Vol. 65 No. 2 (2026)
Articles

Genetic diversity and pathogenicity of Fusarium and Neocosmospora associated with cultivated and wild Asparagus officinalis in The Netherlands

PDF
  • Marcelo SANDOVAL-DENIS,
  • Mark ZWART,
  • Roel BROUWER,
  • Johannes Z. GROENEWALD,
  • Wilfried JONKERS,
  • Diana KATSCHNIG,
  • Wietse DE BOER,
  • Paolina GARBEVA,
  • Pedro W. CROUS
Marcelo SANDOVAL-DENIS
Westerdijk Fungal Biodiversity Institute, Uppsalalaan 8, 3584 CT, Utrecht, The Netherlands
Mark ZWART
Netherlands Institute of Ecology (NIOO-KNAW), 6708 PB, Wageningen, The Netherlands
Roel BROUWER
Westerdijk Fungal Biodiversity Institute, Uppsalalaan 8, 3584 CT, Utrecht, The Netherlands
Johannes Z. GROENEWALD
Westerdijk Fungal Biodiversity Institute, Uppsalalaan 8, 3584 CT, Utrecht, The Netherlands
Wilfried JONKERS
Bejo Zaden B.V., 1749 CZ, Warmenhuizen, The Netherlands
Diana KATSCHNIG
Bejo Zaden B.V., 1749 CZ, Warmenhuizen, The Netherlands
Wietse DE BOER
Netherlands Institute of Ecology (NIOO-KNAW), 6708 PB, Wageningen, The Netherlands
Paolina GARBEVA
Netherlands Institute of Ecology (NIOO-KNAW), 6708 PB, Wageningen, The Netherlands
Pedro W. CROUS
Westerdijk Fungal Biodiversity Institute, Uppsalalaan 8, 3584 CT, Utrecht, The Netherlands
DOI: https://doi.org/10.36253/phyto-17513
Categories

Published 2026-09-10

Keywords

  • Asparagaceae,
  • fungal diversity,
  • fusarioid,
  • pathogens,
  • phylogeny

How to Cite

[1]
M. SANDOVAL-DENIS, “Genetic diversity and pathogenicity of Fusarium and Neocosmospora associated with cultivated and wild Asparagus officinalis in The Netherlands”, Phytopathol. Mediterr., vol. 65, no. 2, pp. 343–358, Sep. 2026.

Copyright (c) 2026 Marcelo SANDOVAL-DENIS, Mark ZWART, Roel BROUWER, Johannes Z. GROENEWALD, Wilfried JONKERS, Diana KATSCHNIG, Wietse DE BOER, Paolina GARBEVA, Pedro W. CROUS

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

Crossref
Scopus
Google Scholar
Europe PMC

Funding data

Abstract

Fusarium crown and root rot is one of the main threats to asparagus production worldwide. The aetiology of the disease, attributed to several species of Fusarium and Neocosmospora, has not been re-evaluated in the context of recent advances in Fusarium taxonomy, and relevant studies in The Netherlands are scarce and outdated. Asparagus officinalis plants and associated soil samples were assessed from 38 cultivated fields and one location where this plant naturally occurs in The Netherlands. A total of 164 specimens were obtained yielding 551 fungal strains. Fungal identification according to DNA sequencing and phylogenetic analyses based on fragments of the translation elongation factor 1-alpha (tef1) and the DNA-directed RNA polymerase II second largest subunit (rpb2) showed that these isolates belonged to 20 taxa (Fusarium acuminatum, F. annulatum, F. avenaceum, F. carminascens, F. celtidicola, F. clavus, F. cugenangense, F. culmorum, F. equiseti, F. flagelliforme, F. flocciferum, F. inflexum, F. nirenbergiae, F. odoratissimum, F. oxysporum, F. redolens, F. vanleeuwenii, Neocosmospora geoasparagicola, N. solani and N. stercicola), of which 11 species (Fusarium avenaceum, F. carminascens, F. celtidicola, F. clavus, F. cugenangense, F. flagelliforme, F. flocciferum, F. inflexum, F. odoratissimum, F. vanleeuwenii and N. stercicola) are first reports on A. officinalis. These results, and testing of Koch’s postulates on A. officinallis plantlets, showed that F. annulatum, F. culmorum, F. redolens, F. nirenbergiae and N. solani were the most prevalent and aggressive species. In contrast, although F. oxysporum is pathogenic to A. officinalis, it was among the least prevalent species encountered in this study.

PDF

Downloads

Download data is not yet available.

References

  1. Aegerter B.J., Davis R.M., Natwick E.T., Smith R.F., Baldwin R.A., 2016. Fusarium crown and root rot. In: Pest Management Guidelines: Asparagus. (Aegerter B, Davis R, Natwick E, et al., ed.). UC ANR Publication 3435. Davis, California, USA.
  2. Baayen R.P., van den Boogert P.H.J.F., Bonants P.J.M., Poll J.T.K, Blok W.J., Waalwijk C., 2000. Fusarium redolens f. sp. asparagi, causal agent of asparagus root rot, crown rot and spear rot. European Journal of Plant Pathology 106: 907–912. https://doi.org/10.1023/A:1008766707266
  3. Bilai V.I., 1955. The fusaria (biology and systematics). Akademia Naukwe Ukrainskii, SSR, Kiev.
  4. Blok W.J., Bollen G.J., 1995. Fungi on roots and stem bases of asparagus in the Netherlands: species and pathogenicity. European Journal of Plant Pathology 101: 15–24. https://doi.org/10.1007/BF01876090
  5. Blok W.J., Bollen G.J., 1996. Etiology of asparagus replant-bound early decline. European Journal of Plant Pathology 102: 87–98. https://doi.org/10.1007/BF01877119
  6. Borrego-Benjumea A., Basallote-Ureba M.J., Melero-Vara J.M., Abbasi P.A., 2014. Characterization of Fusarium isolates from Asparagus fields in southwestern Ontario and influence of soil organic amendments on Fusarium crown and root rot. Ecology and Epidemiology 104(4): 403–415. https://doi.org/10.1094/PHYTO-08-13-0231-R
  7. Brizuela A.M., De la Lastra E., Marín-Guirao J.I., Gálvez L., de Cara-García M., … Palmero D., 2020. Fusarium consortium populations associated with asparagus crop in Spain and their role on field decline syndrome. Journal of Fungi 6(4): 336. https://doi.org/10.3390/jof6040336
  8. Buitrago-Acosta M.C., Minier D.H., Getson S., Medina-Mora C.M., Hausbeck M.K., 2025. Fusarium spp. associated with asparagus crowns and the influence of the preplant fumigant metam-sodium in Michigan crown nurseries. Annals of Applied Biology 186(3): 323–333. https://doi.org/10.1111/aab.12971
  9. Centraal Bureau voor de Statistiek (CBS), 2025. Vegetables; yield and cultivated area per kind of vegetable. Retrieved November 19, 2025, from https://www.cbs.nl/en-gb/figures/detail/37738ENG
  10. Chehri K., Salleh B., Zakaria L., 2014. Fusarium virguliforme, a soybean sudden death syndrome fungus in Malaysian soil. Australasian Plant Disease Notes 9(1): 1–7 https://doi.org/10.1007/s13314-014-0128-z
  11. Cohen S.I., Heald F.D., 1941. A wilt and root rot of asparagus caused by Fusarium oxysporum Schlecht. Plant Disease Reporter 25: 50–509.
  12. Corpas-Hervias C., Meloro-Vara J., Molinero-Ruiz M., Zurera-Muñoz C., Basallote-Ureba M.J., 2006. Characterization of isolates of Fusarium spp. obtained from Asparagus in Spain. Plant Disease 90: 1441–1451. https://doi.org/10.1094/PD-90-1441
  13. Crous P.W., Lombard L., Sandoval-Denis M., Seifert K.A., Schroers H-J., … Thines M., 2021. Fusarium: more than a node or a foot cell. Studies in Mycology 98: 100116. https://doi.org/10.1016/j.simyco.2021.100116
  14. Crous P.W., Sandoval-Denis M., Costa M.M., Groenewald J.Z., van Iperen A.L., … Thines M., 2022. Fusarium and allied fusarioid taxa (FUSA). 1. Fungal Systematics and Evolution 9: 161–200 https://doi.org/10.3114/fuse.2022.09.08
  15. Crous P.W., Verkley G.J.M., Groenewald J.Z., Houbraken J., 2019. Fungal Biodiversity. Utrecht, The Netherlands: Westerdijk Fungal Biodiversity Institute.
  16. Damicone J.P., Manning W.J., 1985. Frequency and pathogenicity of Fusarium spp. isolated from first-year asparagus grown from transplants. Plant Disease 69: 413–416 https://doi.org/10.1094/PD-69-413
  17. Elmer W.H., 1990. Fusarium proliferatum as a causal agent in fusarium crown and root rot of asparagus. Plant Disease 74: 938. https://doi.org/10.1094/PD-74-0938E
  18. Elmer W.H., Summerell B.A., Burgess L.W., Backhouse D., Abubaker A.A., 1997. Fusarium species associated with asparagus crowns and soil in Australia and New Zealand. Australasian Plant Pathology 26: 255–261. https://doi.org/10.1071/AP97041
  19. Elmer W.H., 2015. Management of Fusarium crown and root rot of asparagus. Crop Protection 73: 2–6. https://doi.org/10.1016/j.cropro.2014.12.005
  20. Farr D.F., Rossman A.Y., Castlebury L.A., 2023. United States national fungus collections fungus-host dataset. Ag Data Commons. Retrieved 2023-09-15, from https://fungi.ars.usda.gov/
  21. Gordon W.L., 1952. The occurrence of Fusarium species in Canada. II. Prevalence and taxonomy of Fusarium species in cereal seed. Canadian Journal of Botany 30(2): 209–251. https://doi.org/10.1139/b52-018
  22. Groenewald M., Lombard L., de Vries M., Giraldo A., Smith M., Crous PW., 2018. Diversity of yeast species from Dutch garden soil and the description of six novel Ascomycetes. FEMS Yeast Research 18(7): foy076. https://doi.org/10.1093/femsyr/foy076
  23. Han S.L., Wang M.M., Ma Z.Y., Raza M., Zhao P., … Cai L., 2023. Fusarium diversity associated with diseased cereals in China, with an updated phylogenomic assessment of the genus. Studies in Mycology 104: 87–148. https://doi.org/10.3114/sim.2022.104.02
  24. Hoang D.T., Chernomor O., von Haeseler A., Minh B.Q., Vinh L.S., 2018. UFBoot2: improving the ultrafast bootstrap approximation. Molecular Biology and Evolution 35(2): 518–522. https://doi.org/10.1093/molbev/msx281
  25. Kalyaanamoorthy S., Minh B.Q., Wong T.K.F., von Haeseler A., Jermiin L.S., 2017. ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods 14(6): 587–589. https://doi.org/10.1038/nmeth.4285
  26. Katoh K., Standley D.M. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30(4): 772–780. https://doi.org/10.1093/molbev/mst010
  27. Liu Y.J., Whelen S., Hall B.D., 1999. Phylogenetic relationships among ascomycetes: evidence from an RNA polymerse II subunit. Molecular Phylogenetics and Evolution 16(12): 1799–1808. https://doi.org/10.1093/oxfordjournals.molbev.a026092
  28. Lombard L., Sandoval-Denis M., Lamprecht S.C., Crous P.W., 2019. Epitypification of Fusarium oxysporum: clearing the taxonomic chaos. Persoonia 43: 1–47. https://doi.org/10.3767/persoonia.2019.43.01
  29. Lombard L., van der Merwe N.A., Groenewald J.Z., Crous P.W., 2015. Generic concepts in Nectriaceae. Studies in Mycology 80: 189–245. https://doi.org/10.1016/j.simyco.2014.12.002
  30. Lori G., Wolcan S., Mónaco, C.I., 1998. Fusarium moniliforme and F. proliferatum isolated from crown and root rot of asparagus and their association with asparagus decline in Argentina. Plant Disease 82(12): 1405. https://doi.org/10.1094/PDIS.1998.82.12.1405A
  31. McTaggart A.R., James T.Y., Shivas R.G., Drenth A., Wingfield B.D., … Duong T.A., 2021. Population genomics reveals historical and ongoing recombination in the Fusarium oxysporum species complex. Studies in Mycology 99: 100132. https://doi.org/10.1016/j.simyco.2021.100132
  32. Mendes M.A.S., da Silva V.L., Dianese J.C., Ferreira, M.A.S.V, dos Santos C.E.N., … Castro C., 1998. Fungos em Plantas no Brasil. Embrapa-SPI/Embrapa-Cenargen, Brasilia
  33. Miller M.A., Pfeiffer W., Schwartz T., 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov. 2010, New Orleans, LA pp. 1–8.
  34. Minh B.Q., Schmidt H.A., Chernomor O., Schrempf D., Woodhams M.D., … Lanfear R., 2020. IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution 37: 1530–1534. https://doi.org/10.1093/molbev/msaa015
  35. Nahiyan A.S.M., Boyer L.R., Jeffries P., Matsubara Y., 2011. PCR-SSCP analysis of Fusarium diversity in asparagus decline in Japan. European Journal of Plant Pathology 130: 197–203. https://doi.org/10.1007/s10658-011-9745-y
  36. Nylander J.A.A., 2004. MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University.
  37. Nirenberg H.I., 1976. Untersuchungen über die morphologische und biologische differenzierung in der Fusarium-Sektion Liseola. Mitteilungen der Biologischen Bundesanstalt für Land- und Forstwirtschaft Berlin-Dahlem 169: 1–117.
  38. O’Donnell K., Cigelnik E., Nirenberg H.I., 1998. Molecular systematics and phylogeography of the Gibberella fujikuroi species complex. Mycologia 90(3): 465–493. https://doi.org/10.1080/00275514.1998.12026933
  39. O’Donnell K., Sutton D.A., Rinaldi M.G., Magnon K.C., Cox P.A., … Robinson J.S., 2004. Genetic diversity of human pathogenic members of the Fusarium oxysporum complex inferred from multilocus DNA sequence data and amplified fragment length polymorphism analyses: Evidence for the recent dispersion of a geographically widespread clonal lineage and nosocomial origin. Journal of Clinical Microbiology 42(11): 5109–5120. https://doi.org/10.1128/jcm.42.11.5109-5120.2004
  40. Pennycook S.R., 1989. Plant Diseases Recorded in New Zealand. Plant Disease Division, D.S.I.R., Auckland.
  41. Posada D., Crandall K.A., 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14(9): 817–818. https://doi.org/10.1093/bioinformatics/14.9.817
  42. Richardson M.J., 1990. An Annotated List of Seed-borne Diseases, 4th Edition. The International Seed Testing Association, Bassersdorf, Switzerland, 338 pp.
  43. Ronquist F., Teslenko M., van der Mark P., Ayres D.L., Darling A., … Huelsenbeck J.P., 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61(3): 539–542. https://doi.org/10.1093/sysbio/sys029
  44. Sandoval-Denis M., Lombard L., Crous P.W., 2019. Back to the roots: a reappraisal of Neocosmospora. Persoonia 43: 90–185. https://doi.org/10.3767/persoonia.2019.43.04
  45. Schreuder W., Lamprecht S.C., Marasas W.F.O., Calitz F.J., 1995. Pathogenicity of three Fusarium species associated with asparagus decline in South Africa. Plant Disease 79: 177–181. https://doi.org/10.1094/PD-79-0177.
  46. Schroers H.J., Baayen R.P., Meffert J.P., de Gruyter J., Hooftman M., O’Donnell K., 2004. Fusarium foetens, a new species pathogenic to Begonia elatior hybrids (Begonia x hiemalis) and the sister taxon of the Fusarium oxysporum species complex. Mycologia 96(2): 393–406. https://doi.org/10.1080/15572536.2005.11832984
  47. Schroers H-J., Samuels G.J., Zhang N., Short D.P.G., Juba J., Geiser D.M., 2016. Epitypification of Fusisporium (Fusarium) solani and its assignment to a common phylogenetic species in the Fusarium solani species complex. Mycologia 108(4): 806–819 https://doi.org/10.3852/15-255
  48. Seifert K.A., Aoki T., Baayen R.P., Brayford D., Burgess L.W., … Waalwijk C., 2003. The name Fusarium moniliforme should no longer be used. Mycological Research 107(6): 643–644. https://doi.org/10.1017/S095375620323820X
  49. Snyder W.C., Hansen H.N., 1940. The species concept in Fusarium. American Journal of Botany 27(2): 64–67.
  50. Snyder W.C., Hansen H.N., 1941. The species concept in Fusarium with reference to section Martiella. American Journal of Botany 28(9): 738–742. https://doi.org/10.2307/2436658
  51. Stamatakis A., 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22(21): 2688–2690. https://doi.org/10.1093/bioinformatics/btl446
  52. Tai F.L., 1979. Sylloge Fungorum Sinicorum. Science Press, Academia Sinica, Peking.
  53. Tamura K., Stecher G., Peterson D., Filipski A., Kumar S., 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution 30(12): 2725–2729. https://doi.org/10.1093/molbev/mst197
  54. Tan Y.P., Conroy J.R., 2024. Nomenclatural novelties. Index of Australian Fungi 45: 1–8. https://doi.org/10.5281/zenodo.13858562Tang T., Wang F., Guo J., Guo X., Duan Y., You J., 2021. Fusarium acuminatum associated with root rot of Maidong (Ophiopogon japonicus) in China. Plant Disease 105(6): 1860. https://doi.org/10.1094/PDIS-11-20-2344-PDN
  55. Tan Y.P., Shivas R.G., 2024. Nomenclatural novelties. Index of Australian Fungi 31: 1–1. https://doi.org/10.5281/zenodo.10784072
  56. Tang T., Wang F., Guo J., Guo X., Duan Y., You J., 2021. Fusarium acuminatum associated with root rot of maidong (Ophiopogon japonicus) in China. Plant Disease 105: 6. https://doi.org/10.1094/PDIS-11-20-2344-PDN
  57. Ulaszewski B., Sandoval‑Denis M., Groenewald J.Z., Costa M.M., Mishra B., … Thines M., 2025. Genomic features and evolution of lifestyles support the recognition of distinct genera among fusarioid fungi. Mycological Progress 24(1): 20. https://doi.org/10.1007/s11557-024-02025-4
  58. Vaidya G., Lohman D.J., Meier R., 2011. SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics 27(2): 171–180. https://doi.org/10.1111/j.1096-0031.2010.00329.x
  59. Van Bakel J.M.M., Krom-Kerstens J.J.A., 1974. Deal stem disease of asparagus caused by Fusarium culmorum. Netherlands Journal of Plant Pathology 80: 104–109. https://doi.org/10.1007/BF01980615
  60. Vujanovic V., Hamel C., Yergeau E., St-Arnaud M., 2006. Biodiversity and biogeography of Fusarium species from northeastern North American asparagus fields based on microbiological and molecular approaches. Microbial Ecology 51(2): 242–255. https://doi.org/10.1007/s00248-005-0046-x
  61. Wang M.M., Crous P.W., Sandoval-Denis M., Han S.L., Liu F., … Cai L., 2022. Fusarium and allied genera from China: species diversity and distribution. Persoonia 48: 1–53. https://doi.org/10.3767/persoonia.2022.48.01
  62. Wong J., Jeffries P., 2006. Diversity of pathogenic Fusarium populations associated with asparagus roots in decline soils in Spain and the UK. Plant Pathology 55(3): 331–342. https://doi.org/10.1111/j.1365-3059.2006.01360.x
  63. World Integrated Trade Solution, 2025. Netherlands asparagus, fresh or chilled exports by country in 2023. Retrieved November 19, 2025, from https://wits.worldbank.org/trade/comtrade/en/country/NLD/year/2023/tradeflow/Exports/partner/ALL/product/070920
  64. Yilmaz N., Sandoval-Denis M., Lombard L., Visagie C.M., Wingfield B.D., Crous P.W., 2021. Redefining species limits in the Fusarium fujikuroi species complex. Persoonia 46: 129–162. https://doi.org/10.3767/persoonia.2021.46.05.
  65. Zhuang W.Y., 2005. Fungi of Northwestern China. Mycotaxon, Ltd., Ithaca, NY.