Jump to content

Hymenoscyphus fraxineus

From Wikipedia, the free encyclopedia
(Redirected from Hymenoscyphus pseudoalbidus)

Hymenoscyphus fraxineus
Scientific classification Edit this classification
Domain: Eukaryota
Kingdom: Fungi
Division: Ascomycota
Class: Leotiomycetes
Order: Helotiales
Family: Helotiaceae
Genus: Hymenoscyphus
Species:
H. fraxineus
Binomial name
Hymenoscyphus fraxineus
Baral et al. (2014)[1]
Synonyms
  • Chalara fraxinea (Kowalski et al., 2006)
  • Hymenoscyphus pseudoalbidus (Queloz et al., 2011)

Hymenoscyphus fraxineus is an ascomycete fungus that causes ash dieback, a chronic fungal disease of ash trees in Europe characterised by leaf loss and crown dieback in infected trees. The fungus was first scientifically described in 2006 under the name Chalara fraxinea. Four years later it was discovered that Chalara fraxinea is the asexual (anamorphic) stage of a fungus that was subsequently named Hymenoscyphus pseudoalbidus and then renamed as Hymenoscyphus fraxineus.

It is now believed that the trees reported to have died in Poland in 1992 were infected with this pathogen. It is now widespread in Europe, with up to 85% mortality rates recorded in plantations and 69% in woodlands.[2] It is closely related to a native fungus Hymenoscyphus albidus, which is harmless to European ash trees.[3][4] A 2016 report published in the Journal of Ecology posited that a combination of H. fraxineus and emerald ash borer attacks could result in the extinction of European ash trees.[5]

Genetics

[edit]

The fungus Hymenoscyphus fraxineus was first identified and described in 2006 under the name Chalara fraxinea.[6] In 2009, based on morphological and DNA sequence comparisons, Chalara fraxinea was suggested to be the asexual stage (anamorph) of the ascomycete fungus Hymenoscyphus albidus.[6] However, Hymenoscyphus albidus has been known from Europe since 1851 and is not regarded as pathogenic.[7] In 2010, through molecular genetic methods, the sexual stage (teleomorph) of the fungus was recognized as a new species and named Hymenoscyphus pseudoalbidus.[6] Four years later it was determined that "under the rules for the naming of fungi with pleomorphic life-cycles", the correct name should be Hymenoscyphus fraxineus.[1] Hymenoscyphus fraxineus is "morphologically virtually identical" to Hymenoscyphus albidus, but there are notable genetic differences between the two species.[8]

Crown dieback in a mature ash tree

The lifecycle of Hymenoscyphus fraxineus comprises two phases: sexual and asexual.[9] The asexual stage (anamorph) grows in affected trees attacking the bark and encircling twigs and branches.[9] The sexual, reproductive stage, (teleomorph) grows during summer on ash petioles in the previous year's fallen leaves.[7] The ascospores are produced in asci and are transmitted by wind, which may explain the rapid spread of the fungus.[7] The origins of the disease are uncertain,[10] but researchers are investigating the theory that the fungus originated in Asia, where ash trees are immune to the disease.[11] Genetic analysis of the fungus Lambertella albida which grows harmlessly on petioles of the Manchurian ash (Fraxinus mandschurica) in Japan, has shown that it is likely to be the same species as Hymenoscyphus fraxineus.[12]

In December 2012, teams from The Sainsbury Laboratory (TSL) and the John Innes Centre in Norwich sequenced the genome of the fungus. The sequence has been published on the website OpenAshDieBack and offers insights into the mechanisms of infection in trees by the fungus. The study identified toxin genes and other genes that may be responsible for the virulence of the fungus. In the long term researchers aim to find the genes that confer resistance to the pathogen in some ash trees.[13]

Ash dieback

[edit]
Yellow to red-brown necrosis in a five-year-old ash tree

Trees now believed to have been infected with this pathogen were reported dying in large numbers in Poland in 1992.[14] By the mid 1990s, the fungus had also been identified in Lithuania, Latvia and Estonia.[15] However, it was not until 2006 that the fungus's asexual stage, Chalara fraxinea, was first described by scientists, and 2010 before its sexual stage was described.[14] By 2008, the disease had also been discovered in Scandinavia, the Czech Republic, Slovenia, Germany, Austria and Switzerland.[16] By 2012, it had spread to Belgium, France, Hungary, Italy, Luxembourg,[17] the Netherlands, Romania, Russia, Britain and Ireland.[18][19] By 2016, it was already identified in central Norway, the northernmost distribution area of the ash tree.[20]

Up to 85% mortality rates due to H. fraxineus have been recorded in plantations and 69% in woodlands.[2] The disease has caused a large-scale decline of ash trees across Poland,[21] with evidence suggesting that in the long term "15 to 20 per cent of trees may survive without exhibiting symptoms."[22] In 2012, it was reported that the disease was reaching its peak in Sweden and Denmark, and that it was entering a post-decline (or chronic) phase in Latvia and Lithuania.[10] The disease was first observed in Denmark in 2002, and had spread throughout the country by 2005.[23] In 2009 it was estimated that 50 per cent of Denmark's ash trees were affected by crown dieback,[23] and a 2010 estimate stated that 60–90% of ash trees in Denmark were affected and may eventually disappear.[24] The disease was first reported in Sweden in 2003.[25] A survey conducted in Götaland in 2009 found that more than 50% of the trees had noticeable thinning and 25% were severely injured.[25]

A Danish study found that substantial genetic variation between ash trees resulted in significant differences in their susceptibility to the disease.[26] However, the proportion of trees with a high level of natural resistance seemed to be very low, probably less than 5%.[26] A Lithuanian trial based on the planting of trees derived from both Lithuanian and foreign populations of European ash found 10% of trees survived in all progeny trials to the age of eight years.[27]

So far the fungus has mainly affected the European ash (Fraxinus excelsior) and its cultivars, but it is also known to attack the narrow-leafed ash (Fraxinus angustifolia).[28] The manna ash (Fraxinus ornus) is also a known host, although it is less susceptible than the other European ash species.[28] Experiments in Estonia have shown that several North American ash species are susceptible, especially the black ash (Fraxinus nigra), and to a lesser extent the green ash (Fraxinus pennsylvanica).[28] The white ash (Fraxinus americana) and the Asian species known as Manchurian ash (Fraxinus mandschurica) showed only minor symptoms in the study.[28]

Symptoms and colonisation strategies

[edit]
Wilting of leaves caused by necrosis of the rachis (stem)
Small lens-shaped lesion on the bark of stem
Large lesion extending along a branch

Initially, small necrotic spots (without exudate) appear on stems and branches. These necrotic lesions then enlarge in stretched, perennial cankers on the branches, wilting, premature shedding of leaves and particularly in the death of the top of the crown.[29] Below the bark, necrotic lesions frequently extend to the xylem, especially in the axial and paratracheal ray tissue.[30] The mycelium can pass through the simple pits, perforating the middle lamella but damage to either the plasmalemma or cell walls was not observed.[31] The disease is often chronic but can be lethal.[18] It is particularly destructive to young ash plants, killing them within one growing season of the initial symptoms becoming visible.[32] Older trees can survive initial attacks, but tend to succumb eventually after several seasons of infection.[32]

Management

[edit]

There are currently no effective strategies for managing the disease, and most countries which have tried to control its spread have been unsuccessful.[11] The removal of trees in infected areas has little effect as the fungus lives and grows on leaf litter on the forest floor.[11] Research at the Swedish University of Agricultural Sciences suggests that the deliberate destruction of trees in an infected area can be counterproductive as it destroys the few resistant trees alongside the dying ones.[33] One approach to managing the disease may be to take branches from resistant trees and graft them to rootstock to produce seeds of resistant trees in a controlled environment.[33] A Lithuanian trial aimed at identifying disease-resistant trees has resulted in the selection of fifty such trees for the establishment of breeding populations of European ash in different provinces of Lithuania.[27] A breeding programme for resistant trees is a viable strategy[34] but the process of restoring the ash tree population across Europe with resistant trees is likely to take decades.[33]

Ash dieback in the United Kingdom

[edit]

The fungus was first detected in Britain during February 2012 at sites that had received saplings from nurseries within the preceding five years.[14] A ban on imports of ash from other European countries was imposed in October 2012 after infected trees were found in established woodland.[35] On 29 October Environment minister David Heath confirmed that 100,000 nursery trees and saplings had been deliberately destroyed.[11][36] The government also banned ash imports, but experts described this measure as "too little too late".[37] The UK Government Emergency Committee COBR convened on 2 November to address the crisis.[38] A survey of Scottish trees started in November 2012.[39] A 2020 study suggested that certain landscapes with hedgerows and woods made up of different types of tree resisted the disease better than areas mainly populated with ash trees.[40]

Government and Forestry Commission guidance

[edit]

The Forestry Commission has produced guidance[41] and requested people report[42] possible cases.

Comparisons have been made to the outbreak of Dutch elm disease in the 1960s and 1970s.[43] In 2012 it was estimated that up to 99% of the 90 million ash trees in the UK would be killed by the disease.[44]

On 9 November 2012 the United Kingdom Government presented its strategy. Environment Secretary Owen Paterson announced that the disease was acknowledged to be a long-term presence in the UK, and that efforts would be concentrated on slowing its spread. Young and newly planted trees with the disease would be destroyed; however, mature trees would not be removed due to the implications for wildlife that depends on the trees for their natural habitat. The strategy unveiled by Paterson included:

  • Reducing the rate of spread of the disease
  • Developing resistance to the disease in the native UK ash tree population
  • Encouraging the public and landowners to help monitor trees for signs of ash dieback.[45]

In March 2013 Owen Paterson announced that the United Kingdom Government would plant a quarter of a million ash trees in an attempt to identify strains of the species that are resistant to the fungus.[46]

In February 2016 the BBC program "Countryfile" presented a case study of enhanced resistance to ash dieback following soil treatment by injecting enriched "Biochar" - a type of charcoal. Over a three-year period, twenty trees had remained free of disease despite a severe infestation of the surrounding trees.[47][48]

In December 2016, writing in Nature,[49] Dr Richard Buggs reported that the common ash (Fraxinus excelsior) had been genetically sequenced for the first time and UK specimens appeared more resistant than Danish ones.[50]

In August 2018 Defra and the Forestry Commission announced that at Westonbirt Arboretum the fungus had been found infecting three new hosts: Phillyrea (mock privet), Phillyrea angustifolia (narrow-leaved mock privet) and Chionanthus virginicus (white fringetree).[51][52] These were the first findings on hosts other than Fraxinus anywhere in the world.[53] All three new hosts are in the same taxonomic family as ash, the Oleaceae.[51] The trees were all in the vicinity of infected European ash.[53] In response to the findings on the new hosts, Nicola Spence, the UK Chief Plant Health Office, said that, "Landscapers, gardeners and tree practitioners should be vigilant for signs of ash dieback on these new host species, and report suspicious findings through Tree Alert".[52]

In June 2019, Defra published a report summarising the current state of knowledge regarding ash dieback, and identified priority areas for future research.[54] In 2019 and 2020, the UK government and Future Trees Trust planted 3,000 ash trees in Hampshire to establish the Ash Archive. All the trees came from shoots of trees that demonstrated resistance to the fungus. The Ash Archive will form the basis of a breeding program.[55]

Ash dieback in Ireland

[edit]

On 12 October 2012 the Department of Agriculture, Food and the Marine confirmed the first recorded instance of the fungus in Ireland, at a plantation in County Leitrim.[56] Legislation was introduced in both Northern Ireland and the Republic of Ireland on 26 October banning the importation and movement of ash plants from infected parts of Europe.[56] By 23 September 2013, a survey conducted by the Irish Government revealed that the disease had been identified at ninety-six sites across the Republic of Ireland.[57] As of August 2021, Teagasc warns that: "The disease is now prevalent throughout most of the island of Ireland and is likely to cause the death of the majority of the ash trees over the next two decades."[58]

The first cases in Northern Ireland were confirmed at five sites in counties Down and Antrim on 16 November 2012.[59] By 4 December 2012 the disease had been confirmed at sixteen sites in counties Down, Antrim, Tyrone and Londonderry.[60]

Wider ecological knockon effects

[edit]

Due to the importance of F. excelsior as a host, Jönsson and Thor 2012 find that H. fraxineus is subjecting rare/threatened lichens to an unusually high (0.38) coextinction risk probability vis-a-vis the host tree in the wooded meadows of Gotland, Sweden.[61] Studies detected no signs of ash mortality compensation by the surviving trees, particularly in mixed forests, indicating a mid-term habitat loss and niche replacement of ash.[20]

See also

[edit]

References

[edit]
  1. ^ a b Baral, Hans-Otto; Queloz, Valentin K.; Hosoya, Tsuyoshi S. (June 2014). "Hymenoscyphus fraxineus, the correct scientific name for the fungus causing ash dieback in Europe". IMA Fungus. 5 (1). International Mycological Association: 79–80. doi:10.5598/imafungus.2014.05.01.09. PMC 4107900. PMID 25083409.
  2. ^ a b Coker, T; Rozsypálek, J; Edwards, A; Harwood, T; Butfoy, L; Buggs, R (2019). "Estimating mortality rates of European ash (Fraxinus excelsior) under the ash dieback (Hymenoscyphus fraxineus) epidemic". Plants People Planet. 1 (1): 48–58. doi:10.1002/ppp3.11.
  3. ^ Gross, A.; Grünig, C. R.; Queloz, V.; Holdenrieder, O. (2012). "A molecular toolkit for population genetic investigations of the ash dieback pathogen Hymenoscyphus pseudoalbidus". Forest Pathology. 42 (3): 252–264. doi:10.1111/j.1439-0329.2011.00751.x.
  4. ^ Brian Spooner; Peter Roberts (1 April 2005). Fungi. Collins. p. 246. ISBN 978-0-00-220152-0. Retrieved 31 October 2012.
  5. ^ Claire Marshall (23 March 2016). "Ash tree set for extinction in Europe". BBC News. Retrieved 23 March 2016.
  6. ^ a b c "FRAXBACK – Category: Chalara". FRAXBACK. Archived from the original on 4 August 2014. Retrieved 31 October 2012.
  7. ^ a b c "Hymenoscyphus pseudoalbidus". ETH – Forest Pathology and Dendrology. 14 April 2010. Archived from the original on 5 November 2012. Retrieved 31 October 2012.
  8. ^ Bengtsson, S. B. K.; Vasaitis, R.; Kirisits, T.; Solheim, H.; Stenlida, J. (2012). "Population structure of Hymenoscyphus pseudoalbidus and its genetic relationship to Hymenoscyphus albidus". Fungal Ecology. 5 (2): 147–153. doi:10.1016/j.funeco.2011.10.004.
  9. ^ a b "Chalara dieback of ash". Forestry Commission. Archived from the original on 5 September 2018. Retrieved 31 August 2015.
  10. ^ a b "Decline of Fraxinus excelsior in northern Europe (2010–2012)". SNS – Nordic Forest Research Co-operation Committee. Retrieved 31 October 2012.[permanent dead link‍]
  11. ^ a b c d "Are Europe's ash trees finished?". New Scientist. 31 October 2012. Retrieved 31 October 2012.
  12. ^ Zhao, Y.; Hosoya, T.; Baral, H.; Hosaka, K.; Kakishima, M. (2012). "Hymenoscyphus pseudoalbidus, the correct name for Lambertella albida reported from Japan". Mycotaxon. 122: 25–41. doi:10.5248/122.25.
  13. ^ Ash fungus genetic code unravelled – BBC News
  14. ^ a b c "Chalara dieback of ash (Chalara fraxinea)". Forestry Commission. Archived from the original on 5 September 2018. Retrieved 27 October 2012.
  15. ^ "Ash decline in Nordic and Baltic countries". Metla. 3 July 2007. Archived from the original on 17 June 2012. Retrieved 6 November 2012.
  16. ^ "Eschensterben alarmiert Forstexperten". Spiegel Online (in German). 6 November 2008. Retrieved 29 October 2012.
  17. ^ Cf. p. 35-36 in: Garnier-Delcourt, M., G. Marson, Ch. Reckinger, B. Schultheis & M.-T. Tholl, 2013. Notes mycologiques luxembourgeoises. VII. Bull. Soc. Nat. luxemb. 114 : 35-54. (Pdf 6.5 MB)
  18. ^ a b "Chalara fraxinea – Ash dieback". European and Mediterranean Plant Protection Organization. March 2012. Archived from the original on 17 July 2012. Retrieved 29 October 2012.
  19. ^ "Chalara ash dieback outbreak: Q&A". BBC News. 29 October 2012. Retrieved 31 October 2012.
  20. ^ a b Díaz-Yáñez, Olalla; Mola-Yudego, Blas; Timmermann, Volkmar; Tollefsrud, Mari Mette; Hietala, Ari; Oliva, Jonàs (2020). "The invasive forest pathogen Hymenoscyphus fraxineus boosts mortality and triggers niche replacement of European ash (Fraxinus excelsior)". Scientific Reports. 10 (1): 5310. Bibcode:2020NatSR..10.5310D. doi:10.1038/s41598-020-61990-4. PMC 7093550. PMID 32210276.
  21. ^ Vasaitis, R.; Lygis, V. (2008). "Emerging forest diseases in south-eastern Baltic Sea region" (PDF). Network of Climate Change Risks on Forests (FoRisk): SNS Workshop, Umea, Sweden.: 14–15. Archived from the original (PDF) on 2016-03-03. Retrieved 2012-11-06.
  22. ^ Cole Moreton (11 November 2012). "Ash dieback: the ruined Polish forest where deadly fungus began". The Telegraph. London. Retrieved 17 December 2012.
  23. ^ a b "Udryddelse truer asketræet" (in Danish). Naturstyrelsen. 6 June 2012. Archived from the original on 23 October 2012. Retrieved 9 January 2013.
  24. ^ "Workshop on Chalara fraxinea – Oslo, Norway, 2010-06-30/07-02". European and Mediterranean Plant Protection Organization. 2010. Archived from the original on 2013-01-15. Retrieved 6 November 2012.
  25. ^ a b "Den senaste om askskottsjukan". Svenska Trädföreningen. 2010. Archived from the original on 16 April 2013. Retrieved 6 November 2012.
  26. ^ a b "Ash trees that can survive the emerging infectious die-back disease". NBforest.info. 9 February 2010. Retrieved 31 October 2012.
  27. ^ a b Pliūra, A.; Lygis, V.; Suchockas, V.; Bartkevičius, E. (2011). "Performance of twenty four European Fraxinus excelsior populations in three Lithuanian progeny trials with a special emphasis on resistance to Chalara fraxinea". Baltic Forestry. 17 (1): 17–34. Archived from the original on 2018-09-04. Retrieved 2012-11-05.
  28. ^ a b c d "Update on ash dieback (Chalara fraxinea) in Europe: New confirmed hosts and description of the perfect state". North American Plant Protection Organisation. 10 November 2010. Retrieved 6 November 2012.
  29. ^ Bakys, R.; Vasaitis, R.; Barklund, P.; Ihrmark, K.; Stenlid, J. (1 April 2009). "Investigations concerning the role of Chalara fraxinea in declining Fraxinus excelsior". Plant Pathology. 58 (2): 284–292. doi:10.1111/j.1365-3059.2008.01977.x. S2CID 73530183.
  30. ^ Schumacher, J.; Kehr, R.; Leonhard, S. (1 September 2009). "Mycological and histological investigations of Fraxinus excelsior nursery saplings naturally infected by Chalara fraxinea". Forest Pathology. 40 (5): 419–429. doi:10.1111/j.1439-0329.2009.00615.x.
  31. ^ Dal Maso, E; Fanchin G; Mutto Accordi S; Scattolin L; Montecchio L (December 2012). "Ultrastructural modifications in Common ash tissues colonised by Chalara fraxinea". Phytopathologia Mediterranea. 51 (3): 599–606. Archived from the original on 2013-12-03. Retrieved 2013-01-21.
  32. ^ a b "Chalara dieback of ash – Questions and Answers". Forestry Commission. 16 October 2012. Archived from the original on 30 October 2012. Retrieved 29 October 2012.
  33. ^ a b c Tom Rowley (2 November 2012). "Trees that thrive amid killer fungus hold secret to saving threatened ash". The Telegraph. London. Archived from the original on 3 November 2012. Retrieved 4 November 2012.
  34. ^ Plumb, William J.; Coker, Timothy L. R.; Stocks, Jonathan J.; Woodcock, Paul; Quine, Christopher P.; Nemesio-Gorriz, Miguel; Douglas, Gerry C.; Kelly, Laura J.; Buggs, Richard J. A. (2019-07-17). "The viability of a breeding programme for ash in the British Isles in the face of ash dieback". Plants, People, Planet. 2: 29–40. doi:10.1002/ppp3.10060. ISSN 2572-2611.
  35. ^ David Batty and agencies (27 October 2012). "Ash tree ban may be too late to avert 'UK tragedy', says expert". The Guardian. London. Retrieved 29 October 2012.
  36. ^ "Ash dieback: 100,000 trees destroyed to halt spread". BBC News. 29 October 2012. Retrieved 29 October 2012.
  37. ^ Steven Swinford (30 Oct 2012). "British public could be banned from forests to save ash trees from fungus". Daily Telegraph. London. Archived from the original on 31 October 2012. Retrieved 31 Oct 2012.
  38. ^ "Ash dieback: Government Cobra meeting to tackle disease". BBC News. 2 November 2012. Retrieved 2 November 2012.
  39. ^ "Ash dieback disease: Survey of Scottish tree stocks launched". BBC News. 4 November 2012. Retrieved 5 November 2012.
  40. ^ Kinver, Mark (2020-05-08). "Some landscapes show resistance to ash dieback". BBC News. Retrieved 2020-05-11.
  41. ^ "Ash dieback (Hymenoscyphus fraxineus)".
  42. ^ "TreeAlert".
  43. ^ Tracy McVeigh and Josh Layton (27 October 2012). "More forest sites infected as ash disease takes hold". The Observer. London. Retrieved 29 October 2012.
  44. ^ Cormier, Z. (2012). "UK unveils plan to fight deadly ash disease". Nature. doi:10.1038/nature.2012.11790. S2CID 75216934.
  45. ^ Kinver, Mark; McGrath, Matt (9 November 2012). "Owen Paterson: Ash dieback will not be eradicated". BBC News. Retrieved 9 November 2012.
  46. ^ "Government to plant 250,000 trees to beat ash dieback". BBC News. 26 March 2013.
  47. ^ BBC One "Countryfile" 29 February 2016, accessed 24 April 2021
  48. ^ Biochar Found to Suppress Ash Dieback Archived 2021-04-24 at the Wayback Machine Permaculture 23 February 2016 accessed 24 April 2021
  49. ^ Buggs, Richard J. A.; Caccamo, Mario; Bancroft, Ian; Grant, Murray; Clark, Jo; Lee, Steve; Boshier, David; Downie, J. Allan; Kjær, Erik Dahl (January 2017). "Genome sequence and genetic diversity of European ash trees". Nature. 541 (7636): 212–216. Bibcode:2017Natur.541..212S. doi:10.1038/nature20786. hdl:10871/25034. ISSN 1476-4687. PMID 28024298.
  50. ^ Mark Kinver (26 December 2016). "Ash tree genome sequenced for first time". BBC News. Retrieved 27 December 2016.
  51. ^ a b Defra (7 August 2018). "Ash dieback found on three new host species of tree in the UK". Defra. Retrieved 9 August 2018.
  52. ^ a b "Ash dieback found on new tree species at Westonbirt". BBC. 7 August 2018.
  53. ^ a b "Chalara ash dieback on different ash species and non-ash hosts". Forest Research. 7 August 2018. Retrieved 9 August 2018.
  54. ^ "Conserving our ash trees and mitigating the impacts of pests and diseases of ash: A vision and high-level strategy for ash research". 6 June 2019. Retrieved 8 November 2019.
  55. ^ Pain, Stephanie (2020). "The accidental tree killers". Knowable Magazine. doi:10.1146/knowable-092120-1. S2CID 224939766.
  56. ^ a b "Ash dieback present in Co. Leitrim – statutory and voluntary measures introduced". National Biodiversity Data Centre. Archived from the original on 29 October 2013. Retrieved 5 November 2012.
  57. ^ "Ash Dieback (Chalara)". Archived from the original on 2013-10-29. Retrieved 2013-10-25.
  58. ^ "Ash Dieback Disease: Introduction". Teagasc. Archived from the original on 3 August 2021.
  59. ^ "Ash disease discovered at five Northern Ireland sites". BBC News. 16 November 2012. Retrieved 29 November 2012.
  60. ^ "Ash disease outbreaks in Northern Ireland stand at 16". BBC News. 4 December 2012. Retrieved 12 January 2013.
  61. ^ Oliva, Jonàs; Redondo, Miguel Ángel; Stenlid, Jan (2020-08-25). "Functional Ecology of Forest Disease". Annual Review of Phytopathology. 58 (1). Annual Reviews: 343–361. doi:10.1146/annurev-phyto-080417-050028. ISSN 0066-4286. PMID 32396761. S2CID 218618105.
[edit]
Wikimedia Commons has media related to Hymenoscyphus fraxineus.
Retrieved from "https://wiki.riteme.site/w/index.php?title=Hymenoscyphus_fraxineus&oldid=1258701109"