Cryptic species, native populations and biological invasions by a eucalypt forest pathogen

Molecular Ecology

Volumn 21, Issue 18, 2012, Pages 4452-4471

  Pérez, Guillermo ^a   Slippers, Bernard ^a   Wingfield, Michael J ^a   Wingfield, Brenda D ^a   Carnegie, Angus J ^b   Burgess, Treena I ^c  

^a UNIVERSITY OF PRETORIA   (South Africa)

^b Biosecurity Research Industry and Investment   (Australia)

^c MURDOCH UNIVERSITY   (Australia)

Author keywords

Eucalyptus; forest pathogen; microsatellite; Mycosphaerella leaf disease; population genetics; structure; Teratosphaeria nubilosa

Indexed keywords

FUNGAL DNA; MICROSATELLITE DNA; RIBOSOMAL SPACER DNA;

AGRICULTURE; ARTICLE; ASCOMYCETES; AUSTRALIA; BAYES THEOREM; CLASSIFICATION; DNA SEQUENCE; EUCALYPTUS; GENETIC VARIABILITY; GENETICS; MICROBIOLOGY; MOLECULAR GENETICS; MULTIVARIATE ANALYSIS; NUCLEOTIDE SEQUENCE; PHYLOGENY; POPULATION GENETICS; TREE;

AGRICULTURE; ASCOMYCOTA; AUSTRALIA; BAYES THEOREM; DNA, FUNGAL; DNA, RIBOSOMAL SPACER; EUCALYPTUS; GENETIC VARIATION; GENETICS, POPULATION; MICROSATELLITE REPEATS; MOLECULAR SEQUENCE DATA; MULTIVARIATE ANALYSIS; PHYLOGENY; SEQUENCE ANALYSIS, DNA; TREES;

EUCALYPTUS; MYCOSPHAERELLA; TERATOSPHAERIA;

EID: 84866239078     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2012.05714.x     Document Type: Article

References (86)

1. Andjic V, Barber PA, Carnegie AJ, et al. (2007) Kirramyces viscidus sp. nov., a new eucalypt pathogen from tropical Australia closely related to the serious leaf pathogen, Kirramyces destructans. Australasian Plant Pathology, 36, 478-487.
2. Andjic V, Pegg G, Carnegie AJ, et al. (2010) Phylogeographic study reveals new cryptic species Teratosphaeria pseudoeucalypti responsible for leaf blight of Eucalyptus in subtropical and tropical Australia. Plant Pathology, 59, 900-912.
3. Arnaud-Haond S, Belkhir K, (2007) GENCLONE: a computer program to analyse genotypic data, test for clonality and describe spatial clonal organization. Molecular Ecology Notes, 7, 15-17.
4. Arnaud-Haond S, Duarte CM, Alberto F, Serrào EA, (2007) Standardizing methods to address clonality in population studies. Molecular Ecology, 16, 5115-5139.
5. Barber PA, Carnegie AJ, Burgess TI, Keane PJ, (2008) Leaf diseases caused by Mycosphaerella species in Eucalyptus globulus plantations and nearby native forest in the Green Triangle Region of southern Australia. Australasian Plant Pathology, 37, 372-481.
6. Bickford D, Lohman DJ, Sodhi NS, et al. (2007) Cryptic species as a window on diversity and conservation. Trends in Ecology & Evolution, 22, 148-155.
7. Billiard S, Lõpez-Villavicencio M, Devier B, et al. (2011) Having sex, yes, but with whom? Inferences from fungi on the evolution of anisogamy and mating types. Biological Reviews, 86, 421-442.
8. Brasier CM, (2008) The biosecurity threat to the UK and global environment from international trade in plants. Plant Pathology, 57, 792-808.
9. Brown JKM, Hovmøller MS, (2002) Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science, 297, 537-541.
10. Brumfield RT, Beerli P, Nickerson DA, Edwards SV, (2003) The utility of single nucleotide polymorphisms in inferences of population history. Trends in Ecology and Evolution, 18, 249-256.
11. Burgess TI, Sakalidis ML, Hardy GESJ, (2006) Gene flow of the canker pathogen Botryosphaeria australis between Eucalyptus globulus plantations and native eucalypt forests in Western Australia. Austral Ecology, 31, 559-566.
12. Burgess TI, Barber PA, Sufaati S, et al. (2007) Mycosphaerella spp. on Eucalyptus in Asia; new species; new hosts and new records. Fungal Diversity, 24, 135-157.
13. Burnett JH, (2003) Fungal Populations and Species. Oxford University Press, Oxford.
14. Carnegie AJ, (2007a) Forest health condition in New South Wales, Australia, 1996-2005. I. Fungi recorded from eucalypt plantations during forest health surveys. Australasian Plant Pathology, 36, 213-224.
15. Carnegie AJ, (2007b) Forest health condition in New South Wales, Australia, 1996-2005. II. Fungal damage recorded in eucalypt plantations during forest health surveys and their management. Australasian Plant Pathology, 36, 225-239.
16. Carnegie AJ, Ades PK, (2003) Mycosphaerella leaf disease reduces growth of plantation-grown Eucalyptus globulus. Australian Forestry, 66, 113-119.
17. Carnegie AJ, Keane PJ, Podger FD, (1997) The impact of three species of Mycosphaerella newly recorded on Eucalyptus in Western Australia. Australasian Plant Pathology, 26, 71-77.
18. Carnegie AJ, Burgess TI, Beilharz V, Wingfield MJ, (2007) New species of Mycosphaerella from Myrtaceae in plantations and native forests in eastern Australia. Mycologia, 99, 461-474.
19. Chen RS, Boeger JM, McDonald BA, (1994) Genetic stability in a population of a plant pathogenic fungus over time. Molecular Ecology, 3, 209-218.
20. Clegg SM, Degnan SM, Kikkawa J, et al. (2002) Genetic consequences of sequential founder events by an island-colonizing bird. Proceedings of the National Academy of Sciences of the USA, 99, 8127-8132.
21. Clement M, Posada D, Crandall KA, (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657-1659.
22. Crous PW, (1998) Mycosphaerella spp. and their anamorphs associated with leaf spot diseases of Eucalyptus. Mycologia Memoir, 21, 1-170.
23. Crous PW, Groenewald JZ, Mansilla PJ, Hunter GC, Wingfield MJ, (2004) Phylogenetic reassessment of Mycosphaerella spp. and their anamorphs occurring on Eucalyptus. Studies in Mycology, 50, 195-214.
24. Crous PW, Wingfield MJ, Mansilla JP, Alfenas AC, Groenewald JZ, (2006) Phylogenetic reassessment of Mycosphaerella spp. and their anamorphs occurring on Eucalyptus. II. Studies in Mycology, 55, 99-131.
25. Crous PW, Braun U, Groenewald JZ, (2007) Mycosphaerella is polyphyletic. Studies in Mycology, 58, 1-32.
26. Desprez-Loustau M-L, Robin C, Buée M, et al. (2007) The fungal dimension of biological invasions. Trends in Ecology & Evolution, 22, 472-480.
27. Dettman JR, Jacobson DJ, Turner E, Pringle A, Taylor JW, (2003) Reproductive isolation and phylogenetic divergence in Neurospora: comparing methods of species recognition in a model eukaryote. Evolution, 57, 2721-2741.
28. Dick M, (1982) Leaf-inhabiting fungi of eucalypts in New Zealand. New Zealand Journal of Forestry Science, 12, 525-537.
29. Dlugosch KM, Parker IM, (2007) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Molecular Ecology, 17, 431-449.
30. Dutech C, Fabreguettes O, Capdevielle X, Robin C, (2010) Multiple introductions of divergent genetic lineages in an invasive fungal pathogen, Cryphonectria parasitica, in France. Heredity, 105, 220-228.
31. Estoup A, Guillemaud T, (2010) Reconstructing routes of invasion using genetic data: why, how and so what? Molecular Ecology, 19, 4113-4130.
32. Evanno G, Regnaut S, Goudet J, (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology, 14, 2611-2620.
33. Excoffier L, Laval G, Schneider S, (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1, 47-50.
34. Ficetola GF, Bonin A, Miaud C, (2008) Population genetics reveals origin and number of founders in a biological invasion. Molecular Ecology, 17, 773-782.
35. Fry WE, Goodwin SB, Dyer AT, et al. (1993) Historical and recent migrations of Phytophthora infestans: chronology, pathways, and implications. Plant Disease, 77, 653-661.
36. Gilbert GS, (2002) Evolutionary ecology of plant diseases in natural ecosystems. Annual Review of Phytopathology, 40, 13-43.
37. Giraud T, Roxana Y, Lõpez-Villavicencio M, Refrégier G, Hood ME, (2008) Mating system of the anther smut fungus Microbotryum violaceum: selfing under heterothallism. Eukaryotic Cell, 7, 765-775.
38. Glass NL, Donaldson GC, (1995) Development of primer sets designed for use with PCR to amplify conserved genes from filamentous Ascomycetes. Applied and Environmental Microbiology, 61, 1323-1330.
39. Goodwin SB, Dunkle LD, Zismann VL, (2001) Phylogenetic analysis of Cercospora and Mycosphaerella based on the Internal Transcribed Spacer region of ribosomal DNA. Phytopathology, 91, 648-658.
40. Grünig CR, Brunner PC, Duà A, Sieber TN, (2007) Suitability of methods for species recognition in the Phialocephala fortinii-Acephala applanata species complex using DNA analysis. Fungal Genetics and Biology, 44, 773-788.
41. Grünwald NJ, Goodwin SB, Milgroom MG, Fry WE, (2003) Analysis of genotypic diversity data for populations of microorganisms. Phytopathology, 93, 738-746.
42. Hayden HL, Carlier J, Aitken EAB, (2003) Genetic structure of Mycosphaerella fijiensis populations from Australia, Papua New Guinea and the Pacific Islands. Plant Pathology, 52, 703-712.
43. Hunter GC, Cortinas MN, Wingfield BD, Crous PW, Wingfield MJ, (2006) Development of polymorphic microsatellite markers for the Eucalyptus leaf pathogen Mycosphaerella nubilosa. Molecular Ecology Notes, 6, 900-903.
44. Hunter GC, van der Merwe NA, Burgess TI, et al. (2008) Global movement and population biology of Mycosphaerella nubilosa infecting leaves of cold-tolerant Eucalyptus globulus and E. nitens. Plant Pathology, 57, 235-242.
45. Hunter GC, Crous PW, Carnegie AJ, Wingfield MJ, (2009) Teratosphaeria nubilosa, a serious leaf disease pathogen of Eucalyptus spp. in native and introduced areas. Molecular Plant Pathology, 10, 1-14.
46. Jackson SL, Maxwell A, Burgess TI, Hardy GES, Dell B, (2008) Incidence and new records of Mycosphaerella species within a Eucalyptus globulus plantation in Western Australia. Forest Ecology and Management, 255, 3931-3937.
47. Kolbe JJ, Glor RE, Rodriguez-Schettino L, et al. (2004) Genetic variation increases during biological invasion by a Cuban lizard. Nature, 4, 177-181.
48. Kumar S, Tamura K, Nei M, (2004) MEGA3: integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Briefings in Bioinformatics, 5, 150-163.
49. Lombaert E, Guillemaud T, Cornuet J-M, et al. (2010) Bridgehead effect in the worldwide invasion of the biocontrol harlequin ladybird. PLoS One, 5, e9743.
50. Lundquist JE, Purnell RC, (1987) Effects of Mycosphaerella leaf spot on growth of Eucalyptus nitens. Plant Disease, 71, 1025-1029.
51. Maxwell A, Hardy GESJ, Dell B, (2001) First record of Mycosphaerella nubilosa in Western Australia. Australasian Plant Pathology, 30, 65.
52. McDonald BA, Linde C, (2002) Pathogen population genetics, evolutionary potential, and durable resistance. Annual Review of Phytopathology, 40, 349-379.
53. Milgate AW, Vaillancourt RE, Mohammed C, Powell M, Potts BM, (2005) Genetic structure of a Mycosphaerella cryptica population. Australasian Plant Pathology, 34, 345-354.
54. Milgroom MG, (1996) Recombination and the multilocus structure of fungal populations. Annual Review of Phytopathology, 34, 457-477.
55. Miller MP, (2005) Alleles In Space: computer software for the joint analysis of interindividual spatial and genetic information. Journal of Heredity, 96, 722-724.
56. Mitchell CE, Blumenthal D, Jarosik V, Puckett EE, Pysek P, (2010) Controls on pathogen species richness in plants' introduced and native ranges: roles of residence time, range size and host traits. Ecology Letters, 13, 1525-1535.
57. Mohammed CL, Wardlaw T, Smith A, et al. (2003) Mycosphaerella leaf diseases of temperate eucalypts around the Southern Pacific Rim. New Zealand Journal of Forestry Science, 33, 362-372.
58. Nei M, (1973) Analysis of gene diversity in subdivided populations. Proceedings of the National Academy of Sciences of the USA, 70, 3321-3323.
59. Nei M, Maruyama T, Chakraborty R, (1975) The bottleneck effect and genetic variability in populations. Evolution, 29, 1-10.
60. Nichols JD, Smith RG, Grant J, Glencross K, (2010) Subtropical eucalypt plantations in eastern Australia. Australian Forestry, 73, 53-62.
61. O'Donnell K, Ward TJ, Geiser DM, Kistler HC, Aoki T, (2004) Genealogical concordance between the mating type locus and seven other nuclear genes supports formal recognition of nine phylogenetically distinct species within the Fusarium graminearum clade. Fungal Genetics and Biology, 41, 600-623.
62. O'Donnell K, Gueidan C, Sink S, et al. (2009) A two-locus DNA sequence database for typing plant and human pathogens within the Fusarium oxysporum species complex. Fungal Genetics and Biology, 46, 936-948.
63. Pavlic D, Slippers B, Coutinho TA, Wingfield MJ, (2009) Multiple gene genealogies and phenotypic data reveal cryptic species of the Botryosphaeriaceae: a case study on the Neofusicoccum parvum/N. ribis complex. Molecular Phylogenetics and Evolution, 51, 259-268.
64. Pérez G, (2010) Global Genetic Diversity of the Eucalyptus leaf Pathogen Teratosphaeria nubilosa species complex in native forests and commercial plantations. University of Pretoria, Pretoria, South Africa, p. 260.
65. Pérez G, Hunter GC, Slippers B, et al. (2009a) Teratosphaeria (Mycosphaerella) nubilosa, the causal agent of Mycosphaerella Leaf Disease (MLD), recently introduced into Uruguay. European Journal of Plant Pathology, 125, 109-118.
66. Pérez G, Slippers B, Wingfield BD, Finkenauer E, Wingfield MJ, (2009b) Mycosphaerella leaf disease (MLD) outbreak on Eucalyptus globulus in Brazil caused by Teratosphaeria (Mycosphaerella) nubilosa. Phytopathologia Mediterranea, 48, 302-306.
67. Pérez G, Slippers B, Wingfield BD, Hunter GC, Wingfield MJ, (2010) Micro- and macro spatial scale analyses illustrates mixed mating strategies and extensive geneflow in populations of an invasive haploid pathogen. Molecular Ecology, 19, 1801-1813.
68. Potts BM, Vaillancourt RE, Jordan G, et al. (2004) Exploration of the Eucalyptus globulus gene pool. Proceedings IUFRO Conference, 46-61.
69. Pritchard JK, Stephens M, Donnelly P, (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945-959.
70. Smart CD, Fry WE, (2001) Invasions by the late blight pathogen: renewed sex and enhanced fitness. Biological Invasions, 3, 235-243.
71. Stoddart JA, Taylor JF, (1988) Genotype diversity: estimation and prediction in samples. Genetics, 118, 705-711.
72. Stukenbrock EH, McDonald BA, (2008) The origins of plant pathogens in agro-ecosystems. Annual Review of Phytopathology, 46, 75-100.
73. Stukenbrock EH, Banke S, Javan-Nikkhah M, McDonald BA, (2007) Origin and domestication of the fungal wheat pathogen Mycosphaerella graminicola via sympatric speciation. Molecular Biology and Evolution, 24, 398-411.
74. Suarez AV, Tsutsui ND, (2008) The evolutionary consequences of biological invasions. Molecular Ecology, 17, 351-360.
75. Swofford DL, (2002) PAUP: Phylogenetic Analysis Using Parsimony (and Other Methods), Version 4.0b10. Sinauer Associates, Sunderland, Massachusetts.
76. Taylor JW, Fisher MC, (2003) Fungal multilocus sequence typing-it's not just for bacteria. Current Opinion in Microbiology, 6, 351-356.
77. Taylor JW, Jacobson DJ, Fisher MC, (1999) The evolution of asexual fungi: reproduction, speciation and classification. Annual Review of Phytopathology, 37, 197-246.
78. Taylor JW, Jacobson DJ, Kroken S, et al. (2000) Phylogenetic species recognition and species concepts in fungi. Fungal Genetics and Biology, 31, 21-32.
79. Taylor JW, Turner E, Townsend JP, Dettman JR, Jacobson D, (2006) Eukaryotic microbes, species recognition and the geographic limits of species: examples from the kingdom Fungi. Philosophical Transactions of the Royal Society Biology, 361, 1947-1963.
80. Tibbits WN, Boomsma DB, Jarvis S, (1997) Distribution, biology, genetics and improvement programs for Eucalyptus globulus and E. nitens around the world. In: Proceedings of the 24th Biennial Southern Tree Improvement Conference (eds White T, Huber D, Powell G). pp. 81?95. Southern Tree Improvement Committee, Orlando, Florida.
81. White TJ, Bruns T, Lee S, Taylor J, (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR Protocols: A Guide to Methods and Applications (eds, Innis MA, Gelfand DH, Snindky JJ, and, White TJ,), pp. 315-322. Academic Press, San Diego.
82. Wingfield MJ, (2003) Increasing threat of diseases to exotic plantation forests in the Southern Hemisphere: lessons from Cryphonectria canker. Australasian Plant Pathology, 32, 133-139.
83. Wingfield MJ, Slippers B, Hurley BP, et al. (2008) Eucalypt pests and diseases: growing threats to plantation productivity. Southern Forests, 70, 139-144.
84. Yeh FC, Yang RC, Boyle T, (1999) POPGENE. Version 1.31. Microsoft Windows Based Freeware for Population Genetic Analysis. Molecular Biology and Biotechnology Centre, University of Alberta, Canada (http://www.ualberta. ca~fyeh/popgene.html).
85. Zhan J, Pettway RE, McDonald BA, (2003) The global genetic structure of the wheat pathogen Mycosphaerella graminicola is characterized by high nuclear diversity, low mitochondrial diversity, regular recombination, and gene flow. Fungal Genetics and Biology, 38, 286-297.
86. Zhou X, Burgess TI, De Beer W, et al. (2007) High intercontinental migration rates and population admixture in the sapstain fungus Ophiostoma ips. Molecular Ecology, 16, 89-99.