Pitch canker caused by Fusarium circinatum — a growing threat to pine plantations and forests worldwide

Pitch canker, caused by the fungus Fusarium circinatum, is one of the most important pathogens of Pinus species. Sporadic outbreaks and epidemics caused by this fungus have been reported from numerous countries. Symptoms differ depending on the host species, geographical region, climatic conditions and associated insects. Pitch canker represents a significant threat to countries where non-native and susceptible Pinus spp. are grown intensively in plantations.Athorough understanding of the ecology and epidemiology of the causal agent is an important prerequisite to managing this threat. The aim of this review is to summarise contemporary knowledge relating to the pitch canker pathogen, with a particular focus on its threat to plantation forestry.

[1]  J. Leslie Fungal vegetative compatibility. , 1993, Annual review of phytopathology.

[2]  L. D. Dwinell,et al.  Pitch canker of Pinus luchuensis in Japan. , 1990 .

[3]  B. Wingfield,et al.  Molecular detection of fungi carried by Bradysia difformis (Sciaridae: Diptera) in South African forestry nurseries , 2007 .

[4]  M. Wingfield,et al.  Pine weevil Pissodes nemorensis : threat to South African pine plantations and options for control : review article , 2003 .

[5]  D. Wood,et al.  Modification of coevolved insect–plant interactions by an exotic plant pathogen , 1999 .

[6]  D. Wood,et al.  Pitch canker disease of pines: current and future impacts. , 1997 .

[7]  C. Brasier,et al.  The transmission of Dutch elm disease: a study of the process involved. , 1984 .

[8]  D. Wood,et al.  Incidence of the pitch canker pathogen and associated insects in intact and chipped Monterey pine branches , 2002, The Canadian Entomologist.

[9]  L. D. Dwinell,et al.  Diseases of pines caused by the pitch canker fungus , 2001 .

[10]  W. Marasas,et al.  Female Fertility and Mating Type Distribution in a South African Population of Fusarium subglutinans f. sp.pini , 1998, Applied and Environmental Microbiology.

[11]  T. Tashiro,et al.  Distribution of Fusarium moniliforme var. subglutinans in Kagoshima Prefecture and its pathogenicity to pines. , 1993 .

[12]  G. H. Hepting,et al.  Host relations and spread of the pine pitch canker disease. , 1953 .

[13]  D. Huber,et al.  Genetic dissection of fusiform rust and pitch canker disease traits in loblolly pine , 2005, Theoretical and Applied Genetics.

[14]  L. D. Dwinell,et al.  Pitch canker: a disease complex of southern pines. , 1985 .

[15]  P. E. Nelson,et al.  Characterization of the Fusarium Causing Pitch Canker of Southern Pines , 1978 .

[16]  L. D. Dwinell,et al.  Contamination of Pine Seeds by the Pitch Canker Fungus , 1999 .

[17]  J. Williams,et al.  Incidence of pitch canker among clones of loblolly pine in seed orchards. , 1982 .

[18]  D. Rockwood,et al.  Genetic strategies for reducing pitch canker incidence in slash pine. , 1988 .

[19]  R. Bruck,et al.  Effects of thiabendazole-DMSO treatment of longleaf pine seed contaminated with Fusarium subglutinans on germination and seedling survival , 1988 .

[20]  S. Enebak,et al.  Responses of conifer species of the Great Lakes region of North America to inoculation with the pitch canker pathogen Fusarium circinatum , 2003 .

[21]  M. Dickman,et al.  Sensitivity of field strains of Gibberella fujikuroi (Fusarium section Liseola) to benomyl and Hygromycin B , 1993 .

[22]  John F. Leslie,et al.  The Fusarium laboratory manual. , 2006 .

[23]  Thomas R. Gordon,et al.  Susceptibility of Douglas fir (Pseudotsuga menziesii) to pitch canker, caused by Gibberella circinata (anamorph = Fusarium circinatum) , 2006 .

[24]  D. Wood,et al.  ENGRAVER BEETLES (SCOLYTIDAE: IPS SPECIES) AS VECTORS OF THE PITCH CANKER FUNGUS, FUSARIUM SUBGLUTINANS , 1991, The Canadian Entomologist.

[25]  E. Kuhlman VARIETIES OF GIBBERELLA FUJIKUROI WITH ANAMORPHS IN FUSARIUM SECTION LISEOLA , 1982 .

[26]  D. Wood,et al.  The dynamics of an introduced pathogen in a native Monterey pine (Pinus radiata) forest , 2003 .

[27]  P. E. Nelson,et al.  Fusarium species: an illustrated manual for identification. , 1983 .

[28]  D. Wood,et al.  Susceptibility of five landscape pines to pitch canker disease, caused by Fusarium subglutinans f.sp. pini , 1998 .

[29]  J. Leslie Gibberella fujikuroi: available populations and variable traits , 1995 .

[30]  J. Barrows-Broaddus Colonization of cones and seed of loblolly pine following inoculation with Fusarium subglutinans , 1990 .

[31]  D. Wood,et al.  Evidence of resistance to the pitch canker pathogen (Fusarium circinatum) in native stands of Monterey pine (Pinus radiata). , 1999 .

[32]  D. Wood,et al.  DISTRIBUTION AND ABUNDANCE OF ENGRAVER BEETLES (SCOLYTIDAE: IPS SPECIES) ON MONTEREY PINES INFECTED WITH PITCH CANKER , 1990, The Canadian Entomologist.

[33]  G. H. Hepting,et al.  Pitch canker, a new disease of some Southern Pines. , 1946 .

[34]  D. Wood,et al.  Pitch canker disease in California: pathogenicity, distribution, and canker development on Monterey pine (Pinus radiata) , 1991 .

[35]  W. Marasas,et al.  Genotypic diversity in a South African population of the pitch canker fungus Fusarium subglutinans f.sp. pini , 1997 .

[36]  L. D. Dwinell,et al.  Variation in susceptibility to the pitch canker fungus among half-sib and full-sib families of Virginia pine. , 1984 .

[37]  W. Marasas,et al.  PCR-Based Identification of MAT-1 andMAT-2 in the Gibberella fujikuroi Species Complex , 2000, Applied and Environmental Microbiology.

[38]  J. Leslie,et al.  Female fertility and mating type effects on effective population size and evolution in filamentous fungi. , 1996, Genetics.

[39]  S. Grunwald,et al.  Spatial relationships between nitrogen status and pitch canker disease in slash pine planted adjacent to a poultry operation. , 2007, Environmental pollution.

[40]  D. Wood,et al.  Colonization of cut branches of five coniferous hosts of the pitch canker fungus by Pityophthorus spp. (Coleoptera: Scolytidae) in central, coastal California , 2005, The Canadian Entomologist.

[41]  A. Pérez-Sierra,et al.  Characterization of Fusarium circinatum from Pinus spp. in northern Spain. , 2007, Mycological research.

[42]  E. Kuhlman Effects of inoculation treatment with Fusarium moniliforme var. subglutinans on dieback of loblolly and slash pine seedlings , 1987 .

[43]  M. Wingfield,et al.  Fungus gnats and other Diptera in South African forestry nurseries and their possible association with the pitch canker fungus , 2007 .

[44]  A J Storer,et al.  The Pitch Canker Epidemic in California. , 2001, Plant disease.

[45]  M. Dick Pine pitch canker - the threat to New Zealand. , 1998 .

[46]  K. O’Donnell,et al.  Molecular systematics and phylogeography of Gibberella fujikuroi species complex , 1998 .

[47]  D. Wood,et al.  TRANSMISSION OF THE PITCH CANKER FUNGUS, FUSARIUM SUBGLUTINANS F. SP. PINI, TO MONTEREY PINE, PINUS RADIATA, BY CONE- AND TWIG-INFESTING BEETLES , 1996, The Canadian Entomologist.

[48]  W. Marasas,et al.  First report of Fusarium subglutinans f.sp. pini on pine seedlings in South Africa , 1994 .

[49]  M. Wingfield,et al.  Characterisation of the pitch canker fungus, Fusarium circinatum, from Mexico , 2001 .

[50]  W. R. Phelps,et al.  Pitch Canker of Slash Pine in Florida , 1977 .

[51]  A. Myburg,et al.  Complete genetic linkage maps from an interspecific cross between Fusarium circinatum and Fusarium subglutinans. , 2007, Fungal genetics and biology : FG & B.

[52]  M. Wingfield,et al.  First report of the pitch canker fungus, Fusarium circinatum, on pines in Chile , 2002 .

[53]  D. Wood,et al.  The role of olfactory stimuli in the location of weakened hosts by twig‐infesting Pityophthorus spp. , 2001 .

[54]  E. Barnard,et al.  Pitch canker of slash pine seedlings: a new disease in forest tree nurseries. , 1980 .

[55]  D. Wood,et al.  ASSOCIATION BETWEEN A NATIVE SPITTLEBUG (HOMOPTERA: CERCOPIDAE) ON MONTEREY PINE AND AN INTRODUCED TREE PATHOGEN WHICH CAUSES PITCH CANKER DISEASE , 1998, The Canadian Entomologist.

[56]  S. Enebak,et al.  Pitch Canker Caused by Fusarium circinatum Identified on Spruce Pine in Alabama. , 2003, Plant disease.

[57]  L. G. Arvanitis,et al.  Pitch Canker Impact on Volume Growth: A Case Study In Slash Pine Plantations , 1984 .

[58]  S. Covert,et al.  Partial MAT-2 gene structure and the influence of temperature on mating success in Gibberella circinata. , 1999, Fungal genetics and biology : FG & B.

[59]  D. Woodb,et al.  The dynamics of an introduced pathogen in a native Monterey pine ( Pinus radiata ) forest , 2003 .

[60]  W. Marasas,et al.  Characterization of Fusarium isolates from gladiolus corms pathogenic to pines , 1995 .

[61]  K. O’Donnell,et al.  A multigene phylogeny of theGibberella fujikuroi species complex: Detection of additional phylogenetically distinct species , 2000 .

[62]  A. Pérez-Sierra,et al.  Outbreak of Pitch Canker Caused by Fusarium circinatum on Pinus spp. in Northern Spain. , 2005, Plant disease.

[63]  T. Gordon,et al.  An initial assessment of genetic relationships among populations of Fusarium circinatum in different parts of the world , 2000 .

[64]  D. Vogler,et al.  First Report of the Pitch Canker Fungus (Fusarium circinatum) in the Sierra Nevada of California. , 2004, Plant disease.

[65]  R. Fisher,et al.  Effects of Fertilization on Healthy and Pitch Canker-Infected Pines , 1981 .

[66]  M. Wingfield,et al.  The future of exotic plantation forestry in the tropics and southern Hemisphere: Lessons from pitch canker , 2002 .

[67]  A. Carlucci,et al.  First Report of Pitch Canker Caused by Fusarium circinatum on Pinus halepensis and P. pinea in Apulia (Southern Italy). , 2007, Plant disease.

[68]  C. Ohmart The within-Tree Distributions of Ips paraconfusus (Coleoptera: Scolytidae) and Its Insect Associates in Monterey Pine (Pinus radiata) , 1979 .

[69]  L. D. Dwinell,et al.  Decay and colonization of Gladiolus corms by the pine pitch canker fungus. , 1980 .

[70]  B. Fraedrich,et al.  Influence of fertilizations on pitch canker development on three southern pine species. , 1982 .

[71]  R. K. Dixon,et al.  In vitro host-pathogen interactions of Pinus elliottii calli and Fusarium moniliforme var. subglutinans , 1992 .

[72]  T. Gordon,et al.  Resistance to pitch canker disease, caused by Fusarium subglutinans f.sp. pini, in Monterey pine (Pinus radiata) , 1998 .

[73]  W. Marasas,et al.  Diversity and differentiation in two populations of Gibberella circinata in South Africa , 2005 .

[74]  T. Gordon,et al.  Rates of pitch canker induced seedling mortality among Pinus radiata families varying in levels of genetic resistance to Gibberella circinata (anamorph Fusarium circinatum) , 2006 .

[75]  G. Blakeslee,et al.  Significant mortality associated with pitch canker infection of slash pine in Florida. , 1979 .

[76]  L. D. Dwinell,et al.  Branch dieback and cone and seed infection caused by Fusarium moniliforme var. subglutinans in a loblolly pine seed orchard in South Carolina. , 1985 .

[77]  R. G. Mitchel,et al.  The effect of applying prophylactic measures on the post-planting survival of Pinus patula in South Africa , 2004 .

[78]  A. C. Matheson,et al.  Heritability of response to inoculation by pine pitch canker of seedlings of radiata pine , 2006 .

[79]  D. Wood,et al.  Pitch canker kills pines, spreads to new species and regions , 1994 .

[80]  A. Nel,et al.  Testing of selected South African Pinus hybrids and families for tolerance to the pitch canker pathogen, Fusarium circinatum , 2007, New Forests.

[81]  Effects of pitch canker pathogen on gallery excavation and oviposition by Ips paraconfusus (Coleoptera: Scolytidae) , 2002, The Canadian Entomologist.

[82]  M. Garbelotto,et al.  Detection and Quantification of Airborne Conidia of Fusarium circinatum, the Causal Agent of Pine Pitch Canker, from Two California Sites by Using a Real-Time PCR Approach Combined with a Simple Spore Trapping Method , 2004, Applied and Environmental Microbiology.

[83]  D. Wood,et al.  Twig beetles, Pityophthorus spp. (Coleoptera: Scolytidae), as vectors of the pitch canker pathogen in California , 2004, The Canadian Entomologist.

[84]  T. Gordon,et al.  Evidence for recombination and segregation of virulence to pine in a hybrid cross between Gibberella circinata and G. subglutinans. , 2007, Mycological research.

[85]  C. Koehler,et al.  Pitch canker threatens California pines , 1987 .

[86]  D. Wood,et al.  QUANTITATIVE AND SEASONAL ASSOCIATION OF THE PITCH CANKER FUNGUS, FUSARIUM SUBGLUTINANS F. SP. PINI WITH CONOPHTHORUS RADIATAE (COLEOPTERA: SCOLYTIDAE) AND ERNOBIUS PUNCTULATUS (COLEOPTERA: ANOBIIDAE) WHICH INFEST PINUS RADIATA , 1995, The Canadian Entomologist.

[87]  W. Marasas,et al.  Differentiation of Fusarium subglutinansf. sp. pini by Histone Gene Sequence Data , 1999, Applied and Environmental Microbiology.

[88]  W. A. Carey First Report of Fusarium subglutinans as a Cause of Late-Season Mortality in Longleaf Pine Nurseries , 1994 .

[89]  W. Dvorak,et al.  Differential responses of Central American and Mexican pine species and Pinus radiata to infection by the pitch canker fungus , 2000, New Forests.

[90]  K. O’Donnell,et al.  New Fusarium species and combinations within the Gibberella fujikuroi species complex , 1998 .

[91]  J. Correll,et al.  Genetic diversity in California and Florida populations of the pitch canker fungus Fusarium subglutinans f. sp. pini , 1992 .

[92]  G. H. Hepting,et al.  Fusaria associated with Mimosa wilt, Sumac wilt, and pine pitch canker. , 1949 .

[93]  T. Gordon,et al.  Pitch canker disease of pines. , 2006, Phytopathology.

[94]  R. L. Furniss,et al.  Western forest insects , 1977 .

[95]  Sequence characterized amplified polymorphic markers for the pitch canker pathogen, Fusarium circinatum , 2002 .

[96]  W. Dvorak,et al.  Variation in pitch canker resistance among provenances of Pinus patula and Pinus tecunumanii from Mexico and Central America , 2007, New Forests.

[97]  T. Gordon,et al.  Population structure of the pitch canker pathogen, Fusarium subglutinans f.sp. pini, in California. , 1996 .

[98]  W. Marasas,et al.  Characterization of Fusarium subglutinans f. sp. pini causing root disease of Pinus patula seedlings in South Africa , 1997 .

[99]  A. Rayner,et al.  Invertebrate-Microbial Interactions , 1985 .

[100]  C. Campbell,et al.  Isozyme Variation among Biological Species in the Gibberella fujikuroi Species Complex (Fusarium Section Liseola) , 1996, Applied and environmental microbiology.

[101]  D. Wood,et al.  The role of Pityophthorus spp. as vectors of pitch canker affecting Pinus radiata , 2007, The Canadian Entomologist.

[102]  Gordon,et al.  Systemic induced resistance in Monterey pine , 2001 .

[103]  M. Wingfield,et al.  First outbreak of pitch canker in a South African pine plantation , 2007, Australasian Plant Pathology.

[104]  E. Kuhlman Epidemiology of Pitch Canker Disease in a Loblolly Pine Seed Orchard in North Carolina , 1982 .

[105]  Jane Barrows Broaddus Histopathology ofFusarium moniliformevar.subglutinansin Four Species of Southern Pines , 1983 .

[106]  J. C. Petersen,et al.  Potential diversity in vegetative compatibility groupings in the California population of Gibberella circinata. , 2006, Mycological research.

[107]  D. Owen,et al.  Impact of Pitch Canker on Ornamental Monterey Pines in Santa Cruz County, California, U.S., 1987-2000 , 2001, Arboriculture & Urban Forestry.

[108]  S. Covert,et al.  Pine genes regulated by the necrotrophic pathogen Fusarium circinatum , 2004, Theoretical and Applied Genetics.

[109]  Clark,et al.  Association of the pitch canker fungus, Fusarium subglutinans f.sp. pini, with Monterey pine seeds and seedlings in California , 1998 .

[110]  W. Marasas,et al.  Fusarium subglutinans f. sp.pini Represents a Distinct Mating Population in theGibberella fujikuroi Species Complex , 1999, Applied and Environmental Microbiology.

[111]  W. Marasas,et al.  Susceptibility of pines in South Africa to the pitch canker fungus subglutinans f.sp. pini , 1995 .

[112]  A. Goldarazena,et al.  Quantitative Association of Bark Beetles with Pitch Canker Fungus and Effects of Verbenone on Their Semiochemical Communication in Monterey Pine Forests in Northern Spain , 2007, Environmental entomology.

[113]  T. Gordon,et al.  Factors influencing infection of mechanical wounds by Fusarium circinatum on Monterey pines (Pinus radiata) , 2006 .

[114]  R. Bruck,et al.  Effects of carbofuran and thiabendazole on incidence of pitch canker of loblolly pine. , 1993 .

[115]  L. D. Dwinell,et al.  Evaluation of Arthrobacter sp. for biological control of the pitch canker fungus (Fusarium moniliforme var. subglutinans) on slash pines , 1985 .

[116]  Thomas R. Gordon,et al.  The epidemiology of pitch canker of Monterey pine in California , 2002 .

[117]  D. Shaw,et al.  Limiting Effects of Low Temperature on Growth and Spore Germination in Gibberella circinata, the Cause of Pitch Canker in Pine Species. , 2008, Plant disease.