. V. 2003. The utility of single nucleotide polymorphisms in inferences of population history. Trends Ecol. Evol. 18:249-256.
6. Cacciola, S. O., and Magnano di San Lio, G. 2008. Management of citrus diseases caused by Phytophthora spp. Pages 61-84 in: Integrated Management of Diseases Caused by Fungi, Phytoplasma and Bacteria. A. Ciancio, and K. G. Mukerji, eds. Springer Science+Business Media B.V., Dordrecht, The Netherlands.
7. Cacciola, S. O., Pane, A., and Magnano di San Lio, G. 1997. Identification and quantitative determination of Phytophthora species infecting ornamental plants in nurseries. Pages 483-485 in: Diagnosis and Identification of Plant Pathogens. H. W. Dehne, G. Adam, M. Diekman, J. Frahm, A. Mauler-Machnik, and P. van Halteren, eds. Kluwer Academic Publishers, Dordrecht, The Netherlands.
8. Cárdenas, M., Grajales, A., Sierra, R., Rojas, A., Gonzalez-Almario, A., Vargas, A., Marin, M., Fermin, G., Lagos, L., Grünwald, N., Bernal, A., Salazar, C., and Restrepo, S. 2011. Genetic diversity of Phytophthora infestans in the Northern Andean region. BMC Genet. 12:23.
9. Chen, Y., and Roxby, R. 1996. Characterization of a Phytophthora infestans gene involved in the vesicle transport. Gene 181:89-94.
10. Clement, M., Posada, D., and Crandall, K. A. 2000. TCS: A computer program to estimate gene genealogies. Mol. Ecol. 9:1657-1660.
11. Colas, V., Lacourt, I., Ricci, P., Vanlerberghe-Masutti, F., Venard, P., Poupet, A., and Panabières, F. 1997. Diversity of virulence in Phytophthora parasitica on tobacco, as reflected by nuclear RFLPs. Phytopathology 88:205-212.
12. Cooke, D. E. L., Schena, L., and Cacciola S. O. 2007. Tools to detect, identify and monitor Phytophthora species in natural ecosystems. J. Plant Pathol. 89:13-28.
13. Dobrowolski, M. P., Tommerup, B. L., Blakeman, H. D., and O'Brien, P. A. 2002. Non-Mendelian inheritance revealed in a genetic analysis of sexual progeny of Phytophthora cinnamomi with microsatellite markers. Fungal Genet. Biol. 35:197-212.
14. Erwin, D. C. 1964. A strain of Phytophthora parasitica from okra and its sexual compatibility with isolates from citrus. Phytopathology 54:114-115.
15. Erwin, D. C., and Ribeiro, O. K. 1996. Phytophthora Diseases Worldwide. American Phytopathological Society Press, St. Paul, MN.
16. Excoffier, L., Laval, G., and Schneider, S. 2005. Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evol. Bioinf. Online 1:47-50.
17. Farris, J. S., Kallersjo, M., Kluge, A. G., and Bult, C. 1995. Testing significance of incongruence. Cladistics 10:315-319.
18. Flot, J. F. 2010. Seqphase: A web tool for interconverting phase input/output files and fasta sequence alignments. Mol. Ecol. Resour. 10:162-166.
19. Gobena, D., McGrath, M. T., and Lamour, K. 2012. Survival and spread of Phytophthora capsici on Long Island, New York. Mycol. Prog. 11:761-768.
20. Gobena, D., Roig, J., Galmarini, C., Hulvey, J., and Lamour, K. 2012. Genetic diversity of Phytophthora capsici isolates from pepper and pumpkin in Argentina. Mycologia 104:102-107.
21. Godinho, R., Crespo, E. G., and Ferrand, N. 2008. The limits of mtDNA phylogeography: Complex patterns of population history in a highly structured Iberian lizard are only revealed by the use of nuclear markers. Mol. Ecol. 17:4670-4683.
22. Gomez-Alpizar, L., Carbone, I., and Ristaino, J. B. 2007. An Andean origin of Phytophthora infestans inferred from mitochondrial and nuclear gene genealogies. Proc. Natl. Acad. Sci. USA 104:3306-3311.
23. Goodwin, S. B. 1997. The population genetics of Phytophthora. Phytopathology 87:462-473.
24. Goss, E. M., Carbone, I., and Grünwald, N. J. 2009. Ancient isolation and independent evolution of the three clonal lineages of the exotic sudden oak death pathogen Phytophthora ramorum. Mol. Ecol. 18:1161-1174.
25. Goss, E. M., Larsen, M., Vercauteren, A., Werres, S., Heungens, K., and Grünwald, N. J. 2011. Phytophthora ramorum in Canada: Evidence for migration within North America and from Europe. Phytopathology 101:166-171.
26. Grünwald, N. J., and Flier, W. G. 2005. The biology of Phytophthora infestans at its center of origin. Annu. Rev. Phytopathol. 43:171-190.
27. Grünwald, N. J., and Goss, E. M. 2011. Evolution and population genetics of exotic and re-emerging pathogens: novel tools and approaches. Annu. Rev. Phytopathol. 49:249-267.
28. Guindon, S., and Gascuel, O. 2003. A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52:696-704.
29. Hu, J. H., Hong, C. X. Stromberg, E. L., and Moorman, G. W. 2008. Mefenoxam sensitivity and fitness analysis of Phytophthora nicotianae isolates from nurseries in Virginia, USA. Plant Pathol. 57:728-736.
30. Hulvey, J., Gobena, D., Finley, L., and Lamour, K. 2010. Co-occurrence and genotypic distribution of Phytophthora species recovered from watersheds and plant nurseries of eastern Tennessee. Mycologia 102: 1127-1133.
31. Hulvey, J., Hurtado-Gonzalez, O., Aragón-Caballero, L., Gobena, D., Storey, D., Finley, L., and Lamour, K. 2011. Genetic diversity of the pepper pathogen Phytophthora capsici on farms in the Amazonian high jungle of Peru. Am. J. Plant Sci. 2:461-466.
32. Hurtado-Gonzales, O., Aragon-Caballero, L., Apaza-Tapia, W., Donahoo, R., and Lamour, K. 2008. Survival and spread of Phytophthora capsici in Coastal Peru. Phytopathology 98:688-694.
33. Jiang, R. H. Y., Brett, M. T., Whisson, S. C., Hardham, A. R., and Govers, F. 2006. Ancient origin of elicitin gene clusters in Phytophthora genomes. Mol. Biol. Evol. 23:338-351.
34. Johnson, E. S., Wolff, M. F., Wernsman, E. A., Atchely, W. R., and Shew, H. D. 2002. Origin of the black shank resistance gene, Ph, in tobacco cultivar Coker 371-gold. Plant Dis. 86:1080-1084.
35. Kebdani, N., Pieuchot, L., Deleury, E., Panabières, F., Le Berre, J. Y., and Gourgues, M. 2010. Cellular and molecular characterization of Phytophthora parasitica appressorium-mediated penetration. New Phytol. 185: 248-257.
36. Lamour, K. H., Daughtrey, M. L., Benson, D. M., Hwang, J., and Hausbeck, M. K. 2003. Etiology of Phytophthora drechsleri and P. nicotianae (=P. parasitica) diseases affecting floriculture crops. Plant Dis. 87:854-858.
37. Lamour, K. H., Stam, R., Jupe, J., and Huitema, E. 2011. The oomycete broad-host-range pathogen Phytophthora capsici. Mol. Plant Pathol. 13:329-337.
38. Librado, P., and Rozas, J. 2009. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451-1452.
39. Mammella, M. A., Cacciola, S. O., Martin, F., and Schena, L. 2011. Genetic characterization of Phytophthora nicotianae by the analysis of polymorphic regions of the mitochondrial DNA. Fungal Biol. 115:432-442.
40. Martin, F. 1995. Meiotic instability of Pythium sylvaticum as demonstrated by inheritance of nuclear markers and karyotype analysis. Genetics 139:1233-1246.
41. Martin, F. N. 2008. Mitochondrial haplotype determination in the oomycete plant pathogen Phytophthora ramorum. Curr. Genet. 54:23-34.
42. Martin, F. N., Abad, Z. G., Balci, Y., and Ivors, K. 2012. Identification and detection of Phytophthora: reviewing our progress, identifying our needs. Plant Dis. 96:1080-1103.
43. Martin, F. N., and Coffey, M. D. 2012. Mitochondrial haplotype analysis for differentiation of isolates of Phytophthora cinnamomi. Phytopathology 102:229-239.
44. Martin, F. N., and Tooley, P. W. 2003. Phylogenetic relationships among Phytophthora species inferred from sequence analysis of mitochondrially encoded cytochrome oxidase I and II genes. Mycologia 95:269-284.
45. Matheron, M. E., and Matejka, J. C. 1990. Differential virulence of Phytophthora parasitica recovered from Citrus and other plants to rough lemon and tomato. Plant Dis. 74:138-140.
46. Milne, I., Lindner, D., Bayer, M., Husmeier, D., McGuire, G., Marshall, D. F., and Wright, F. 2009. TOPALi v2: A rich graphical interface for evolutionary analyses of multiple alignments on HPC clusters and multicore desktops. Bioinformatics 25:126-127.
47. Moralejo, E., Pérez-Sierra, A. M., Álvarez, L. A., Belbahri, L., Lefort, F., and Descals, E. 2009. Multiple alien Phytophthora taxa discovered on diseased ornamental plants in Spain. Plant Pathol. 58:100-110.
48. Ospina-Giraldo, M. D., and Jones, R. W., 2003. Characterization of the glucose-6-phosphate isomerase gene in Phytophthora infestans reveals the presence of multiple alleles. Fungal Genet. Biol. 40:197-206.
49. Pane, A., Martini, P., Chimento, A., Rapetti, S., Savona, S., Grasso, F. M., and Cacciola, S. O. 2005. Phytophthora species on ornamental plants in Italy. J. Plant Pathol. S87:301.
50. Parkunan, V., Johnson, C. S., Bowman, B. C., and Hong, C. X. 2010. Population structure, mating type, and mefenoxam sensitivity of Phytophthora nicotianae in Virginia tobacco fields. Plant Dis. 94:1361-1365.
51. Qutob, D., Kamoun, S., and Gijzen, M. 2002. Expression of a Phytophthora sojae necrosis-inducing protein occurs during transition from biotrophy to necrotrophy. Plant J. 32:361-373.
52. Ronquist, F., and Huelsenbeck, J. P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574.
53. Schena, L., Cardle, L., and Cooke, D. 2008. Use of genome sequence data in the design and testing of SSR markers for Phytophthora species. BMC Genomics 9:620.
54. Schena, L., and Cooke, D. E. L. 2006. Assessing the potential of regions of the nuclear and mitochondrial genome to develop a "molecular tool box" for the detection and characterization of Phytophthora species. J. Microbiol. Methods 67:70-85.
55. Schlotterer, C. 2000. Evolutionary dynamics of microsatellite DNA. Chromosoma 109:365-371.
56. Schwingle, B. W., Smith, J. A., and Blanchette, R. A. 2007. Phytophthora Species associated with diseased woody ornamentals in Minnesota nurseries. Plant Dis. 91:97-102.
57. Shan, W., and Hardham, A.R. 2004. Construction of a bacterial artificial chromosome library, determination of genome size, and characterization of an Hsp70 gene family in Phytophthora nicotianae. Fungal Genet. Biol. 41:369-380.
58. Stokstad, E. 2004. Nurseries may have shipped sudden oak death pathogen nationwide. Science 303:1959.
59. Sullivan, M. J., Parks, E. J., Cubeta, M. A., Gallup, C.A., Melton, T. A., Moyer, J. W., and Shew, H. D. 2010. An assessment of the genetic diversity in a field population of Phytophthora nicotianae with a changing race structure. Plant Dis. 94:455-460.
60. Van der Lee, T., Testa, A., Robold, A., van 't Klooster, J., and Govers, F. 2004. High-density genetic linkage maps of Phytophthora infestans reveal trisomic progeny and chromosomal rearrangements. Genetics 167:1643-1661.
61. Vercauteren, A., Boutet, X., D'hondt, L., Van Bockstaele, E., Maes, M., Leus, L., Chandelier, A., and Heungens, K. 2011. Aberrant genome size and instability of Phytophthora ramorum oospore progenies. Fungal Genet. Biol. 48:537-543.
62. Wright, S. 1965. The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution 19:395-420.
63. Yakabe, L. E., Blomquist, C. L., Thomas, S. L., and MacDonald, J. D. 2009. Identification and frequency of Phytophthora species associated with foliar diseases in California ornamental nurseries. Plant Dis. 93:884-890.
64. Zhang, D. X., and Hewitt, G. M. 2003. Nuclear DNA analyses in genetic studies of populations: Practice problems and prospects. Mol. Ecol. 12:563-584.
65. Zhang, X. G., Sun, W. X., Guo, L., Yu, J. F., and Chang, C. J. 2003. Genetic and pathogenic variation among tobacco black shank strains of Phytophthora parasitica var. nicotianae from the main tobacco growing in China. J. Phytopathol. 151:259-266.