Hymenoscyphus pseudoalbidus, the causal agent of European ash dieback.

UNLABELLED The ascomycete Hymenoscyphus pseudoalbidus (anamorph Chalara fraxinea) causes a lethal disease known as ash dieback on Fraxinus excelsior and Fraxinus angustifolia in Europe. The pathogen was probably introduced from East Asia and the disease emerged in Poland in the early 1990s; the subsequent epidemic is spreading to the entire native distribution range of the host trees. This pathogen profile represents a comprehensive review of the state of research from the discovery of the pathogen and points out knowledge gaps and research needs. TAXONOMY Members of the genus Hymenoscyphus (Helotiales, Leotiomycetidae, Leotiomycetes, Ascomycota) are small discomycetes which form their ascomata on dead plant material. A phylogeny based on the internal transcribed spacers (ITSs) of the rDNA indicated the avirulent Hymenoscyphus albidus, a species native to Europe, as the closest relative of H. pseudoalbidus. SYMPTOMS Hymenoscyphus pseudoalbidus causes necrotic lesions on leaves, twigs and stems, eventually leading to wilting and dieback of girdled shoots. Bark lesions are characterized by a typical dark- to cinnamon-brown discoloration. LIFE CYCLE Hymenoscyphus pseudoalbidus is heterothallic and reproduces sexually on ash petioles in the litter once a year. Ascospores are wind dispersed and infect ash leaves during the summer. The asexual spores only serve as spermatia. TOOLS AND TECHNIQUES The most important techniques for fungal handling, such as detection, isolation, culturing, storage, crossing and ascocarp production, are briefly described. MANAGEMENT Once the disease is established, management is hardly possible. The occurrence of a small fraction of partially tolerant trees constitutes hope for resistance breeding in the future. Healthy-looking trees should be preserved.

[1]  T. Kowalski,et al.  Genetic variability of Chalara fraxinea, dieback cause of European ash (Fraxinus excelsior L.) , 2010, Mycological Progress.

[2]  O. Mittapalli,et al.  Evaluation of Reference Genes for Expression Studies in Ash (Fraxinus spp.) , 2011, Plant Molecular Biology Reporter.

[3]  T. Sieber Endophytic fungi in forest trees: are they mutualists? , 2007 .

[4]  O. Holdenrieder,et al.  The teleomorph of Chalara fraxinea, the causal agent of ash dieback , 2009 .

[5]  T. Sieber,et al.  ENDOPHYTIC FUNGI IN SCOTS PINE NEEDLES : SPATIAL VARIATION AND CONSEQUENCES OF SIMULATED ACID RAIN , 1994 .

[6]  L. J. Crawford,et al.  Molecular analysis of evolutionary changes in populations of Ophiostma novo-ulmi , 2004 .

[7]  Remigijus Bakys,et al.  Investigations concerning the role of Chalara fraxinea in declining Fraxinus excelsior , 2009 .

[8]  D. Jurc,et al.  Chalara fraxinea causing common ash dieback newly reported in Slovenia , 2009 .

[9]  O. Holdenrieder,et al.  A molecular toolkit for population genetic investigations of the ash dieback pathogen Hymenoscyphus pseudoalbidus , 2012 .

[10]  Four new species of the genus Hymenoscyphus (fungi) based on morphology and molecular data , 2012, Science China Life Sciences.

[11]  S. Raffaele,et al.  Genome evolution in filamentous plant pathogens: why bigger can be better , 2012, Nature Reviews Microbiology.

[12]  B. McDonald,et al.  Pathogen population genetics, evolutionary potential, and durable resistance. , 2002, Annual review of phytopathology.

[13]  J. Henson,et al.  THE DARK SIDE OF THE MYCELIUM: Melanins of Phytopathogenic Fungi. , 1999, Annual review of phytopathology.

[14]  M. Gijzen,et al.  Nep1-like proteins from plant pathogens: recruitment and diversification of the NPP1 domain across taxa. , 2006, Phytochemistry.

[15]  Joost A. Stalpers,et al.  Ainsworth and Bisby's dictionary of the fungi: 9th edition. , 1995 .

[16]  L. Rabenhorst,et al.  Ascomyceten : Hysteriaceen und Discomyceten , 1896 .

[17]  W. Cleveland LOWESS: A Program for Smoothing Scatterplots by Robust Locally Weighted Regression , 1981 .

[18]  L. V. McKinney,et al.  Genetic resistance to Hymenoscyphus pseudoalbidus limits fungal growth and symptom occurrence in Fraxinus excelsior , 2012 .

[19]  T. Giraud,et al.  Sex, outcrossing and mating types: unsolved questions in fungi and beyond , 2012, Journal of evolutionary biology.

[20]  M. Elgar,et al.  The Use of Corridors by Mammals in Fragmented Australian Eucalypt Forests , 1997 .

[21]  Bernardo J. Clavijo,et al.  Crowdsourcing genomic analyses of ash and ash dieback – power to the people , 2013, GigaScience.

[22]  J. P. Skovsgaard,et al.  Associations among symptoms of dieback in even-aged stands of ash (Fraxinus excelsior L.) , 2010 .

[23]  E. Krause,et al.  Rapid In-Vitro and In-Vitro Detection of Chalara fraxinea by Means of Mass Spectrometric Techniques , 2013 .

[24]  Pierre F Andersson,et al.  Viridin-like steroids from Hymenoscyphus pseudoalbidus. , 2013, Phytochemistry.

[25]  B. Thomma,et al.  Fungal LysM effectors: extinguishers of host immunity? , 2009, Trends in microbiology.

[26]  J. Schumacher The general situation regarding ash dieback in Germany and investigations concerning the invasion and distribution strategies of Chalara fraxinea in woody tissue , 2011 .

[27]  O. Holdenrieder,et al.  Eine neue Pilzkrankheit an Esche in Europa | A new fungal disease of ash in Europe , 2008 .

[28]  H. Butin Krankheiten der Wald- und Parkbäume : Diagnose - Biologie - Bekämpfung , 1989 .

[29]  K. Przybył,et al.  Frost Injury as a Possible Inciting Factor in Bud and Shoot Necroses of Fraxinus excelsior L. , 2005 .

[30]  I. Sache,et al.  Species diversity and drivers of spread of alien fungi (sensu lato) in Europe with a particular focus on France , 2009, Biological Invasions.

[31]  J. Burdon,et al.  Variation in infectivity and aggressiveness in space and time in wild host–pathogen systems: causes and consequences , 2012, Journal of evolutionary biology.

[32]  A. Gross,et al.  Reproductive mode and life cycle of the ash dieback pathogen Hymenoscyphus pseudoalbidus. , 2012, Fungal genetics and biology : FG & B.

[33]  T. Poland,et al.  Breeding strategies for the development of emerald ash borer - resistant North American ash , 2012 .

[34]  C. Robin,et al.  Chestnut blight in Europe: Diversity of Cryphonectria parasitica, hypovirulence and biocontrol , 2001 .

[35]  Thomas Kirisits,et al.  Ash dieback: pathogen spread and diurnal patterns of ascospore dispersal, with special emphasis on Norway. , 2011 .

[36]  T. Kowalski O zamieraniu jesionow , 2001 .

[37]  F. Asiegbu,et al.  The effect of latitude, season and needle-age on the mycota of Scots pine (Pinus sylvestris) in Finland , 2011 .

[38]  A. Chandelier,et al.  Detection of Chalara fraxinea in common ash (Fraxinus excelsior) using real time PCR , 2010 .

[39]  Sarah Calvo,et al.  Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis , 2006, Nature.

[40]  I. Szabó First report of Chalara fraxinea affecting common ash in Hungary , 2009 .

[41]  C. Leach,et al.  A practical guide to the effects of visible and ultraviolet light on fungi , 1971 .

[42]  P. Sunnucks,et al.  Efficient genetic markers for population biology. , 2000, Trends in ecology & evolution.

[43]  L. V. McKinney,et al.  Presence of natural genetic resistance in Fraxinus excelsior (Oleraceae) to Chalara fraxinea (Ascomycota): an emerging infectious disease , 2011, Heredity.

[44]  L. Nageleisen,et al.  Occurrence of Hymenoscyphus pseudoalbidus on infected ash logs , 2012 .

[45]  T. Sieber,et al.  Mycobiota in symptomless needles of Pinus mugo ssp. uncinata , 1999 .

[46]  T. Kirisits,et al.  Hymenoscyphus albidus is not associated with an anamorphic stage and displays slower growth than Hymenoscyphus pseudoalbidus on agar media , 2013 .

[47]  T. Kowalski,et al.  Studies on secondary metabolite producedby Chalara fraxinea and its phytotoxic influence on Fraxinus excelsior , 2010 .

[48]  L. V. McKinney,et al.  Adaptive potential of ash (Fraxinus excelsior) populations against the novel emerging pathogen Hymenoscyphus pseudoalbidus , 2011, Evolutionary applications.

[49]  K. H. Wong,et al.  Transcriptional control of nmrA by the bZIP transcription factor MeaB reveals a new level of nitrogen regulation in Aspergillus nidulans , 2007, Molecular microbiology.

[50]  J. Schumacher,et al.  Mycological and histological investigations of Fraxinus excelsior nursery saplings naturally infected by Chalara fraxinea. , 2009 .

[51]  J. Stenlid,et al.  Natural infection of Fraxinus excelsior seeds by Chalara fraxinea. , 2012 .

[52]  K. Larsson,et al.  Wood-inhabiting fungi in stems of Fraxinus excelsior in declining ash stands of northern Lithuania, with particular reference to Armillaria cepistipes , 2005 .

[53]  S. Opiyo,et al.  Interspecific Comparison of Constitutive Ash Phloem Phenolic Chemistry Reveals Compounds Unique to Manchurian Ash, a Species Resistant to Emerald Ash Borer , 2012, Journal of Chemical Ecology.

[54]  D. Jurc,et al.  Temperature effect on Chalara fraxinea: heat treatment of saplings as a possible disease control method , 2013 .

[55]  T. Kirisits,et al.  Ash dieback caused by Hymenoscyphus pseudoalbidus in a seed plantation of Fraxinus excelsior in Austria , 2012 .

[56]  C. Brasier The population biology of Dutch elm disease: its principle features and some implications for other host-pathogen systems. , 1986 .

[57]  J. Pajares,et al.  Effects of associated fungi Sclerophoma pythiophila and Cenangium ferruginosum on Gremmeniella abietina dieback in Spain , 2007 .

[58]  B. Schulz,et al.  Hymenoscyphus pseudoalbidus and Hymenoscyphus albidus: viridiol concentration and virulence do not correlate , 2014 .

[59]  T. Kirisits,et al.  The current situation of ash dieback caused by Chalara fraxinea in Austria , 2009 .

[60]  S. Pietravalle,et al.  Plant health and global change – some implications for landscape management , 2010, Biological reviews of the Cambridge Philosophical Society.

[61]  G. Boland,et al.  Population structure of the butternut canker fungus, Ophiognomonia clavigignenti-juglandacearum, in North American forests , 2012, Ecology and evolution.

[62]  J. Stenlid,et al.  Detection of Chalara fraxinea from tissue of Fraxinus excelsior using species-specific ITS primers , 2010 .

[63]  T. Kirisits,et al.  Ash dieback associated with Hymenoscyphus pseudoalbidus in forest nurseries in Austria , 2012 .

[64]  T. Harwood,et al.  Learning from history, predicting the future: the UK Dutch elm disease outbreak in relation to contemporary tree disease threats , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[65]  Peter Wipf,et al.  Structure reassignment of the fungal metabolite TAEMC161 as the phytotoxin viridiol. , 2003, Journal of natural products.

[66]  A. Phillips,et al.  Botryosphaeria and Related Taxa Causing Oak Canker in Southwestern Spain. , 2003, Plant disease.

[67]  J. Stenlid,et al.  Isolation, identification and necrotic activity of viridiol from Chalara fraxinea, the fungus responsible for dieback of ash , 2010 .

[68]  K. D. Macdonald,et al.  The genetics of Aspergillus nidulans. , 1953, Advances in genetics.

[69]  B. Marçais,et al.  Chalara fraxinea is an invasive pathogen in France , 2011, European Journal of Plant Pathology.

[70]  B. Metzler,et al.  Temporal development of ash dieback symptoms and spatial distribution of collar rots in a provenance trial of Fraxinus excelsior , 2013, European Journal of Forest Research.

[71]  M. Ueda,et al.  Making headway in understanding pine wilt disease: what do we perceive in the postgenomic era? , 2013, Journal of bioscience and bioengineering.

[72]  T. Kirisits,et al.  The ash dieback pathogen Hymenoscyphus pseudoalbidus is associated with leaf symptoms on ash species (Fraxinus spp.) , 2012 .

[73]  J. Stenlid,et al.  Root rot, associated fungi and their impact on health condition of declining Fraxinus excelsior stands in Lithuania , 2011 .

[74]  F. Meier,et al.  Chalara-Krankheit an Eschen. Das Triebsterben der Esche in der Schweiz , 2009 .

[75]  J. Webber Experimental studies on factors influencing the transmission of Dutch elm disease , 2004 .

[76]  T. Kowalski,et al.  Badania nad zamieraniem jesionu w drzewostanach nadleśnictwa Rokita , 2012 .

[77]  David Lonsdale,et al.  Tree diseases and landscape processes: the challenge of landscape pathology. , 2004, Trends in ecology & evolution.

[78]  T. Kowalski,et al.  Chalara fraxinea sp. nov. associated with dieback of ash (Fraxinus excelsior) in Poland , 2006 .

[79]  八谷 正義 FREMDLANDISCHE WALD-UND PARKBAUME Ein Buch fur alle Forstwirte und Dendrologen von Dr. phil. Carl Alwin Schenck Verlag von Paul Parey in Berlin 1939(價格 RM.46.50) , 1939 .

[80]  S. Ōmura,et al.  Materials for the fungus flora of Japan (47) , 1994 .

[81]  G. Thor,et al.  Estimating Coextinction Risks from Epidemic Tree Death: Affiliate Lichen Communities among Diseased Host Tree Populations of Fraxinus excelsior , 2012, PloS one.

[82]  T. Kowalski,et al.  Badania nad zamieraniem jesionu (Fraxinus excelsior L.) w drzewostanach Nadleśnictwa Włoszczowa [The studies on ash dying (Fraxinus excelsior L.) in the Włoszczowa Forest Unit stands] , 2012 .

[83]  J. Stenlid,et al.  Occurrence and pathogenicity of fungi in necrotic and non-symptomatic shoots of declining common ash (Fraxinus excelsior) in Sweden , 2008, European Journal of Forest Research.

[84]  P. Cortesi,et al.  Mixed mating in natural populations of the chestnut blight fungus, Cryphonectria parasitica , 2004, Heredity.

[85]  T. Sieber,et al.  Cryptic speciation in Hymenoscyphus albidus , 2011 .

[86]  Christian Schlötterer,et al.  The evolution of molecular markers — just a matter of fashion? , 2004, Nature Reviews Genetics.

[87]  W. Knogge,et al.  When and how to kill a plant cell: infection strategies of plant pathogenic fungi. , 2011, Journal of plant physiology.

[88]  H. Solheim,et al.  The invasive ash dieback pathogen Hymenoscyphus pseudoalbidus exerts maximal infection pressure prior to the onset of host leaf senescence , 2013 .

[89]  L. V. McKinney,et al.  Rapid invasion by an aggressive pathogenic fungus (Hymenoscyphus pseudoalbidus) replaces a native decomposer (Hymenoscyphus albidus): a case of local cryptic extinction? , 2012 .

[90]  T. Hosoya,et al.  Hymenoscyphus pseudoalbidus, the correct name for Lambertella albida reported from Japan. , 2013 .

[91]  T. Kirisits,et al.  Population structure of Hymenoscyphus pseudoalbidus and its genetic relationship to Hymenoscyphus albidus , 2012 .

[92]  S. Jose,et al.  Ecological consequences of an exotic fungal disease in eastern U.S. hardwood forests. , 2010 .

[93]  O. Holdenrieder,et al.  Pathogenicity of Chalara fraxinea. , 2009 .

[94]  P. Baldrian Fungal laccases - occurrence and properties. , 2006, FEMS microbiology reviews.

[95]  G. Daniel,et al.  Light and scanning electron microscopy studies of the early infection stages of Hymenoscyphus pseudoalbidus on Fraxinus excelsior. , 2013 .

[96]  T. Sieber,et al.  Cryptic speciation in Hymenoscyphus albidus (vol. 41, pa 133, 2011) , 2012 .

[97]  C. Brasier,et al.  Intercontinental Spread and Continuing Evolution of the Dutch Elm Disease Pathogens , 2000 .

[98]  R. W. Jones,et al.  Conversion of viridin to viridiol by viridin-producing fungi. , 1987, Canadian journal of microbiology.

[99]  Pierre F. Andersson,et al.  B-norsteroids from Hymenoscyphus pseudoalbidus , 2012, Molecules.

[100]  Cyril Dutech,et al.  Finding Single Copy Genes Out of Sequenced Genomes for Multilocus Phylogenetics in Non-Model Fungi , 2011, PloS one.

[101]  D. Herms,et al.  Interspecific Variation in Resistance to Emerald Ash Borer (Coleoptera: Buprestidae) Among North American and Asian Ash (Fraxinus spp.) , 2008, Environmental entomology.

[102]  T. Kowalski,et al.  Morphologial variation in colonies of Chalara fraxinea isolated from ash (Fraxinus excelsior L.) stems with symptoms of dieback and effects of temperature on colony growth and structure , 2012 .

[103]  K. Przybył Fungi associated with necrotic apical parts of Fraxinus excelsior shoots , 2002 .

[104]  O. Holdenrieder,et al.  On the longevity of Hymenoscyphus pseudoalbidus in petioles of Fraxinus excelsior. , 2013 .

[105]  A. Mayer,et al.  Laccase: new functions for an old enzyme. , 2002, Phytochemistry.

[106]  E. Limpert Dispersal of cereal mildews across Europe , 1999 .

[107]  O. Holdenrieder,et al.  European ash (Fraxinus excelsior) dieback - a conservation biology challenge. , 2013 .

[108]  S. Neuvonen,et al.  Interactions of Gremmeniella abietina and endophytic fungi in shoots of Scots pine trees treated with simulated acid rain , 1995 .

[109]  V. Lygis,et al.  Performance of twenty four European Fraxinus excelsior populations in three Lithuanian progeny trials with a special emphasis on resistance to Chalara fraxinea. , 2011 .

[110]  R. Ennos,et al.  Variation in host resistance and pathogen selective value in the interaction between Pinus sylvestris and the fungus Crumenulopsis sororia , 2003, Heredity.

[111]  C. Dunn The Elms: "Breeding,Conservation, And Disease Management" , 2012 .

[112]  L. Stener Clonal differences in susceptibility to the dieback of Fraxinus excelsior in southern Sweden , 2013 .

[113]  D. Hibbett,et al.  Evolution of helotialean fungi (Leotiomycetes, Pezizomycotina): a nuclear rDNA phylogeny. , 2006, Molecular phylogenetics and evolution.

[114]  R. Drenkhan,et al.  First record of Chalara fraxinea in Finland and genetic variation among isolates sampled from Åland, mainland Finland, Estonia and Latvia , 2011 .

[115]  A. J. Hayes,et al.  The prediction of Crumenulopsis sororia (Karst.) Groves. Incidence on lodgepole pine (Pinus contorta Dougl.) using multiple regression techniques , 1981 .

[116]  M. Wingfield,et al.  Micro‐ and macrospatial scale analyses illustrates mixed mating strategies and extensive geneflow in populations of an invasive haploid pathogen , 2010, Molecular ecology.

[117]  P. Savill,et al.  Ash Species in Europe: Biological Characteristics and Practical Guidelines for Sustainable Use , 2005 .

[118]  E. D. Maso,et al.  Ultrastructural modifications in Common ash tissues colonised by Chalara fraxinea , 2012 .

[119]  R. Drenkhan,et al.  New host species for Chalara fraxinea , 2010 .

[120]  T. Cech,et al.  Biogeographical patterns and determinants of invasion by forest pathogens in Europe. , 2013, The New phytologist.

[121]  T. Kirisits,et al.  Chalara fraxinea associated with dieback of narrow‐leafed ash (Fraxinus angustifolia) , 2010 .

[122]  C. K. Campbell,et al.  Evaluation of the Viability of Pathogenic Filamentous Fungi after Prolonged Storage in Sterile Water and Review of Recent Published Studies on Storage Methods , 2006, Mycopathologia.

[123]  O. Holdenrieder,et al.  Rapid in planta detection of Chalara fraxinea by a real-time PCR assay using a dual-labelled probe , 2009, European Journal of Plant Pathology.