Molecular analyses of Pythium irregulare isolates from grapevines in South Africa suggest a single variable species

Fungal Biology

Volumn 115, Issue 12, 2011, Pages 1210-1224

  Spies, Christoffel F J ^a   Mazzola, Mark ^b   Botha, Wilhelm J ^c   Langenhoven, Shaun D ^a   Mostert, Lizel ^a   Mcleod, Adéle ^a  

^a STELLENBOSCH UNIVERSITY   (South Africa)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

^c AGRICULTURAL RESEARCH COUNCIL   (South Africa)

Author keywords

tubulin; Cox1; Cox2; ITS; Oomycete; Pythium cryptoirregulare; Pythium cylindrosporum; Pythium irregulare; Pythium regulare; Species complex; Taxonomy

Indexed keywords

FUNGAL DNA; FUNGAL PROTEIN; RIBOSOMAL SPACER DNA;

EUKARYOTE; MOLECULAR ANALYSIS; MORPHOLOGY; PHYLOGENETICS; PHYLOGENY; POLYPLOIDY; TAXONOMY; VINE;

ARTICLE; CLASSIFICATION; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR GENETICS; PHYLOGENY; PYTHIUM; SOUTH AFRICA; VITIS;

DNA, FUNGAL; DNA, RIBOSOMAL SPACER; FUNGAL PROTEINS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PYTHIUM; SOUTH AFRICA; VITIS;

SOUTH AFRICA;

OOMYCETES; PYTHIUM; PYTHIUM CYLINDROSPORUM; PYTHIUM IRREGULARE; PYTHIUM REGULARE; VITIS;

EID: 81955162891     PISSN: 18786146     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.funbio.2011.08.006     Document Type: Article

References (71)

1. Allain-Boulé N., Tweddell R., Mazzola M., Bélanger R., Lévesque C.A. Pythium attrantheridium sp. nov.: taxonomy and comparison with related species. Mycological Research 2004, 108:795-805.
2. álvarez I., Wendel J.F. Ribosomal ITS sequences and plant phylogenetic inference. Molecular Phylogenetics and Evolution 2003, 29:417-434.
3. Bala K., Robideau G.P., Désaulniers N., De Cock A.W.A.M., Lévesque C.A. Taxonomy, DNA barcoding and phylogeny of three new species of Pythium from Canada. Persoonia 2010, 25:22-31.
4. Barr D.J.S., Warwick S.I., Desaulniers N.L. Isozyme variation, morphology, and growth response to temperature in Pythium irregulare. Canadian Journal of Botany 1997, 75:2073-2081.
5. Belbahri L., McLeod A., Paul B., Calmin G., Moralejo E., Spies C.F.J., Botha W.J., Clemente A., Descals E., Sánchez-Hernández E., Lefort F. Intraspecific and within-isolate sequence variation in the ITS rRNA gene region of Pythium mercuriale sp. nov. (Pythiaceae). FEMS Microbiology Letters 2008, 284:17-27.
6. Bhat R.G., Schmitthenner A.F. Genetic crosses between physiological races of Phytophthora sojae. Experimental Mycology 1993, 17:122-129.
7. Biesbrock J.A., Hendrix F.F. A taxonomic study of Pythium irregulare and related species. Mycologia 1967, 59:943-952.
8. Blair J.E., Coffey M.D., Park S.Y., Geiser D.M., Kang S. A multi-locus phylogeny for Phytophthora utilizing markers derived from complete genome sequences. Fungal Genetics and Biology 2008, 45:266-277.
9. Bowers J.H., Martin F.N., Tooley P.W., Luz E.D.M.N. Genetic and morphological diversity of temperate and tropical isolates of Phytophthora capsici. Phytopathology 2007, 97:492-503.
10. Campbell C.S., Wojciechowski M.F., Baldwin B.G., Alice L.A., Donoghue M.J. Persistent nuclear ribosomal DNA sequence polymorphism in the Amelanchier agamic complex (Rosaceae). Molecular Biology and Evolution 1997, 14:81-90.
11. Chamnanpunt J., Shan W., Tyler B.M. High frequency mitotic gene conversion in genetic hybrids of the oomycete Phytophthora sojae. Proceedings of the National Academy of Sciences 2001, 98:14530-14535.
12. Chen W., Schneider R.W., Hoy J.W. Taxonomic and phylogenetic analyses of ten Pythium species using isozyme polymorphisms. Phytopathology 1992, 82:1234-1244.
13. Cooke D.E., Duncan J.M. Phylogenetic analysis of Phytophthora species based on ITS1 and ITS2 sequences of the ribosomal RNA gene repeat. Mycological Research 1997, 101:667-677.
14. Dhingra O.D., Sinclair J.S. Basic Plant Pathology Methods 1985, CRC Press, Florida.
15. Dick M.W. Keys to Pythium 1990, Published by the author, Reading.
16. Drenth A., Wagels G., Smith B., Sendall B., O'Dwyer C., Irvine G., Irwin J.A.G. Development of a DNA-based method for detection and identification of Phytophthora species. Australasian Plant Pathology 2006, 35:147-159.
17. Feliner G.N., Rosselló J.A. Better the devil you know? Guidelines for insightful utilization of nrDNA ITS in species-level evolutionary studies in plants. Molecular Phylogenetics and Evolution 2007, 44:911-919.
18. Förster H., Coffey M.D. Mating behavior of Phytophthora parasitica: evidence for sexual recombination in oospores using DNA restriction fragment length polymorphisms as genetic markers. Experimental Mycology 1990, 14:351-359.
19. Förster H., Tyler B.M., Coffey M.D. Phytophthora sojae races have arisen by clonal evolution and by rare outcrosses. Molecular Plant-Microbe Interactions 1994, 7:780-791.
20. Francis D.M., St.Clair D.A. Outcrossing in the homothallic oomycete, Pythium ultimum, detected with molecular markers. Current Genetics 1993, 24:100-106.
21. Francis D.M., Gehlen M.F., St Clair D.A. Genetic variation in homothallic and hyphal swelling isolates of Pythium ultimum var. ultimum and P. ultimum var. sporangiferum. Molecular Plant-Microbe Interactions 1994, 7:766-775.
22. Francis D.M., St.Clair D.A. Population genetics of Pythium ultimum. Phytopathology 1997, 87:454-461.
23. Galindo J., Gallegly M.E. The nature of sexuality in Phytophthora infestans. Phytopathology 1960, 50:123-128.
24. Gams W., Hoekstra E.S., Aptroot A. CBS Course of Mycology 1998, Centraalbureau voor Schimmelcultures, Baarn, The Netherlands. 4th edn.
25. Gandolfi A., Bonilauri P., Rossi V., Menozzi P. Intraindividual and intraspecies variability of ITS1 sequences in the ancient asexual Darwinula stevensoni (Crustacea: Ostracoda). Heredity 2001, 87:449-455.
26. Garzón C.D., Geiser D.M., Moorman G.W. Amplified fragment length polymorphism analysis and internal transcribed spacer and coxII sequences reveal a species boundary within Pythium irregulare. Phytopathology 2005, 95:1489-1498.
27. Garzón C.D., Yánez J.M., Moorman G.W. Pythium cryptoirregulare, a new species within the P. irregulare complex. Mycologia 2007, 99:291-301.
28. Goodwin S.B., Drenth A., Fry W.E. Cloning and genetic analyses of two polymorphic, moderately repetitive nuclear DNAs from Phytophthora infestans. Current Genetics 1992, 22:107-115.
29. Harvey P.R., Butterworth P.J., Hawke B.G., Pankhurst C.E. Genetic variation among populations of Pythium irregulare in southern Australia. Plant Pathology 2000, 49:619-627.
30. Harvey P.R., Butterworth P.J., Hawke B.G., Pankhurst C.E. Genetic and pathogenic variation among cereal, medic and sub-clover isolates of Pythium irregulare. Mycological Research 2001, 105:85-93.
31. Hendrix F.F., Papa K.E. Taxonomy and genetics of Pythium. Procedures of the American Phytopathological Society 1974, 1:200-207.
32. Hey J. The mind of the species problem. Trends in Ecology & Evolution 2001, 16:326-329.
33. Kageyama K., Senda M., Asano T., Suga H., Ishiguro K. Intra-isolate heterogeneity of the ITS region of rDNA in Pythium helicoides. Mycological Research 2007, 111:416-423.
34. Katoh K., Toh H. Recent developments in the MAFFT sequence alignment program. Bioinformatics 2008, 9:286-298.
35. Kroon L.P.N.M., Bakker F.T., van den Bosch G.B.M., Bonants P.J.M., Flier W.G. Phylogenetic analysis of Phytophthora species based on mitochondrial and nuclear DNA sequences. Fungal Genetics and Biology 2004, 41:766-782.
36. Lee S., Moorman G.W. Identification and characterization of simple sequence repeat markers for Pythium aphanidermatum, P. cryptoirregulare, and P. irregulare and the potential use in Pythium population genetics. Current Genetics 2008, 53:81-93.
37. Lee S.B., Taylor J.W. Isolation of DNA from fungal mycelia and single spores. PCR Protocols: a guide to methods and applications 1990, 282-287. Academic Press, New York, USA. M.A. Innis, D.H. Gelfand, J.J. Sninsky, T.J. White (Eds.).
38. Lévesque C.A., De Cock A.W.A.M. Molecular phylogeny and taxonomy of the genus Pythium. Mycological Research 2004, 108:1363-1388.
39. Man in't Veld W.A., Govers F., Meijer H.J.G. Correlation of isozyme profiles with genomic sequences of Phytophthora ramorum and its P. sojae orthologues. Current Genetics 2007, 52:247-257.
40. Marais P.G. Fungi associated with root rot in vineyards in the Western Cape. Phytophylactica 1979, 11:65-68.
41. Marais P.G. Fungi associated with decline and death of nursery grapevines in the Western Cape. Phytophylactica 1980, 12:9-12.
42. Martin F.N. Variation in the ribosomal DNA repeat unit within single-oospore isolates of the genus Pythium. Genome 1990, 33:585-591.
43. Martin F.N. Electrophoretic karyotype polymorphisms in the genus Pythium. Mycologia 1995, 87:333-353.
44. Martin F.N. Meiotic instability of Pythium sylvaticum as demonstrated by inheritance of nuclear markers and karyotype analysis. Genetics 1995, 139:1233-1246.
45. Martin F.N. Phylogenetic relationships among some Pythium species inferred from sequence analysis of the mitochondrially encoded cytochrome oxidase II gene. Mycologia 2000, 92:711-727.
46. Martin F.N., Tooley P.W. Phylogenetic relationships among Phytophthora species inferred from sequence analysis of the mitochondrially encoded cytochrome oxidase I and II genes. Mycologia 2003, 95:269-284.
47. Masih I., Paul B. Pythium regulare sp. nov, isolated from the Canary Islands, its taxonomy, its region of rDNA, and comparison with related species. Current Microbiology 2003, 47:309-313.
48. Matsumoto C., Kageyama K., Suga H., Hyakumachi M. Intraspecific DNA polymorphisms of Pythium irregulare. Mycological Research 2000, 104:1333-1341.
49. McLeod A., Denman S., Sadie A., Denner F.D.N. Characterization of South African isolates of Phytophthora infestans. Plant Disease 2001, 85:287-291.
50. McLeod A., Botha W.J., Meitz J.C., Spies C.F.J., Tewoldemedhin Y.T., Mostert L. Morphological and phylogenetic analyses of Pythium species in South Africa. Mycological Research 2009, 113:933-951.
51. Moralejo E., Clemente A., Descals E., Belbahri L., Calmin G., Lefort F., Spies C.F.J., McLeod A. Pythium recalcitrans sp. nov. revealed by multigene phylogenetic analysis. Mycologia 2008, 100:296-305.
52. Morrison D.A., Ellis J.T. Effect of nucleotide sequence alignment on phylogeny estimations: a case study of 18S rDNAs of Apicomplexa. Molecular Biology and Evolution 1997, 14:428-444.
53. Mostowfizadeh-Ghalamfarsa R., Cooke D.E.L., Banihashemi Z. Phytophthora parsiana sp. nov., a new high-temperature tolerant species. Mycological Research 2008, 112:783-794.
54. Nechwatal J., Mendgen K. Evidence or the occurrence of natural hybridization in reed-associated Pythium species. Plant Pathology 2009, 58:261-270.
55. Palmer J.D. The symbiotic birth and spread of plastids: how many times and whodunit?. Journal of Phycology 2003, 39:4-11.
56. Paul B. Pythium cylindrosporum: a new soil fungi from Germany. International Journal of Mycology and Lichenology 1992, 4:337-345.
57. Pawlowska T.E., Taylor J.W. Organization of genetic variation in individuals of arbuscular mycorrhizal fungi. Nature 2004, 427:733-737.
58. Razafimandimbison S.G., Kellogg E.A., Bremer B. Recent origin and phylogenetic utility of divergent ITS putative pseudogenes: a case study from Naucleeae (Rubiaceae). Systematic Biology 2004, 53:177-192.
59. Ronquist F., Huelsenbeck J.P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
60. Rosselló J.A., Lázaro A., Cosín R., Molins A. A phylogeographic split in Buxus balearica (Buxaceae) as evidenced by nuclear ribosomal markers: when ITS paralogues are welcome. Journal of Molecular Evolution 2007, 64:143-157.
61. Schurko A., Mendoza L., De Cock A.W.A.M., Klassen G.R. Evidence for geographic clusters: molecular genetic differences among strains of Pythium insidiosum from Asia, Australia and the Americas are explored. Mycologia 2003, 95:200-208.
62. Simon U.K., Weiß M. Intragenomic variation of fungal ribosomal genes is higher than previously thought. Molecular Biology and Evolution 2008, 25:2251-2254.
63. Spies C.F.J., Mazzola M., McLeod A. Characterisation and detection of the Pythium and Phytophthora species associated with grapevines in South Africa. European Journal of Plant Pathology 2011, 131:113-119.
64. Spies C.F.J., Mazzola M., Botha W.J., Van der Rijst M., Mostert L., McLeod A. Oogonial biometry and phylogenetic analyses of the Pythium vexans species group from woody agricultural hosts in South Africa reveal distinct groups within this taxon. Fungal Biology 2011, 115:157-168.
65. Taylor J.W., Jacobson D.J., Kroken S., Kasuga T., Geiser D.M., Hibbett D.S., Fisher M.C. Phylogenetic species recognition and species concepts in fungi. Fungal Genetics and Biology 2000, 31:21-32.
66. Van der Plaats-Niterink J. Monograph of the genus Pythium. Studies in Mycology 1981, 21. Centraalbureau voor Schimmelcultures, Baarn, The Netherlands.
67. Van Wintzingerode F., Göbel U.B., Stackebrandt E. Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis. FEMS Microbiology Reviews 1997, 21:213-229.
68. Villa N.O., Kageyama K., Asano T., Suga H. Phylogenetic relationships of Pythium and Phytophthora species based on ITS rDNA, cytochrome oxidase II and ß-tubulin gene sequences. Mycologia 2006, 98:410-422.
69. Whisson S.C., Drenth A., Maclean D.J., Irwin J.A.G. Evidence for outcrossing in Phytophthora sojae and linkage of a DNA marker to two avirulence genes. Current Genetics 1994, 27:77-82.
70. White T.J., Bruns T., Lee S., Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols: a guide to methods and applications 1990, 315-322. Academic Press, New York. M.A. Innis, D.H. Gelfand, J.J. Sninsky, T.J. White (Eds.).
71. Zheng X., Cai D., Yao L., Teng Y. Non-concerted ITS evolution, early origin and phylogenetic utility of ITS pseudogenes in Pyrus. Molecular Phylogenetics and Evolution 2008, 48:892-903.