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Fungal Diversity

, 50:145 | Cite as

Mycosphaerella and Teratosphaeria diseases of Eucalyptus; easily confused and with serious consequences

  • Gavin C. Hunter
  • Pedro W. Crous
  • Angus J. Carnegie
  • Treena I. Burgess
  • Michael J. Wingfield
Review

Abstract

The Mycosphaerella complex accommodates thousands of taxa. Many of these species are economically important plant pathogens, notably on native and commercially propagated Eucalyptus species where they cause a wide range of disease symptoms including leaf spot, leaf blotch, shoot blight and stem cankers. Some of these diseases represent major impediments to sustainable Eucalyptus forestry in several countries where infection by Mycosphaerella and Teratosphaeria species can result in reduction of wood volume and in severe cases tree death. Extensive research has been conducted on these disease complexes over the past 40 years. The incorporation of DNA-based molecular techniques has made it possible to define and to better understand the differences between the Mycosphaerella and Teratosphaeria species occurring on Eucalyptus. These studies have also enabled refinement of anamorph and teleomorph generic concepts for the genera and thus facilitated the more accurate identification of species. They have also promoted a more lucid understanding of the biology, life cycles, population biology and epidemiology of the most important pathogens in the group.

Keywords

Capnodiales Eucalyptus Mycosphaerellaceae Teratosphaeriaceae Tree diseases Leaf spots 

References

  1. Abd-Elsalam K, Bahkali AH, Moslem M, De Wit PJGM, Verreet JA (2011) Detection of Mycosphaerella graminicola in wheat leaves by a microsatellite dinucleotide specific-primer. Int J Mol Sci 12:682–693PubMedGoogle Scholar
  2. Andjic V, Barber PA, Carnegie AJ, Pegg GS, Hardy GEStJ, Wingfield MJ, Burgess TI (2007) Kirramyces viscidus sp. nov., a new eucalypt pathogen from tropical Australia closely related to the serious leaf pathogen, Kirramyces destructans. Australas Plant Pathol 36:478–487Google Scholar
  3. Andjic V, Pegg GS, Carnegie AJ, Callister A, Hardy GEStJ, Burgess T (2010a) Teratosphaeria pseudoeucalypti, new cryptic species responsible for leaf blight of Eucalyptus in subtropical and tropical Australia. Plant Pathol 59:900–912Google Scholar
  4. Andjic V, Whyte G, Hardy G, Burgess T (2010b) New Teratosphaeria species occurring on eucalypts in Australia. Fungal Divers 43:27–38Google Scholar
  5. Andjic V, Dell B, Barber P, Hardy G, Wingfield MJ, Burgess T (2011) Plants for planting; evidence for the movement of serious forest pathogens, Teratosphaeria destructans on infected germplasm. Eur J Plant Pathol. doi: 10.1007/s10658-011-9786-2
  6. Aptroot A (2006) Mycosphaerella and its anamorphs: 2. Conspectus of Mycosphaerella. CBS Biodivers Ser 5:1–231Google Scholar
  7. Arzanlou M, Abeln ECA, Kema GHJ, Waalwijk C, Carlier J, de Vries I, Guzman M, Crous PW (2007) Molecular diagnostics for the Sigatoka disease complex of banana. Phytopathol 97:1112–1118Google Scholar
  8. Barber PA, Smith IW, Keane PJ (2003) Foliar diseases of Eucalyptus spp. grown for ornamental cut foliage. Australas Plant Pathol 32:109–111Google Scholar
  9. 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. Australas Plant Pathol 37:472–481Google Scholar
  10. Bensch K, Groenewald JZ, Dijksterhuis J, Starink-Willemse M, Andersen B, Summerell BA, Shin H-D, Dugan FM, Schroers H-J, Braun U, Crous PW (2010) Species and ecological diversity within the Cladosporium cladosporioides complex (Davidiellaceae, Capnodiales). Stud Mycol 67:1–94PubMedGoogle Scholar
  11. Beresford RM (1978) Mycosphaerella nubilosa (Cooke) Hansf. on Eucalyptus delegatensis R. T. Baker: further studies of the epidemiology in the North island of New Zealand. Dissertation, University of AucklandGoogle Scholar
  12. Boeger JM, Chen RS, McDonald BA (1993) Gene flow between geographic populations of Mycosphaerella graminicola (Anamorph Septori tritici) detected with restriction fragment length polymorphism markers. Phytopathol 83:1148–1154Google Scholar
  13. Braun U (1990) Taxonomic problems of the Ramularia/Cercosporella complex. Stud Mycol 32:65–75Google Scholar
  14. Braun U (2001) Taxonomic notes on some species of the Cercospora complex (VII). Fungal Divers 8:41–71Google Scholar
  15. Braun U, Dick MA (2002) Leaf spot diseases of eucalyptus in New Zealand caused by Pseudocercospora species. N Z J For Sci 32:221–234Google Scholar
  16. Braun U, Crous PW, Dugan F, Groenewald JZ, de Hoog GS (2003) Phylogeny and taxonomy of Cladosporium-like hyphomycetes, including Davidiella gen. nov., the teleomorph of Cladosporium s. str. Mycol Prog 2:3–18Google Scholar
  17. Brown BN, Ferreira FA (2000) Diseases during propagation of eucalypts. In: Keane PJ, Kile GA, Podger FD, Brown BN (eds) Diseases and pathogens of Eucalypts. CSIRO Publishing, Melbourne, pp 119–151Google Scholar
  18. Burgess TI, Andjic V, Hardy GEStJ, Dell B, Xu Dong Z (2006) First report of Phaeophleospora destructans in China. J Trop For Sci 18:144–146Google Scholar
  19. Burgess TI, Barber PA, Sufaati S, Xu D, Hardy GEStJ, Dell B (2007a) Mycosphaerella spp. on Eucalyptus in Asia; new species; new hosts and records. Fungal Divers 24:135–157Google Scholar
  20. Burgess TI, Andjic V, Wingfield MJ, Hardy GEStJ (2007b) The eucalypt leaf blight pathogen Kirramyces destructans discovered in Australia. Australas Plant Dis Notes 2:141–144Google Scholar
  21. Carlier J, Lebrun MH, Zapater MF, Dubois C, Mourichon X (1996) Genetic structure of the global population of banana black streak fungus, Mycosphaerella fijiensis. Mol Ecol 5:499–510Google Scholar
  22. Carnegie AJ (2000) A study of the species of Mycosphaerella on eucalypts in Australia and the impact of Mycosphaerella leaf diseases on Eucalyptus globulus Labill. University of Melbourne, PhD DissertationGoogle Scholar
  23. Carnegie AJ (2007a) Forest health condition in New South Wales, Australia, 1996–2005. I. Fungi recorded from eucalypt plantations during forest health surveys. Australas Plant Pathol 36:213–224Google Scholar
  24. 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. Australas Plant Pathol 36:225–239Google Scholar
  25. Carnegie AJ, Ades PK (2002) The proportion of leaf spots caused by Mycosphaerella cryptica and M. nubilosa on Eucalyptus globulus, E. nitens and their F1 hybrids in a family trial in Tasmania, Australia. Australas Mycol 21:53–63Google Scholar
  26. Carnegie AJ, Ades PK (2003) Mycosphaerella leaf disease reduces growth of plantation-grown Eucalyptus globulus. Aust For 66:113–119Google Scholar
  27. Carnegie AJ, Ades PK (2005) Variation in Eucalyptus globulus Labill. and E. nitens Dean and Maiden in susceptibility of adult foliage to disease caused by Mycosphaerella cryptica (Cooke) Hansf. Silvae Genet 54:174–184Google Scholar
  28. Carnegie AJ, Keane PJ (1994) Further Mycosphaerella species associated with leaf diseases of Eucalyptus. Mycol Res 98:413–418Google Scholar
  29. Carnegie AJ, Keane PJ (1997) A revised Mycosphaerella gregaria nom. nov. for M. aggregata on Eucalyptus. Mycol Res 101:843–844Google Scholar
  30. Carnegie AJ, Keane PJ (1998) Mycosphaerella vespa sp. nov. from diseased Eucalyptus leaves in Australia. Mycol Res 102:1274–1276Google Scholar
  31. Carnegie AJ, Keane PJ, Ades PK, Smith IW (1994) Variation in susceptibility of Eucalyptus globulus provenances to Mycosphaerella leaf disease. Can J For Res 24:1751–1757Google Scholar
  32. Carnegie AJ, Keane PJ, Podger FD (1997) The impact of three species of Mycosphaerella newly recorded on Eucalyptus in Western Australia. Australas Plant Pathol 26:71–77Google Scholar
  33. Carnegie AJ, Ades PK, Keane PJ, Smith IW (1998) Mycosphaerella diseases of juvenile foliage in a eucalypt species and provenance trial in Victoria, Australia. Aust For 61:190–194Google Scholar
  34. Carnegie AJ, Johnson IG, Henson M (2004) Variation among provenances and families of blackbutt (Eucalyptus pilularis) in early growth and susceptibility to damage from leaf spot fungi. Can J For Res 34:2314–2326Google Scholar
  35. Carnegie AJ, Burgess TI, Beilharz V, Wingfield MJ (2007) New species of Mycosphaerella from Myrtaceae in plantations and native forests in eastern Australia. Mycologia 99:461–474PubMedGoogle Scholar
  36. Carnegie AJ, Pegg GS, White D, Burgess TI (2011) Species of Mycosphaerellaceae and Teratosphaeriaceae from eucalypts in eastern Australia. Australas Plant Pathol. doi: 10.1007/s13313-13011-10049-13317
  37. Cheah LH (1977) Aerobiology and epidemiology of Mycosphaerella nubilosa (Cooke) Hansf. in Eucalyptus spp. Dissertation, University of AucklandGoogle Scholar
  38. Cheah LH, Hartill WFT (1987) Ascospore release in Mycosphaerella cryptica (Cooke) Hansford. Eur J For Pathol 17:129–141Google Scholar
  39. Cheewangkoon R, Crous PW, Hyde KD, Groenewald JZ, To-anan C (2008) Species of Mycosphaerella and related anamorphs on Eucalyptus leaves from Thailand. Persoonia 21:77–91PubMedGoogle Scholar
  40. Cheewangkoon R, Groenewald JZ, Summerell BA, Hyde KD, To-anun C, Crous PW (2009) Myrtaceae, a cache of fungal biodiversity. Persoonia 23:55–85PubMedGoogle Scholar
  41. Chen S, Barnes I, Chungu D, Roux J, Wingfield MJ, Xie Y, Zhou X (2011) High population diversity and increasing importance of the Eucalyptus stem canker pathogen, Teratosphaeria zuluensis, in South China. Australas Plant Pathol. doi: 10.1007/sl3313-011-0051-0
  42. Corlett M (1991) An annotated list of the published names in Mycosphaerella and Sphaerella. Mycol Mem 18:1–328Google Scholar
  43. Corlett M (1995) An annotated list of the published names in Mycosphaerella and Sphaerella: corrections and additions. Mycotaxon 53:37–56Google Scholar
  44. Cortinas MN, Barnes I, Wingfield BD, Wingfield MJ (2006a) Polymorphic microsatellite markers for the Eucalyptus fungal pathogen Colletogloeopsis zuluensis. Mol Ecol Notes 6:780–783Google Scholar
  45. Cortinas MN, Burgess T, Dell B, Xu D, Crous PW, Wingfield BD, Wingfield MJ (2006b) First record of Colletogloeopsis zuluense comb. nov., causing a stem canker of Eucalyptus in China. Mycol Res 110:229–236PubMedGoogle Scholar
  46. Cortinas MN, Crous PW, Wingfield BD, Wingfield MJ (2006c) Multi-gene phylogenies and phenotypic characters distinguish two species within the Colletogloeopsis zuluensis complex associated with Eucalyptus stem cankers. Stud Mycol 55:133–146PubMedGoogle Scholar
  47. Cortinas MN, Barnes I, Wingfield MJ, Wingfield BD (2010) Genetic diversity in the Eucalyptus stem pathogen Teratosphaeria zuluensis. Australas Plant Pathol 39:383–393Google Scholar
  48. Crous PW (1998) Mycosphaerella species and their anamorphs associated with leaf spot diseases of Eucalyptus. Mycol Mem 21:1–170Google Scholar
  49. Crous PW (2009) Taxonomy and phylogeny of the genus Mycosphaerella and its anamorphs. Fungal Divers 38:1–24Google Scholar
  50. Crous PW, Alfenas AC (1995) Mycosphaerella gracilis and other species of Mycosphaerella associated with leaf spots of Eucalyptus in Indonesia. Mycologia 87:121–126Google Scholar
  51. Crous PW, Groenewald JZ (2005) Hosts, species and genotypes: opinions versus data. Australas Plant Pathol 34:463–470Google Scholar
  52. Crous PW, Swart WJ (1995) Foliicolous fungi of Eucalyptus spp. from Eastern Madagascar: Implications for South Africa. S Afr For J 172:1–5Google Scholar
  53. Crous PW, Wingfield MJ (1996) Species of Mycosphaerella and their anamorphs associated with leaf blotch disease of Eucalyptus in South Africa. Mycologia 88:441–458Google Scholar
  54. Crous PW, Wingfield MJ (1997a) Colletogloeopsis, a new coelomycete genus to accommodate anamorphs of two species of Mycosphaerella on Eucalyptus. Can J Bot 75:667–674Google Scholar
  55. Crous PW, Wingfield MJ (1997b) New species of Mycosphaerella occurring on Eucalyptus leaves in Indonesia and Africa. Can J Bot 75:781–790Google Scholar
  56. Crous PW, Knox-Davies PS, Wingfield MJ (1988) Phaeoseptoria eucalypti and Coniothyrium ovatum on Eucalyptus spp. in South Africa. Phytophylactica 20:337–340Google Scholar
  57. Crous PW, Knox-Davies PS, Wingfield MJ (1989a) A summary of fungal leaf pathogens of Eucalyptus and the diseases they cause in South Africa. S Afr For J 149:9–16Google Scholar
  58. Crous PW, Wingfield MJ, Marasas WFO, Sutton BC (1989b) Pseudocercospora eucalyptorum sp. nov. on Eucalyptus leaves. Mycol Res 93:394–398Google Scholar
  59. Crous PW, Wingfield MJ, Park RF (1991) Mycosphaerella nubilosa a synonym of M. molleriana. Mycol Res 95:628–632Google Scholar
  60. Crous PW, Ferreira FA, Alfenas A, Wingfield MJ (1993a) Mycosphaerella suberosa associated with corky leaf spots on Eucalyptus in Brazil. Mycologia 85:705–710Google Scholar
  61. Crous PW, Wingfield MJ, Ferreira FA, Alfenas A (1993b) Mycosphaerella parkii and Phyllosticta eucalyptorum, two new species from Eucalyptus leaves in Brazil. Mycol Res 97:582–584Google Scholar
  62. Crous PW, Wingfield MJ, Mohammed C, Yuan ZQ (1998) New foliar pathogens of Eucalyptus from Australia and Indonesia. Mycol Res 102:527–532Google Scholar
  63. Crous PW, Hong L, Wingfield MJ, Wingfield B, Kang JC (1999) Uwebraunia and Dissoconium, two morphologically similar anamorph genera with different teleomorph affinities. Sydowia 51:155–166Google Scholar
  64. Crous PW, Aptroot A, Kang J-C, Braun U, Wingfield MJ (2000) The genus Mycosphaerella and its anamorphs. Stud Mycol 45:107–121Google Scholar
  65. Crous PW, Kang J, Braun U (2001) A phylogenetic redefinition of anamorph genera in Mycosphaerella based on ITS rDNA sequence and morphology. Mycologia 93:1081–1101Google Scholar
  66. Crous PW, Groenewald JZ, Wingfield MJ, Aptroot A (2003) The value of ascospore septation in separating Mycosphaerella from Sphaerulina in the Dothideales: A Saccardoan myth? Sydowia 55:136–152Google Scholar
  67. Crous PW, Groenewald JZ, Mansilla JP, Hunter GC, Wingfield MJ (2004) Phylogenetic reassessment of Mycosphaerella spp. and their anamorphs occurring on Eucalyptus. Stud Mycol 50:195–214Google Scholar
  68. Crous PW, Wingfield MJ, Mansilla JP, Alfenas AC, Groenewald JZ (2006) Phylogenetic reassessment of Mycosphaerella spp. and their anamorphs occurring on Eucalyptus. II. Stud Mycol 55:99–131PubMedGoogle Scholar
  69. Crous PW, Braun U, Groenewald JZ (2007a) Mycosphaerella is polyphyletic. Stud Mycol 58:1–32PubMedGoogle Scholar
  70. Crous PW, Summerell BA, Carnegie AJ, Mohammed C, Himaman W, Groenewald JZ (2007b) Foliicolous Mycosphaerella spp. and their anamorphs on Corymbia and Eucalyptus. Fungal Divers 26:143–185Google Scholar
  71. Crous PW, Summerell BA, Mostert L, Groenewald JZ (2008) Host specificity and speciation of Mycosphaerella and Teratosphaeria species associated with leaf spots of Proteaceae. Persoonia 20:59–86PubMedGoogle Scholar
  72. Crous PW, Groenewald JZ, Summerell BA, Wingfield BD, Wingfield MJ (2009a) Co-occurring species of Teratosphaeria on Eucalyptus. Persoonia 22:38–48PubMedGoogle Scholar
  73. Crous PW, Schoch CL, Hyde KD, Wood AR, Gueidan C, de Hoog GS, Groenewald JZ (2009b) Phylogenetic lineages in the Capnodiales. Stud Mycol 64:17–47PubMedGoogle Scholar
  74. Crous PW, Summerell BA, Carnegie AJ, Wingfield MJ, Groenewald JZ (2009c) Novel species of Mycosphaerellaceae and Teratosphaeriaceae. Persoonia 23:119–146PubMedGoogle Scholar
  75. Crous PW, Summerell BA, Carnegie AJ, Wingfield MJ, Hunter GC, Burgess TI, Andjic V, Barber PA, Groenewald JZ (2009d) Unravelling Mycosphaerella: do you believe in genera. Persoonia 23:99–118PubMedGoogle Scholar
  76. Crous PW, Wingfield MJ, Groenewald JZ (2009e) Niche sharing reflects a poorly understood biodiversity phenomenon. Persoonia 22:83–94PubMedGoogle Scholar
  77. Crous PW, Groenewald JZ, Shivas RG, Edwards J, Seifert KA, Alfenas AC, Alfenas RF, Burgess TI, Carnegie AJ, Hardy GEStJ, Hiscock N, Huberli D, Jung T, Louis-Seize G, Okada G, Pereira OL, Stukely MJC, Wang W, White GP, Young AJ, McTaggart AR, Pascoe IG, Porter IJ, Quadvlieg W (2011a) Fungal planet description sheets: 69–91. Persoonia 26:108–156Google Scholar
  78. Crous PW, Tanaka K, Summerell BA, Groenewald JZ (2011b) Additions to the Mycosphaerella complex. IMA Fungus 2:49–64Google Scholar
  79. Dick M (1982) Leaf inhabiting fungi of eucalypts in New Zealand. N Z J For Sci 12:525–537Google Scholar
  80. Dick MA, Dobbie K (2001) Mycosphaerella suberosa and M. intermedia sp. nov. on Eucalyptus in New Zealand. N Z J Bot 39:269–276Google Scholar
  81. Dick M, Gadgil PD (1983) Eucalyptus leaf spots. Forest Pathology in New Zealand No. 1. Forest Research Institute, RotoruaGoogle Scholar
  82. Dungey HS, Potts BM, Carnegie AJ, Ades PK (1997) Mycosphaerella leaf disease: genetic variation in damage to Eucalyptus nitens, Eucalyptus globulus, and their F1 hybrid. Can J For Res 27:750–759Google Scholar
  83. Elders (2010) Completion and outcome of Forestry Asset Review. http://www.eldersforestry.com.au/mediaCentre/news/article.php?newsID=86
  84. Elliott HJ, Ohmart CP, Wylie FR (1998) Insect pests of Australian forests: ecology and management. Inkata Press, AustraliaGoogle Scholar
  85. FAO (2007) State of the worlds forests 2007. Food and Agricultural Organisation of the United Nations, RomeGoogle Scholar
  86. Feau N, Hamelin RC, Vandecasteele C, Stanosz GR, Bernier L (2005) Genetic structure of Mycosphaerella populorum (anamorph Septoria musiva) populations in North-Central and North-eastern North America. Phytopathology 95:608–616PubMedGoogle Scholar
  87. Gadgil PD, Dick M (1983) Fungi eucalyptorum Novozelandiae: Septoria pulcherima sp. nov. and Trimmatostroma bifarium sp. nov. N Z J Bot 21:49–52Google Scholar
  88. Gadgil PD, Wardlaw TJ, Ferreira FA, Sharma JK, Dick MA, Wingfield MJ, Crous PW (2000) Management of disease in eucalypt plantations. In: Keane PJ, Kile GA, Podger FD, Brown BN (eds) Diseases and pathogens of Eucalypts. CSIRO Publishing, Melbourne, pp 519–529Google Scholar
  89. Gezahgne A, Roux J, Wingfield MJ (2003) Diseases of exotic Eucalyptus and Pinus species in Ethiopian plantations. S Afr J Sci 99:29–33Google Scholar
  90. Gezahgne A, Roux J, Hunter GC, Wingfield MJ (2006) Mycosphaerella species associated with leaf diseases of Eucalyptus globulus in Ethiopia. For Pathol 36:253–263Google Scholar
  91. Gilmour JW (1966) The pathology of forest trees in New Zealand. The fungal, bacterial, and algal pathogens. Technical paper No. 48. New Zealand Forest Service, WellingtonGoogle Scholar
  92. Glen M, Smith AH, Langrell SRH, Mohammed CL (2007) Development of nested polymerase chain reaction detection of Mycosphaerella spp. and its application to the study of leaf disease in Eucalyptus plantations. Phytopathology 97:132–144PubMedGoogle Scholar
  93. Guo JR, Schneider F, Vereet JA (2006) Presymptomatic and quantitative detection of Mycosphaerella graminicola development in wheat using real-time PCR assay. FEMS Microbiol Let 262:223–229Google Scholar
  94. Hayden HL, Carlier J, Aitken EAB (2003a) Genetic structure of Mycosphaerella fijiensis populations from Australia, Papua New Guinea and the Pacific Islands. Plant Pathol 52:703–712Google Scholar
  95. Hayden HL, Carlier J, Aitken EAB (2003b) Population differentiation in the banana leaf spot pathogen Mycosphaerella musicola, examined at a global scale. Plant Pathol 52:713–719Google Scholar
  96. Hood IA, Alexander N (2006) A survey of Septoria leaf blight. N Z Tree Grower 27:36–39Google Scholar
  97. Hood IA, Gardner JF, Kimberley MO, Molony KI (2002) Variation among eucalypt species in early susceptibility to the leaf spot fungi Phaeophleospora eucalypti and Mycosphaerella spp. N Z J For Sci 32:235–255Google Scholar
  98. Hunter GC, Crous PW, Roux J, Wingfield BD, Wingfield MJ (2004a) Identification of Mycosphaerella species associated with Eucalyptus nitens leaf defoliation in South Africa. Australas Plant Pathol 33:349–355Google Scholar
  99. Hunter GC, Roux J, Wingfield BD, Crous PW, Wingfield MJ (2004b) Mycosphaerella species causing leaf disease in South African Eucalyptus plantations. Mycol Res 108:672–681PubMedGoogle Scholar
  100. Hunter GC, Cortinas MN, Wingfield BD, Crous PW, Wingfield MJ (2006a) Development of polymorphic microsatellite markers for the Eucalyptus leaf pathogen Mycosphaerella nubilosa. Mol Ecol Notes 6:900–903Google Scholar
  101. Hunter GC, Wingfield BD, Crous PW, Wingfield MJ (2006b) A multi-gene phylogeny for species of Mycosphaerella occurring on Eucalyptus leaves. Stud Mycol 55:147–161PubMedGoogle Scholar
  102. Hunter GC, van der Merwe NA, Burgess TI, Carnegie AJ, Wingfield BD, Crous PW, Wingfield MJ (2008) Global movement and population biology of Mycosphaerella nubilosa infecting leaves of cold-tolerant Eucalyptus globulus and E. nitens. Plant Pathol 57:235–242Google Scholar
  103. Hunter GC, Crous PW, Carnegie AJ, Wingfield MJ (2009) Teratosphaeria nubilosa, a serious leaf disease pathogen of Eucalyptus spp. in native and introduced areas. Mol Plant Pathol 10:1–14PubMedGoogle Scholar
  104. Jackson SL, Maxwell A, Dell B, Hardy GEStJ (2005) New records of Mycosphaerella leaf disease from Eucalypts in Western Australia. Australas Plant Pathol 34:423–424Google Scholar
  105. Jackson SL, Maxwell A, Burgess TI, Hardy GEStJ, Dell B (2008) Incidence and new records of Mycosphaerella species within a Eucalyptus globulus plantation in Western Australia. For Ecol Manag 255:3931–3937Google Scholar
  106. Keane PJ, Kile GA, Podger FD, Brown BN (2000) Diseases and pathogens of Eucalypts. CSIRO Publishing, AustraliaGoogle Scholar
  107. Kularatne HAGC, Lawrie AC, Barber PA, Keane PJ (2004) A specific primer PCR and RFLP assay for the rapid detection and differentiation in planta of some Mycosphaerella species associated with foliar diseases of Eucalyptus globulus. Mycol Res 108:1476–1493PubMedGoogle Scholar
  108. Ladiges PY (1997) Phylogenetic history and classification of eucalypts. In: Williams J, Woinarski J (eds) Eucalypt ecology: individuals to ecosystems. Cambridge University Press, Cambridge, pp 16–29Google Scholar
  109. Linde CC, Zhan J, McDonald BA (2002) Population structure of Mycosphaerella graminicola: from lesions to continents. Phytopathology 92:946–955PubMedGoogle Scholar
  110. Lundquist JE, Purnell RC (1987) Effects of Mycosphaerella leaf spot on growth of Eucalyptus nitens. Plant Dis 71:1025–1029Google Scholar
  111. Marks GC, Fuhrer BA, Walters NEM (1982) Tree diseases in Victoria. Forest Commission Victoria Handbook No. 1. Forest Commision, MelbourneGoogle Scholar
  112. Maxwell A, Hardy GEStJ, Dell B (2001) First record of Mycosphaerella nubilosa in Western Australia. Australas Plant Pathol 30:65Google Scholar
  113. Maxwell A, Dell B, Neumeister-Kemp G, Hardy GEStJ (2003) Mycosphaerella species associated with Eucalyptus in south-western Australia: new species, new records and a key. Mycol Res 107:351–359PubMedGoogle Scholar
  114. Maxwell A, Jackson SL, Dell B, Hardy GEStJ (2005) PCR-identification of Mycosphaerella species associated with leaf diseases of Eucalyptus. Mycol Res 109:992–1004PubMedGoogle Scholar
  115. McDonald BA (1997) The population genetics of fungi: tools and techniques. Phytopathology 87:448–453PubMedGoogle Scholar
  116. Milgate AW, Yuan ZQ, Vaillancourt RE, Mohammed C (2001) Mycosphaerella species occurring on Eucalyptus globulus and Eucalyptus nitens plantations of Tasmania, Australia. For Pathol 31:53–63Google Scholar
  117. Milgate AW, Potts BM, Joyce K, Mohammed C, Vaillancourt RE (2005a) Genetic variation in Eucalyptus globulus for susceptibility to Mycosphaerella nubilosa and its association with tree growth. Australas Plant Pathol 34:11–18Google Scholar
  118. Milgate AW, Vaillancourt RE, Mohammed C, Powell M, Potts BM (2005b) Genetic structure of a Mycosphaerella cryptica population. Australas Plant Pathol 34:345–354Google Scholar
  119. Mohammed C, Wardlaw T, Smith A, Pinkard E, Battaglia M, Glen M, Tommerup I, Potts B, Vaillancourt R (2003) Mycosphaerella leaf diseases of temperate eucalypts around the southern pacific rim. N Z J For Sci 33:362–372Google Scholar
  120. Old KM, Davison EM (2000) Canker diseases of eucalypts. In: Keane PJ, Kile GA, Podger FD, Brown BN (eds) Diseases and pathogens of Eucalypts. CSIRO Publishing, Australia, pp 241–253Google Scholar
  121. Old KM, Wingfield MJ, Yuan ZQ (2003) A manual of diseases of Eucalypts in South-East Asia. Centre for International Forestry Research, IndonesiaGoogle Scholar
  122. Otero L, Aguin O, Sainz MJ, Mansilla P (2007a) Incidencia y severidad de la enfermedad foliar causada por Mycosphaerella spp. en Eucaliptales de galicia. Bol del Cideu 4:3–8Google Scholar
  123. Otero L, Aguin O, Sainz MJ, Mansilla JP (2007b) El género Mycosphaerella en plantaciones de Eucalyptus en Galicia. Bol Sanid Veg Plagas 33:503–516Google Scholar
  124. Park RF (1988) Epidemiology of Mycosphaerella nubilosa and M. cryptica on Eucalyptus spp. in south-eastern Australia. Trans Br Mycol Soc 91:261–266Google Scholar
  125. Park RF, Keane PJ (1982a) Three Mycosphaerella species from leaf diseases of Eucalyptus. Trans Br Mycol Soc 79:95–100Google Scholar
  126. Park RF, Keane PJ (1982b) Leaf diseases of Eucalyptus associated with Mycosphaerella species. Trans Br Mycol Soc 79:101–115Google Scholar
  127. Park RF, Keane PJ (1984) Further Mycosphaerella species causing leaf diseases of Eucalyptus. Trans Br Mycol Soc 83:93–105Google Scholar
  128. Park RF, Keane PJ, Wingfield MJ, Crous PW (2000) Fungal diseases of Eucalypt foliage. In: Keane PJ, Kile GA, Podger FD, Brown BN (eds) Diseases and pathogens of Eucalypts. CSIRO publishing, Australia, pp 153–230Google Scholar
  129. Pegg G, Brown B, Ivory MH (2003) Eucalypt diseases in hardwood plantations in Queensland. Hardwoods Queensland Report No. 16, Forestry Research, Agency for Food and Fibre Sciences, Queensland DPI, Indooroopilly, QueenslandGoogle Scholar
  130. Perez CA, Wingfield MJ, Altier NA, Blanchette RA (2009a) Mycosphaerellaceae and Teratosphaeriaceae associated with Eucalyptus leaf diseases and stem cankers in Uruguay. For Pathol 39:349–360Google Scholar
  131. Perez G, Hunter GC, Slippers B, Perez C, Wingfield BD, Wingfield MJ (2009b) Teratosphaeria (Mycosphaerella) nubilosa, the causal agent of Mycosphaerella leaf disease (MLD), recently introduced into Uruguay. Eur J Plant Pathol 125:109–118Google Scholar
  132. Perez G, Slippers B, Wingfield BD, Finkenauer E, Wingfield MJ (2009c) Mycosphaerella Leaf Disease (MLD) outbreak on Eucalyptus globulus in Brazil caused by Teratosphaeria (Mycosphaerella) nubilosa. Phytopathol Mediterr 48:302–306Google Scholar
  133. Perez G, Slippers B, Wingfield BD, Hunter GC, Wingfield MJ (2010) Micro and macro spatial scale analyses illustrates mixed mating strategies and extensive gene flow in populations of an invasive haploid pathogen. Mol Ecol 9:1801–1813Google Scholar
  134. Pinkard EA, Mohammed CL (2006) Photosynthesis of Eucalyptus globulus with Mycosphaerella leaf disease. New Phytol 170:119–127PubMedGoogle Scholar
  135. Potts BM, Pederick LA (2000) Morphology, phylogeny, origin, distribution and genetic diversity of Eucalypts. In: Keane PJ, Kile GA, Podger FD, Brown BN (eds) Diseases and pathogens of Eucalypts. CSIRO publishing, Australia, pp 11–34Google Scholar
  136. Poynton RJ (1979) Tree planting in Southern Africa, vol. 2. The Eucalypts. Department of Forestry, South AfricaGoogle Scholar
  137. Purnell RC, Lundquist JE (1986) Provenance variation of Eucalyptus nitens on the Eastern Transvaal Highveld in South Africa. S Afr For J 138:23–31Google Scholar
  138. Quaedvlieg W, Kema GHJ, Groenewald JZ, Verkley GJM, Seifbarghi S, Razavi M, Mirzadi Gohari A, Mehrabi R, Crous PW (2011) Zymoseptoria gen. nov.: a new genus to accommodate Septoria-like species occurring on graminicolous hosts. Persoonia 26:57–69Google Scholar
  139. Rockwood DL, Rudie AW, Ralph SA, Zhu JY, Winandy JE (2008) Energy product options for Eucalyptus species grown as short rotation woody crops. Int J Mol Sci 9:1361–1378PubMedGoogle Scholar
  140. Roux J, Meke G, Kanyi B, Mwangi L, Mbaga A, Hunter GC, Nakabonge G, Heath RN, Wingfield MJ (2005) Diseases of plantation forestry trees in Eastern and Southern Africa. S Afr J Sci 101:409–413Google Scholar
  141. Schoch CL, Shoemaker RA, Seifert KA, Hambleton S, Spatafora JW, Crous PW (2006) A multigene phylogeny of the Dothideomycetes using four nuclear loci. Mycologia 98:1041–1052PubMedGoogle Scholar
  142. Schubert K, Groenewald JZ, Braun U, Dijksterhuis J, Starink M, Hill CF, Zalar P, de Hoog GS, Crous PW (2007) Biodiversity in the Cladosporium herbarum complex (Davidiellaceae, Capnodiales), with standardisation of methods for Cladosporium taxonomy and diagnostics. Stud Mycol 58:105–156PubMedGoogle Scholar
  143. Silva M, Valente C, Neves L (2008) Evaluation of Mycosphaerella impact on eucalypts plantations in Portugal. Rev Ciênc Agrár 31:112–118Google Scholar
  144. Silva M, Machado H, Phillips AJL (2009) Mycosphaerella species occurring on Eucalyptus globulus in Portugal. Eur J Plant Pathol 125:425–433Google Scholar
  145. Simon UK, Groenewald JZ, Crous PW (2009) Cymadothea trifolii, an obligate biotrophic leaf parasite of Trifolium, belongs to Mycosphaerellaceae as shown by nuclear ribosomal DNA analyses. Persoonia 22:49–55PubMedGoogle Scholar
  146. Slippers B, Stenlid J, Wingfield MJ (2005) Emerging pathogens: fungal host jumps following anthropogenic introduction. Trends Ecol Evol 20:420–421PubMedGoogle Scholar
  147. Smith AH, Gill WM, Pinkard EA, Mohammed CL (2007) Anatomical and histochemical defence responses induced in juvenile leaves of Eucalyptus globulus and Eucalyptus nitens by Mycosphaerella infection. For Pathol 37:361–373Google Scholar
  148. Summerell BA, Groenewald JZ, Carnegie AJ, Summerbell RC, Crous PW (2006) Eucalyptus microfungi known from culture. 2. Alysidiella, Fusculina and Phlogicylindrium genera nova, with notes on some other poorly known taxa. Fungal Divers 23:323–350Google Scholar
  149. Taylor JE, Crous PW, Palm ME (2001) Foliar and stem fungal pathogens of Proteaceae in Hawaii. Mycotaxon 78:449–490Google Scholar
  150. Taylor KM, Barber PA, Hardy GEStJ, Burgess TI (2011) Isolation and characterisation of polymorphic microsatellite loci in Teratosphaeria cryptica, a destructive foliar pathogen of Eucalyptus spp. Mol Ecol Resour 11:418–421PubMedGoogle Scholar
  151. Tejedor C (2007) Seleccion de una variedad clonal de Eucalyptus globulus ssp. globulus tolerante a la enfermedad foliar Mycosphaerella sp. en el norte de espana. Bol del Cideu 3:57–66Google Scholar
  152. Turnbull JW (2000) Economic and social importance of eucalypts. In: Keane PJ, Kile GA, Podger FD, Brown BN (eds) Diseases and pathogens of Eucalypts. CSIRO Publishing, Australia, pp 1–9Google Scholar
  153. Verkley GJM, Priest MJ (2000) Septoria and similar coelomycetous anamorphs of Mycosphaerella. Stud Mycol 45:123–128Google Scholar
  154. Verkley GJM, Crous PW, Groenewald JZ, Braun U, Aptroot A (2004) Mycosphaerella punctiformis revisited: morphology, phylogeny, and epitypification of the type species of the genus Mycosphaerella (Dothideales, Ascomycota). Mycol Res 108:1271–1282PubMedGoogle Scholar
  155. von Arx JA (1983) Mycosphaerella and its anamorphs. Proc K Ned Akad Wet Ser C 86:15–54Google Scholar
  156. Walker J, Sutton BC, Pascoe IG (1992) Phaeoseptoria eucalypti and similar fungi on Eucalyptus, with description of Kirramyces gen. nov. (Coelomycetes). Mycol Res 96:911–924Google Scholar
  157. Weston GC (1957) Exotic trees in New Zealand. Statement prepared for the 7th British Commonwealth Forestry Conference, Australia and New ZealandGoogle Scholar
  158. Whyte G, Burgess TI, Barber PA, Hardy GEStJ (2005) First record of Mycosphaerella heimii in Australia. Australas Plant Pathol 34:605–606Google Scholar
  159. Wingfield MJ (1999) Pathogens in exotic plantation forestry. Int For Rev 1:163–168Google Scholar
  160. Wingfield MJ (2003) Increasing threat of diseases to exotic plantation forests in the Southern Hemisphere: lesson from Cryphonectria canker. Australas Plant Pathol 32:133–139Google Scholar
  161. Wingfield MJ, Crous PW, Peredo HL (1995) A preliminary, annotated list of foliar pathogens of Eucalyptus spp. in Chile. S Afr For J 173:53–57Google Scholar
  162. Wingfield MJ, Crous PW, Boden D (1996a) Kirramyces destructans sp. nov., a serious leaf pathogen of Eucalyptus in Indonesia. S Afr J Bot 62:325–327Google Scholar
  163. Wingfield MJ, Crous PW, Coutinho TA (1996b) A serious new canker disease of Eucalyptus in South Africa caused by a new species of Coniothyrium. Mycopathologia 136:139–145PubMedGoogle Scholar
  164. Wingfield MJ, Roux J, Coutinho T, Govender P, Wingfield BD (2001) Plantation disease and pest management in the next century. S Afr For J 190:67–71Google Scholar
  165. Wingfield MJ, Slippers B, Hurley BP, Coutinho TA, Wingfield BD, Roux J (2008) Eucalypt pests and diseases: growing threats to plantation productivity. South For 70:139–144Google Scholar
  166. Wingfield MJ, Slippers B, Wingfield BD (2010) Novel associations between pathogens, insects and tree species threaten world forests. NZ J For Sci 40:S95–S103Google Scholar
  167. Zhan J, McDonald BA (2004) The interaction among evolutionary forces in the pathogenic fungus Mycosphaerella graminicola. Fungal Genet Biol 41:590–599PubMedGoogle Scholar
  168. Zhan J, Pettway RE, McDonald BA (2003) The global genetic structure of the wheat pathogen Mycosphaerella graminicola is characterised by high nuclear diversity, low mitochondrial diversity, regular recombination, and gene flow. Fungal Genet Biol 38:286–297PubMedGoogle Scholar
  169. Zhou XD, Wingfield MJ (2011) Eucalypt diseases and their management in China. Australas Plant Pathol. doi: 10.1007/s13313-011-0053-y
  170. Zhou XD, Xie YJ, Chen SF, Wingfield MJ (2008) Diseases of eucalypt plantations in China: challenges and opportunities. Fungal Divers 32:1–7Google Scholar
  171. Zobel BJ (1993) Clonal forestry in the Eucalypts. In: Ahuja MR, Libby WJ (eds) Clonal forestry II. Conservation and application. Springer, Germany, pp 139–148Google Scholar

Copyright information

© Kevin D. Hyde 2011

Authors and Affiliations

  • Gavin C. Hunter
    • 1
    • 2
  • Pedro W. Crous
    • 2
  • Angus J. Carnegie
    • 3
  • Treena I. Burgess
    • 4
  • Michael J. Wingfield
    • 1
  1. 1.Forestry and Agricultural Biotechnology Institute (FABI)University of PretoriaPretoriaSouth Africa
  2. 2.CBS-KNAW Fungal Biodiversity CentreUtrechtNetherlands
  3. 3.Forest Biosecurity and Resource Assessment, Biosecurity ResearchNew South Wales Department of Primary IndustriesBeecroftAustralia
  4. 4.Center of Excellence for Climate Change, Woodland and Forest Health, School of Biological Sciences and BiotechnologyMurdoch UniversityMurdochAustralia

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