Diversity of tree-infecting Botryosphaeriales on native and non-native trees in South Africa and Namibia

  • Fahimeh Jami
  • Michael J. Wingfield
  • Marieka Gryzenhout
  • Bernard Slippers
Review

Abstract

The Botryosphaeriales includes serious plant pathogens with a broad host and geographic distribution globally. In South Africa and Namibia, these fungi include important pathogens of native and non-native woody plants, and have consequently been studied extensively. Here we synthesize the information from the previous studies, particularly in the last decade, that report 62 species in the Botryosphaeriales from 66 hosts across South Africa and Namibia. Of these, 52 species have been reported from native hosts, 17 are from non-native hosts and twelve of these species occur on both native and non-native trees in the region. Much of the diversity of the Botryosphaeriales can be ascribed to native species that have fairly limited host and geographic ranges. Neofusicoccum parvum is amongst the most common species on both native and non-native hosts and it is thought to be native to the region. In contrast, Botryosphaeria dothidea, which is certainly an introduced species, is also widespread, and is very common on both native and non-native plants. Overall this synthesis underscores the growing understanding of the diversity of an important group of tree pathogens, their apparently common global spread as latent agents of disease, as well as their apparently common movement between commercial and native ecosystems.

Keywords

Aplosporellaceae Botryosphaeriales Pseudofusicoccumaceae Saccharataceae Host association Fungal biogeography 

Supplementary material

13313_2017_516_MOESM1_ESM.docx (28 kb)
ESM 1(DOCX 28 kb)

References

  1. Ahimera N, Gisler S, Morgan DP, Michailides TJ (2004) Effects of single-drop impactions and natural and simulated rains on the dispersal of Botryosphaeria dothidea conidia. Phytopathology 94:1189–1197CrossRefPubMedGoogle Scholar
  2. Ahumada R (2003) Pathogens in commercial Eucalyptus plantations in Chile, with special reference to Mycosphaerella and Botryosphaeria species. University of Pretoria, Pretoria, South Africa, M.Sc. ThesisGoogle Scholar
  3. Barradas C, Phillips AJ, Correia A, Diogo E, Bragança H, Alves A (2016) Diversity and potential impact of Botryosphaeriaceae species associated with Eucalyptus globulus plantations in Portugal. Eur J Plant Pathol 146:245–257Google Scholar
  4. Begoude BAD, Slippers B, Wingfield MJ, Roux J (2010) Botryosphaeriaceae associated with Terminalia catappa in Cameroon, South Africa and Madagascar. Mycol Prog 9:101–123Google Scholar
  5. Bihon W, Slippers B, Burgess T, Wingfield M, Wingfield B (2010) Diplodia scrobiculat a found in the southern hemisphere. For Pathol 41:175–181CrossRefGoogle Scholar
  6. Bihon W, Slippers B, Burgess T, Wingfield M, Wingfield B (2011) Sources of Diplodia pinea endophytic infections in Pinus patula and P. radiata seedlings in South Africa. For Pathol 41:370–375CrossRefGoogle Scholar
  7. Bihon W, Burgess T, Slippers B, Wingfield MJ, Wingfield BD (2012a) High levels of genetic diversity and cryptic recombination is widespread in introduced Diplodia pinea populations. Australas Plant Pathol 41:41–46CrossRefGoogle Scholar
  8. Bihon W, Slippers B, Burgess T, Wingfield MJ, Wingfield BD (2012b) Diverse sources of infection and cryptic recombination revealed in south African Diplodia pinea populations. Fungal Biology 116:112–120CrossRefPubMedGoogle Scholar
  9. Billones-Baaijens R, Jones E, Ridgway H, Jaspers M (2012) Pathogenicity of a New Zealand grapevine isolate of Neofusicoccum macroclavatum on Eucalyptus globulus. New Zealand Plant Protection 65:262–266Google Scholar
  10. Burgess T, Wingfield MJ (2002) Quarantine is important in restricting the spread of exotic seed-borne tree pathogens in the southern hemisphere. Int For Rev 4:56–65Google Scholar
  11. Burgess TI, Wingfield MJ (2017) Pathogens on the move: a 100-year global experiment with planted eucalypts. Bioscience 67:14–25CrossRefGoogle Scholar
  12. Burgess TI, Gordon TR, Wingfield MJ, Wingfield BD (2004a) Geographic isolation of Diplodia scrobiculata and its association with native Pinus radiata. Mycol Res 108:1399–1406CrossRefPubMedGoogle Scholar
  13. Burgess TI, Wingfield MJ, Wingfield BD (2004b) Global distribution of Diplodia pinea genotypes revealed using simple sequence repeat (SSR) markers. Australas Plant Pathol 33:513–519CrossRefGoogle Scholar
  14. 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 Ecol 31:559–566Google Scholar
  15. Burgess TI, Crous CJ, Slippers B, Hantula J, Wingfield MJ (2016) Tree invasions and biosecurity: eco-evolutionary dynamics of hitchhiking fungi. AoB Plants 8:plw076Google Scholar
  16. Chen SF, Pavlic D, Roux J, Slippers B, Xie Y, Wingfield MJ, Zhou X (2011) Characterization of Botryosphaeriaceae from plantation grown Eucalyptus species in South China. Plant Pathol 60:739–751CrossRefGoogle Scholar
  17. Conradie DC (2012) South Africa’s climatic zones: today, tomorrow. International Green Building Conference and Exhibition; Future Trends and Issues Impacting on the Built Environment, Sandton, South AfricaGoogle Scholar
  18. Copes WE, Hendrix FF (2004) Effect of temperature on sporulation of Botryosphaeria dothidea, B. obtusa, and B. rhodina. Plant Dis 88:292–296CrossRefGoogle Scholar
  19. Crous PW, Phillips AJL, Baxter AP (2000) Phytopathogenic fungi from South Africa. Department of Plant Pathology Press, Stellenbosch, South AfricaGoogle Scholar
  20. Crous PW, Slippers B, Wingfield MJ, Rheeder J, Marasas WFO, Philips AJL, Alves A, Burgess T, Barber P, Groenewald JZ (2006) Phylogenetic lineages in the Botryosphaeriaceae. Stud. Mycol 55:235–253Google Scholar
  21. Crous CJ, Jacobs SM, Esler KJ (2012) Drought-tolerance of an invasive alien tree, Acacia mearnsii and two native competitors in fynbos riparian ecotones. Biol Invasions 14:619–631CrossRefGoogle Scholar
  22. Crous PW, Groenewald JZ, Slippers B, Wingfield MJ (2016) Global food and fibre security threatened by current inefficiencies in fungal identification. Philos Trans R Soc B 371:20160024CrossRefGoogle Scholar
  23. Cruywagen EM, Slippers B, Roux J, Wingfield MJ (2017) Phylogenetic species recognition and hybridisation in Lasiodiplodia: a case study on species from baobabs. Fungal Biol 121:420–436Google Scholar
  24. Cunnington JH, Priest MJ, Powney RA, Cother NJ (2007) Diversity of Botryosphaeria species on horticultural plants in Victoria and new South Wales. Australas Plant Pathol 36:157–159CrossRefGoogle Scholar
  25. Damm U, Crous PW, Fourie PH (2007) Botryosphaeriaceae as potential pathogens of Prunus species in South Africa, with descriptions of Diplodia africana and Lasiodiplodia plurivora sp. nov. Mycologia 99:664–680Google Scholar
  26. Denman S, Crous PW, Groenewald JZ, Slippers B, Wingfield BD, Wingfield MJ (2003) Circumscription of Botryosphaeria species associated with Proteaceae based on morphology and DNA sequence data. Mycologia 95:294–307Google Scholar
  27. Epstein L, Sukhwinder K, Vandergheynst J (2008) Botryosphaeria-related dieback and control investigated in noncoastal California grapevines. Calif Agric 62:161–166CrossRefGoogle Scholar
  28. Flowers J, Hartman J, Vaillancourt L (2003) Detection of latent Sphaeropsis sapinea infections in Austrian pine tissues using nested-polymerase chain reaction. Phytopathology 93:1471–1477CrossRefPubMedGoogle Scholar
  29. Fourie P, Halleen F (2001) Diagnosis of fungal diseases and their involvement in dieback diseases of young vines. Winelands 12:19–23Google Scholar
  30. Geldenhuys CJ (1997) Native forest regeneration in pine and eucalypt plantations in Northern Province, South Africa. For Ecol Manag 99:101–116CrossRefGoogle Scholar
  31. Gibson IAS (1975) The Leguminosae. In diseases of forest trees widely planted as exotics in the tropics and southern hemisphere. Part I. Important members of the Myrtaceae, Leguminosae, Verbenaceae and MeliaceaeGoogle Scholar
  32. Heath RN, Roux J, Slippers B, Drenth A, Pennycook S, Wingfield BD, Wingfield MJ (2011) Occurrence and pathogenicity of Neofusicoccum parvum and N. mangiferae on ornamental Tibouchina species. For Pathol 41:48–51Google Scholar
  33. Http://En.Wikipedia.Org/Wiki/Climate_of_South_Africa (2007)Google Scholar
  34. Http://Www.Forestry.Co.Za/Statistical-Data/ (2011) South African Forestry and Forest Products Industry Facts [Online]Google Scholar
  35. Iturritxa E, Slippers B, Mesanza N, Wingfield MJ (2011) First report of Neofusicoccum parvum causing canker and die-back of Eucalyptus in Spain. Australasian Plant Dis Notes 6:57–59Google Scholar
  36. Jami F, Slippers B, Wingfield MJ, Gryzenhout M (2012) Five new species of the Botryosphaeriaceae from Acacia karroo in South Africa. Cryptogam Mycol 33:245–266CrossRefGoogle Scholar
  37. Jami F, Slippers B, Wingfield MJ, Gryzenhout M (2013) Greater Botryosphaeriaceae diversity in healthy than associated diseased Acacia karroo tree tissues. Australas Plant Pathol 42:421–430CrossRefGoogle Scholar
  38. Jami F, Slippers B, Wingfield MJ, Gryzenhout M (2014) Botryosphaeriaceae species overlap on four unrelated, native south African hosts. Fungal Biol 118:168–179Google Scholar
  39. Jami F, Slippers B, Wingfield MJ, Gryzenhout M (2015) Temporal and spatial variation of Botryosphaeriaceae associated with Acacia karroo in South Africa. Fungal Ecol 15:51–62CrossRefGoogle Scholar
  40. Kemler M, Garnas J, Wingfield MJ, Gryzenhout M, Pillay K-A, Slippers B (2013) Ion torrent PGM as tool for fungal community analysis: a case study of endophytes in Eucalyptus grandis reveals high taxonomic diversity. PLoS One 8:e81718CrossRefPubMedPubMedCentralGoogle Scholar
  41. Linde C, Kemp G, Wingfield M (1997) First report of Sphaeropsis canker on cypress in South Africa. Eur J For Pathol 27:173–177Google Scholar
  42. Maleme H (2009) Characterisation of latent Botryosphaeriaceae on diverse Eucalyptus species. Department of Microbiology and Plant Pathology, University of Pretoria, South Africa, M.Sc. ThesisGoogle Scholar
  43. Marincowitz S, Groenewald JZ, Wingfield MJ, Crous PW (2008) Species of Botryosphaeriaceae occurring on Proteaceae. Persoonia 21:111–118Google Scholar
  44. Marsberg A, Kemler M, Jami F, Nagel JH, Postma-Smidt A, Naido S, Wingfield MJ, Crous PW, Spatafora J, Hesse CN (2017) Botryosphaeria dothidea: a latent pathogen of global importance to woody plant health. Mol Plant Pathol 18:477–488Google Scholar
  45. Martínez-Minaya J, Conesa D, López-Quílez A, Vicent A (2015) Climatic distribution of citrus black spot caused by Phyllosticta citricarpa. A historical analysis of disease spread in South Africa Eur J Plant Pathol 143:69–83Google Scholar
  46. Mehl JWM, Slippers B, Roux J, Wingfield MJ (2011) Botryosphaeriaceae associated with Pterocarpus angolensis (kiaat) in South Africa. Mycologia 103:534–553CrossRefPubMedGoogle Scholar
  47. Mehl J, Slippers B, Roux J, Wingfield M (2014) Botryosphaeriaceae associated with die-back of Schizolobium parahyba trees in South Africa and Ecuador. For Pathol 44:396–408CrossRefGoogle Scholar
  48. Mehl JW, Slippers B, Roux J, Wingfield MJ (2017a) Overlap of latent pathogens in the Botryosphaeriaceae on a native and agricultural host. Fungal Biol 121:405–149Google Scholar
  49. Mehl J, Wingfield MJ, Roux J, Slippers B (2017b) Invasive everywhere? Phylogeographic analysis of the globally distributed tree pathogen Lasiodiplodia theobromae. Forests 8:145CrossRefGoogle Scholar
  50. Michailides TJ, Morgan DP (1992) Effects of temperature and wetness duration on infection of pistachio by Botryosphaeria dothidea and management of disease by reducing duration of irrigation. Phytopathology 82:1399–1406CrossRefGoogle Scholar
  51. Mohali S, Slippers B, Wingfield MJ (2007) Identification of Botryosphaeriaceae from Eucalyptus, Acacia and Pinus in Venezuela. Fungal Divers 25:103–125Google Scholar
  52. Nakabonge G (2002) Diseases associated with plantation forestry in Uganda. University of Pretoria, South Africa, MSc Thesis. Department of Microbiolgy and Plant PathologyGoogle Scholar
  53. Ndove L (2015) Botryosphaeriaceae associated with Southern Hemisphere gymnosperms. University of Pretoria, South Africa, MSc Thesis. Department of Microbiolgy and Plant PathologyGoogle Scholar
  54. Osorio JA, Crous CJ, De Beer ZW, Wingfield MJ, Roux J (2017) Endophytic Botryosphaeriaceae, including five new species, associated with mangrove trees in South Africa. Fungal Biol 121:361–393Google Scholar
  55. Pavlic D, Slippers B, Coutinho TA, Gryzenhout M, Wingfield MJ (2004) Lasiodiplodia gonubiensis sp. nov., a new Botryosphaeria anamorph from native Syzygium cordatum in South Africa. Stud Mycol 50:313–322Google Scholar
  56. Pavlic D, Slippers B, Coutinho TA, Wingfield MJ (2007) Botryosphaeriaceae occurring on native Syzygium cordatum in South Africa and their potential threat to Eucalyptus. Plant Pathol 56:624–636CrossRefGoogle Scholar
  57. 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. Mol Phylogenet Evol 51:259–268CrossRefPubMedGoogle Scholar
  58. Pérez C, Altier N, Simeto S, Wingfield M, Slippers B, Blanchette R (2008) Botryosphaeriaceae from Eucalyptus and native Myrtaceae in Uruguay. Agrociencia 12:19–30Google Scholar
  59. Pérez CA, Wingfield MJ, Slippers B, Altier NA, Blanchette RA (2009) Neofusicoccum eucalyptorum, a Eucalyptus pathogen, on native Myrtaceae in Uruguay. Plant Pathol 58:964–970CrossRefGoogle Scholar
  60. Phillips A, Alves A, Abdollahzadeh J, Slippers B, Wingfield M, Groenewald J, Crous P (2013) The Botryosphaeriaceae: genera and species known from culture. Stud Mycol 76:51–167CrossRefPubMedPubMedCentralGoogle Scholar
  61. Pillay K, Slippers B, Wingfield MJ, Gryzenhout M (2013) Diversity and distribution of co-infecting Botryosphaeriaceae from Eucalyptus grandis and Syzygium cordatum in South Africa. S Afr J Bot 84:38–43CrossRefGoogle Scholar
  62. Punithalingam E (1976) Botryodiplodia theobromae. Commonwealth Mycological Institute, Kew, Surrey, EnglandGoogle Scholar
  63. Punithalingam E (ed) (1980) Plant diseases attributed to Botryodiplodia theobromae. Biblioteca Mycologica, J. Cramer, Berlin, Germany, InGoogle Scholar
  64. Rodas C, Slippers B, Gryzenhout M, Wingfield M (2009) Botryosphaeriaceae associated with eucalyptus canker diseases in Colombia. For Pathol 39:110–123CrossRefGoogle Scholar
  65. Rodríguez-Gálvez E, Guerrero P, Barradas C, Crous PW, Alves A (2017) Phylogeny and pathogenicity of Lasiodiplodia species associated with dieback of mango in Peru. Fungal Biol 121:425–465Google Scholar
  66. Roux J (1998) Diseases of Acacia mearnsii in South Africa with particular reference to Ceratocystis wilt. PhD thesis, University of Pretoria, Pretoria, South AfricaGoogle Scholar
  67. Roux J, Wingfield MJ (1997) Survey and virulence of fungi occurring on diseased Acacia mearnsii in South Africa. Forest Ecol Manag 99:327–336Google Scholar
  68. Roux J, Wingfield MJ, Morris MJ (1997) Botryosphaeria dothidea as a pathogen of Acacia mearnsii in South Africa. S Afr J Sci 99:327–336Google Scholar
  69. Roux J, Coutinho T, Wingfield M, Bouillet J (2000) Diseases of plantation Eucalyptus in the Republic of Congo. S Afr J Sci 96:454–456Google Scholar
  70. Sakalidis ML, Hardy GESJ, Burgess TI (2011) Class III endophytes, clandestine movement amongst hosts and habitats and their potential for disease; a focus on Neofusicoccum australe. Australas Plant Pathol 40:510–521CrossRefGoogle Scholar
  71. Sakalidis ML, Slippers B, Wingfield BD, Hardy GESJ, Burgess TI (2013) The challenge of understanding the origin, pathways and extent of fungal invasions: global populations of the Neofusicoccum parvum–N. ribis species complex. Divers Distrib 19:873–1094CrossRefGoogle Scholar
  72. Slippers B (2003) Taxonomy, phylogeny- and ecology of botryosphaeriaceous fungi occurring on various woody hosts. Ph.D. Thesis, Department of Microbiology and Plant Pathology, University of Pretoria, South AfricaGoogle Scholar
  73. Slippers B, Wingfield MJ (2007) Botryosphaeriaceae as endophytes and latent pathogens of woody plants: diversity, ecology and impact. Fungal Biol Rev 21:90–106Google Scholar
  74. Slippers B, Fourie G, Crous PW, Coutinho TA, Wingfield BD, Carnegie AJ, Wingfield MJ (2004) Speciation and distribution of Botryosphaeria spp. on native and introduced Eucalyptus trees in Australia and South Africa. Stud Mycol 50:343–358Google Scholar
  75. Slippers B, Stenlid J, Wingfield MJ (2005) Emerging pathogens: fungal host jumps following anthropogenic introduction. Trends Ecol Evol 20:420–421CrossRefPubMedGoogle Scholar
  76. Slippers B, Smit WA, Crous PW, Coutinho TA, Wingfield BD, Wingfield MJ (2007) Taxonomy, phylogeny and identification of Botryosphaeriaceae associated with pome and stone fruit trees in South Africa and other regions of the world. Plant Pathol 56:128–139CrossRefGoogle Scholar
  77. Slippers B, Burgess T, Pavlic D, Ahumada R, Maleme H, Mohali S, Rodas C, Wingfield MJ (2009) A diverse assemblage of Botryosphaeriaceae infect Eucalyptus in native and non-native environments. South Forests 71:101–110Google Scholar
  78. Slippers B, Boissin E, Phillips A, Groenewald J, Lombard L, Wingfield M, Postma A, Burgess T, Crous P (2013) Phylogenetic lineages in the Botryosphaeriales: a systematic and evolutionary framework. Stud Mycol 76:31–49CrossRefPubMedPubMedCentralGoogle Scholar
  79. Slippers B, Roux J, Wingfield MJ, Van Der Walt FJJ, Jami F, Marais GJ (2014) Confronting the constraints of morphological taxonomy in the fungi: a Botryosphaeriaceae case study. Persoonia 33:155–168CrossRefPubMedPubMedCentralGoogle Scholar
  80. Slippers B, Crous P, Jami F, Groenewald J, Wingfield M (2017) Diversity in the Botryosphaeriales: looking back, looking forward. Fungal Biol 121:307–321Google Scholar
  81. Smith H, Kemp GHJ, Wingfield MJ (1994) Canker and die-back of Eucalyptus in South Africa caused by Botryosphaeria dothidea. Plant Pathol 43:1031–1034CrossRefGoogle Scholar
  82. Smith H, Wingfield MJ, Petrini O (1996a) Botryosphaeria dothidea endophytic in Eucalyptus grandis and Eucalyptus nitens in South Africa. For Ecol Manag 89:189–195CrossRefGoogle Scholar
  83. Smith H, Wingield MJ, Crous PW, Coutinho TA (1996b) Sphaeropsis sapinea and Botryosphaeria dothidea endophytic in Pinus spp. and Eucalyptus spp. in South Africa. S Afr J Bot 62:86–88CrossRefGoogle Scholar
  84. Smith H, Wingfield M, De Wet J, Coutinho T (2000) Genotypic diversity of Sphaeropsis sapinea from South Africa and northern Sumatra. Plant Dis 84:139–142CrossRefGoogle Scholar
  85. Smith H, Crous PW, Wingfield MJ, Coutinho TA, Wingfield BD (2001) Botryosphaeria eucalyptorum sp. nov., a new species in the B. dothidea complex on Eucalyptus in South Africa. Mycologia 93:277–285Google Scholar
  86. Stanosz GR, Carlson JC (1996) Association of mortality of recently planted seedlings and established saplings in red pine plantations with Sphaeropsis collar rot. Plant Dis 80:750–753CrossRefGoogle Scholar
  87. Steenkamp ET, Wingfield MJ (2013) Global forest research, science education and community service positively impacted by a unique Centre of Excellence in tree health biotechnology. South Forests 75:71–80Google Scholar
  88. Swart H (1986) Australian leaf-inhabiting fungi XXII. Microthyrium-like fungi on Eucalyptus. T Brit Mycol Soc 87:81–91Google Scholar
  89. Swart WJ, Wingfield MJ (1991) Biology and control of Sphaeropsis sapinea on Pinus species in South Africa. Plant Dis 75:761–766CrossRefGoogle Scholar
  90. Swart WJ, Knox Davies PS, Wingfield MJ (1985) Sphaeropsis sapinea, with special reference to its occurrence on Pinus spp. in South Africa. South African Forestry Journal 35:1–8CrossRefGoogle Scholar
  91. Swart W, Wingfield M, Knox-Davies P (1987) Conidial dispersal of Sphaeropsis sapinea in three climatic regions of South Africa. Plant Dis 71:1038–1040CrossRefGoogle Scholar
  92. Taylor K, Barber PA, Hardy GESJ, Burgess TI (2009) Botryosphaeriaceae from tuart (Eucalyptus gomphocephala) woodland, including descriptions of four new species. Mycol Res 113:337–353CrossRefPubMedGoogle Scholar
  93. Úrbez-Torres J, Battany M, Bettiga L, Gispert C, Mcgourty G, Roncoroni J, Smith R, Verdegaal P, Gubler W (2010) Botryosphaeriaceae species spore-trapping studies in California vineyards. Plant Dis 94:717–724CrossRefGoogle Scholar
  94. Urbez-Torres J, Bruez E, Hurtado J, Gubler W (2010) Effect of temperature on conidial germination of Botryosphaeriaceae species infecting grapevines. Plant Dis 94:1476–1484CrossRefGoogle Scholar
  95. Van Der Linde JA, Begoude BAD, Roux J (2010) High levels of Botryosphaeriaceae diversity on native and introduced Acacia spp. in South Africa. Proceedings of the 9th Conference of the International Mycological Society, 2010 Edinburgh, ScotlandGoogle Scholar
  96. Van Der Linde J, Six DL, Wingfield MJ, Roux J (2011) Lasiodiplodia species associated with dying Euphorbia ingens in South Africa. South Forests 73:165–173Google Scholar
  97. Van Niekerk JM, Crous PW, Groenewald JZ, Fourie PH, Halleen F (2004) DNA phylogeny, morphology and pathogenicity of Botryosphaeria species on grapevines. Mycologia 96:781–798CrossRefPubMedGoogle Scholar
  98. Van Niekerk J, Fourie P, Hallenn F, Crous P (2006) Botryosphaeria spp. as grapevine trunk disease pathogens. Phytopathol Mediterr 45:43–54Google Scholar
  99. Van Niekerk J, Bester W, Halleen F, Crous P, Fourie P (2010a) First report of Lasiodiplodia crassispora as a pathogen of grapevine trunks in South Africa. Plant Dis 94:1063–1063CrossRefGoogle Scholar
  100. Van Niekerk JM, Calitz FJ, Halleen F, Fourie PH (2010b) Temporal spore dispersal patterns of grapevine trunk pathogens in South Africa. Eur J Plant Pathol 127:375–390CrossRefGoogle Scholar
  101. Van Niekerk J, Strever AE, Du Toit GP, Halleen F, Fourie PH (2011) Influence of water stress on Botryosphaeriaceae disease expression in grapevines. Phytopathol Mediterr 50:151–165Google Scholar
  102. Zenni RD, Dickie IA, Wingfield MJ, Hirsch H, Crous CJ, Meyerson LA, Burgess TI, Zimmermann TG, Klock MM, Siemann E (2016) Evolutionary dynamics of tree invasions: complementing the unified framework for biological invasions. AoB Plants 9:plw085Google Scholar
  103. Zwolinski J, Swart W, Wingfield M (1990) Economic impact of a post-hail outbreak of dieback induced by Sphaeropsis sapinea. Eur J For Pathol 20:405–411CrossRefGoogle Scholar
  104. Zwolinski J, Swart W, Wingfield M (1995) Association of Sphaeropsis sapinea with insect infestation following hail damage of Pinus radiata. For Ecol Manag 72:293–298CrossRefGoogle Scholar

Copyright information

© Australasian Plant Pathology Society Inc. 2017

Authors and Affiliations

  • Fahimeh Jami
    • 1
  • Michael J. Wingfield
    • 1
  • Marieka Gryzenhout
    • 2
  • Bernard Slippers
    • 3
  1. 1.Department of Microbiology and Plant Pathology, Forestry & Agricultural Biotechnology Institute (FABI)University of PretoriaPretoriaSouth Africa
  2. 2.Department of GeneticsUniversity of the Free StateBloemfonteinSouth Africa
  3. 3.Department of Genetics, Forestry & Agricultural Biotechnology Institute (FABI)University of PretoriaPretoriaSouth Africa

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