Preferred name: Fusarium foetens
Authority: Schroers & al.
Taxonomic position: Fungi: Ascomycota: Pezizomycotina: Sordariomycetes: Hypocreomycetidae: Hypocreales: Nectriaceae
Common names in English: fusarium wilt of Hiemalis begonia
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Notes on taxonomy and nomenclature EPPO Categorization: A2 list
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EPPO Code: FUSAFO

Fusarium wilt is most severe on the Hiemalis begonias (Begonia × hiemalis or begonia elatior hybrids) (Brand & Weinberg, 2005; Elmer, 2008; Hamelink &van Noort, 2009). Other begonia species have shown less susceptibility or complete immunity in artificial inoculation tests. Symptoms on Lorraine begonia (Begonia ×cheimantha ‘Kardinal’) and Tuberous begonia (Begonia × tuberhybrida ‘Champagner’ were delayed when inoculated, but the plants eventually died (Brand & Wienberg, 2005). Of nine Rex begonia (B. rex) cultivars tested, two varieties (‘Hurricane Bay’ and ‘White Caps’) had significant stunting compared to uninoculated controls, but no wilt appeared (Elmer, 2008). No wilt symptoms or stunting was detected on angelwing begonias (B. coccinea Hook), or wax begonias (Begonia × semperflorens-cultorum) when tested.

Lamprecht & Tewoldemedhin (2017) isolated F. foetens from wilting rooibos (Aspalathus linearis) seedlings, grown for tea production in South Africa. Identification was confirmed via matched sequences of EF-alpha gene, and pathogenicity tests show that the rooibos plant is another host for F. foetens.

Liu et al. (2023) isolated F. foetens from wilting potatoes and completed Koch postulates showing potato to be another host.

A few other asymptomatic hosts have been identified including maize, on which it affects the kernels, (González-Jartín et al., 2018) and coastal heath plants that were not identified (Summerell et al., 2011).

During artificial inoculation tests, the following plants were shown to be symptomatic experimental hosts:

• - Begonia × cheimantha ‘Kardinal’, and Begonia × tuberhybrida ‘Champagner’ (Brand & Wienberg, 2005)
  - Begonia rex cultivars ‘Hurricane Bay’ and ‘White Caps’ (Elmer, 2008).
  - Bell pepper (Capsicum annuum var. grossum) (Amobonye et al., 2021).
  - Cyclamen (Cyclamen persicum, Schroers et al 2004).
  - Cayenne pepper (Capsicum annuum var. longum, Amobonye et al., 2021).
  - Lupin Lupinus angustifolius (Lamprecht & Tewoldemedhin, 2017).
  - Tomato (Solanum lycopersicum) (Amobonye et al., 2021).

Host list: Aspalathus linearis, Begonia x hiemalis, Solanum tuberosum

Fusarium foetens was first identified causing disease in Begonia × hiemalis in the Netherlands in 2001 (Schroers et al., 2004). The fungus quickly spread and was found in Germany in 2002 (Neubauer & Nirenberg, 2002) and the USA in 2003 (Elmer et al., 2004), then to Japan in 2006 (Sekine et al., 2008), and to Belgium and Canada in 2010 (Tian et al., 2010). The pathogen was intercepted in England (Jones & Baker 2007) and has been eradicated in France in 2007 (Saurat et al., 2013).

The fungus was isolated from diseased rooibos (Aspalathus linearis) in South African nurseries (Lamprecht & Tewoldemedhin, 2017) and from garden soils near Durban, South Africa (Amobonye et al., 2021). In 2023 F. foetens was isolated from wilting potato (Solanum tuberosum) plants in Laiyang city, China (Liu et al., 2023). Summerell et al. (2011) reported on two isolates of F. foetens isolated from coastal heath vegetation from the Cape Arid National Park in Western Australia, Australia. F. foetens could be isolated from 75% of raw processed beef, chicken, and fish meat samples obtained in markets in Iraq (Abedzaid et al., 2014). One unconfirmed Indian publication reported a F. foetens-like culture from a saltworks in Villupuram Tamil Nadu State, India (Panchal et al., 2022). In Panchal et al. (2022) report, the isolates were identified using morphology only and no molecular confirmation was provided.

EPPO Region: Czech Republic, Germany, Netherlands, Norway
Africa: South Africa
Asia: China (Shandong), Japan (Honshu)
North America: Canada (Ontario), United States of America (Connecticut)
Oceania: New Zealand

Since no teleomorph is known for F. foetens, it is concluded that the fungus spreads asexually. On Begonia × hiemalis, the infective propagules are microconidia, macroconidia, and chlamydospores. The infecting structure in all propagules is the mycelium which invades roots and colonizes the basal stems and vascular tissue. The fungus eventually sporulates profusely on dying blackened stems. Heavily colonized stems attract fungus gnats which can aid in spread of the fungus to healthy plants. The pathogen can also move in irrigation water and studies found that less than 100 conidia/mL was sufficient to lead to disease on Begonia × hiemalis (Wohanka, 2003; Elmer, 2008).

On Potato dextrose agar (PDA), the distinct odour of the colonies is pungent and irritating, but less distinct on synthetic nutrient-poor agar (SNA) (Schroers et al., 2004; Tschöpe et al., 2007). The name, ‘foetens‘, meaning fetid, stinking, or smelly in Latin refers to this. F. foetens is easily distinguished from another Fusarium stem rot disease reported in the 1990s that also attacked Hiemalis begonias. That disease, caused by Fusarium begoniae (Nirenberg & O’Donnell, 1998), caused a dry rot canker on stems of begonias, and was not associated with root damage or vascular discoloration.

Some putative isolates of F. foetens have been reported to be toxigenic (Abedzaid & Abd Al-Reda, 2014), but their identification was based on matching ITS sequences and not by the more accepted and informative EF-alpha gene sequences. González-Jartín et al. (2019) isolated a strain of F. foetens from maize and reported that it produced the mycotoxins beauvericin and fusaric acid. O’Donnell et al., (2009) reported no detectable level of fumonisin and moniiformin in their strain (NRRL 31852). Isolates may vary in their toxigenicity.

Results from China and South Africa suggest chlamydospores might play an important role in survival and persistence in soil during temperature extremes (Amobonye et al., 2021; Li et al., 2023). The role of the mycotoxins produced by F. foetens in pathogenicity is unclear (González-Jartín et al., 2019). The fungus produces an array of volatile sesquiterpenes and cyclohexane derivatives which can be useful in identification (Tschöpe et al., 2007), but their role in its biology and/or pathogenicity is not clear. Elmer (2008) hypothesized these metabolites might attract fungus gnats and aid in the pathogens’ dissemination.

Symptoms

Symptoms on Begonia × hiemalis begonias appear as a very slight chlorosis in the dark green foliage followed by vein clearing and stunting. Root rot usually begins before the onset of foliar symptoms. As the disease progresses, basal stems begin to discolor. Wilting and vascular discoloration is also common. Dying stems are frequently covered with orange sporodochia that reveal microconidia and macroconidia when examined microscopically. In severe cases, the disease can cause mortality in less than two weeks. On rooibos, F. foetens causes symptoms such as damping off and root rot. On potato, F. foetens caused typical symptoms of wilt.

Morphology

Colonies grown on PDA develop white aerial mycelium while undersides of the agar dish can be variable depending on the quality of light during incubation. At 21 °C, colonies expand about 4.8 mm/day. When sub-cultured for 10-14 days on SNA amended with 1 x 3 cm filter papers (Nirenberg, 1976), short or long conidiophores bearing microconidia in monophialides or less frequently polyphialides are produced. Microconidia are one cell (rarely 2 to 3 celled) ovoidal to ellipsoidal (averaging 6.5 µm × 2.8 µm). Pale to light orange sporodochia are abundant on SNA and bear macroconidia in monophialides. Macroconidia are mostly 3 septate, slightly curved with the two central cells almost straight and average 34 µm × 4.4 µm. Chlamydospores are rare or abundant, globose, smooth or warted, and borne on terminal conidiophores, but can be intercalary in the mycelium. Chlamydospores are 7–13 µm × 7–11 µm (Schroers et al., 2004).

Detection and inspection methods

On Hiemalis begonia, the pathogen may not cause visible symptoms on young seedlings or cuttings whereas on rooibos seedlings a damping off/root rot was apparent. Molecular tools are available for detection in asymptomatic tissue (de Weerdt et al., 2006). Once symptoms are noted, affected tissue should be surface-disinfested with 70% ethanol or 10 % household bleach, thoroughly rinsed with water, and placed on selective agar such as Peptone PCNB (Laurence et al., 2012) or Komada’s selective medium (Komada, 1975). Sub-cultures arising from single spores should be grown on SNA agar amended with pieces of sterile filter paper for 10-14 days under 12 hr. photoperiods at 20-23 °C and microscopically examined under 100x and 400 x (Schroers et al. 2004).

F. foetens closely resembles members of the F. oxysporum species complex (FOSC) except for two distinguishing characteristics. The presence of microconidia borne in polyphialides and monophialides on long and short conidiophores in the aerial mycelium. The strong pungent colony odour detectable on cultures grown on PDA can be useful for identification (Schroers et al., 2004; Tschöpe et al., 2007). Confirmation using genotyping should also be done by sequencing partial fragments of the Efα and β-tubulin gene and blasting the sequences in Fusarium ID database (Geiser et al., 2004) or GenBank. More specific molecular probes have been designed by Huvenne et al. (2011) for real-time PCR detection and confirmation.

For morphological and molecular identification see the EPPO Diagnostic protocol PM 7/111 (EPPO, 2013).

F. foetens was shown to spread short distances by irrigation water (Wohank, 2003). Ebb and flow systems commonly used in Begonia × hiemalis greenhouse operations provided rapid means to spread. Inoculum levels as low as 100 conidia mL⁻¹ could lead to disease, but filtration and sanitation products such as chlorine dioxide and H₂O₂ disinfectants are effective in killing the spores. (Wohanka et al. 2005; Elmer, 2008). In Connecticut, fungus gnats (Bradysia spp.) were implicated as vectors for short distances. Long distance spread is likely due to infested plant material. Within the EPPO region, F. foetens was presumed to be introduced to the Netherlands (Schroers et al., 2004) and from there spread to other countries presumably on infested Begonia × hiemalis cuttings. However, since F. foetens has since been found to cause root diseases on plants other than begonias that were not associated with begonia production (Lamprecht & Tewoldemedhin, 2017; Liu et al., 2023), the origin of the pathogen is not clear. The fungus was also isolated from soils (Amobonye et al., 2021; Panchal et al., 2022) and from asymptomatic plants (González-Jartín et al., 2018; Laurence et al., 2012) which could suggest a diverse biology and possibly diverse genetic origins.

Economic impact

F. foetens was first reported to cause severe damage to various Begonia × hiemalis cultivars and was highly destructive for growers. Economic data specific to Begonia × hiemalis losses were not available, but begonia sales, in general, reached over 27 million USD in 2019 in the USA (Anon 2019). Since other Begonia species are significantly less or not susceptible, no economic impact has been reported on these. In South Africa, F. foetens lead to damping off/root rot in nurseries producing rooibos seedlings and over 50% losses were reported in affected nurseries. Economic data are not available. In Laiyang city, China, F. foetens was one of several Fusarium species capable of causing Fusarium wilt on potato. Although the losses specific to F. foetens versus the other species of Fusarium is difficult to determine, potato losses due to Fusarium wilt and result in 30 to 78 % losses in certain areas in China (Xia et al., 2022).

Control

Management techniques for F. foetens depend on the host. Strategies should always be multifaceted and integrate cultural controls, biological controls, and genetic resistance when possible. Chemical products such as fungicides have not been explored in begonia production but were examined on potato.

Begonia growers should ensure all incoming propagation material is disease free. If material is suspected to be infected, it should be segregated to make sure it remains asymptomatic. If available, molecular tests could be used to assess the possibility that material is infested. Use of clean potting soil, pots, and trays is very important. If trays or pots are reused, they should be disinfected. Since irrigation water can be a source of inoculum, Wohanka et al. (2005) found water filtration and the use of chlorine dioxide applied at 1.5–1.7 ug mL⁻¹ eliminated F. foetens from recycled water. Several hydrogen peroxide products were very effective in disinfesting F. foetens from irrigation sources (Elmer, 2008). Adding composts protected begonias in Germany (Van der Gaag et al., 2007) and rooibos in South Africa (Lamprecht & Tewoldemedhin, 2017). In potato fields in China, chemical fungicides, crop rotation, and use of tolerant cultivars is recommended, however, the authors cautioned that Fusarium wilt is difficult to manage (Liu et al., 2023).

In relation to biological control in Ontario Canada, Tian et al. (2012) examined five laboratory Bacillus subtilis strains along with biocontrol agents such as Streptomyces lydicus, Streptomyces griseoviridis, Trichoderma harzianum, Gliocladium catenulatum for efficacy in suppressing F. foetens on Hiemalis begonias. When applied as soil drenches before inoculation, all biocontrol agents significantly reduced the disease, increased biomass, and chlorophyll content when compared to untreated inoculated controls (Tian et al., 2013).

Genetic resistance is also an important aspect. Although most Hiemalis begonia cultivars are susceptible, tolerance has been reported in ‘Dragone’ and’ Kristy’ (Huvenne et al., 2011), and ‘Rainbow Spectrum Camilla’ (Tian et al., 2012). No reports of resistance to F. foetens in rooibos plants or potato cultivars have been made, but varieties of each plant that show tolerance to F. oxysporum would likely be resistant to F. foetens. This information needs to be validated.

Phytosanitary risk

F. foetens continues to pose a global threat to the Begonia x hiemalis industry and the risk to Begonia production is high. This pest has the potential to be spread via trade. Pathogenicity tests on begonia with isolates of F. foetens from Australia, China, European countries, India, the Middle East, South Africa, and the USA are needed to determine whether these isolates are pathogens or non-pathogenic isolates. Potential risks have been highlighted by more recent reports noting that F. foetens may be a common inhabitant of agricultural soils and natural landscapes in different countries (Lamprecht & Tewoldemedhin, 2017; Laurence et al., 2012; Li et al., 2023; Panchal et al., 2022). Until a more comprehensive multigene phylogenetic analysis is conducted with isolates of F. foetens along with cross pathogenicity tests with Hiemalis begonias, the risk of continued re-introduction remains high.

When F. foetens was discovered in the EPPO region, the Netherlands conducted a PRA (Van der Gaag & Van Raak, 2010) and regulated it for propagation material. It has been recommended for regulation as a quarantine pest by EPPO in 2007 and was deregulated in the Netherland in 2011 (Van der Gaag et al., 2017). F. foetens has since been prioritized by the Netherlands Food and Consumer Product Safety Authority as a pathogen which has a strong likelihood of establishment (Van der Gaag et al., 2017). Continued monitoring for symptoms is necessary. Phytosanitary Measures have been identified by EPPO (2007). These incudes that plants for planting of Begonia x hiemalis and Begonia x cheimantha come from a pest-free area or a pest-free place of production. An alternative option could be that plants for planting are produced in a pest-free production site. Careful inspection should be made for all propagative material being moved. Given the difficulty in observing visual symptoms in propagative material or small transplants, the use of molecular probes could be highly beneficial if this is economically feasible.

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This datasheet was prepared in 2023 by Wade Elmer, The Connecticut Agricultural Experiment Station (USA). His valuable contribution is gratefully acknowledged.

EPPO (2024) Fusarium foetens. EPPO datasheets on pests recommended for regulation. https://gd.eppo.int (accessed 2024-12-21)

This datasheet was first published online in 2023. It is maintained in an electronic format in the EPPO Global Database. The sections on 'Identity', ‘Hosts’, and 'Geographical distribution' are automatically updated from the database. For other sections, the date of last revision is indicated on the right.