Puccinia horiana (white rust of chrysanthemum)
- Taxonomic Tree
- Distribution Table
- Risk of Introduction
- Hosts/Species Affected
- Host Plants and Other Plants Affected
- Growth Stages
- List of Symptoms/Signs
- Biology and Ecology
- Plant Trade
- Detection and Inspection
- Prevention and Control
- Distribution Maps
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Puccinia horiana Henn.
Preferred Common Name
- white rust of chrysanthemum
International Common Names
- Spanish: roya blanca del crisantemo; roya japonesa del crisantemo
- French: rouille blanche du chrysanthème; rouille japonaise du chrysanthème
Local Common Names
- Germany: Japanischer Chrysantheme Rost; Mehliger: Chrysantheme Rost; weisser Chrysanthemenrost
- PUCCHN (Puccinia horiana)
Taxonomic TreeTop of page
- Domain: Eukaryota
- Kingdom: Fungi
- Phylum: Basidiomycota
- Subphylum: Pucciniomycotina
- Class: Pucciniomycetes
- Order: Pucciniales
- Family: Pucciniaceae
- Genus: Puccinia
- Species: Puccinia horiana
DescriptionTop of page Telia hypophyllous, rarely epiphyllous, compact, pinkish-buff to white, 2-4 mm diameter. Teliospores pedicellate, up to 45 µm long, pale-yellow, oblong to oblong-clavate, slightly constricted, 30-45 x 13-17 µm, with thin walls, 1-2 µm thick at sides, commonly thicker (4-9) µm at apex. Teliospores germinating in situ. Basidiospores hyaline, slightly curved, broadly ellipsoid to fusiform, 7-14 x 5-9 µm.
For more details see Hennings (1901), Baker (1967) and Punithalingam (1968).
DistributionTop of page
P. horiana originated in Japan and has spread to other Far Eastern countries, to South Africa, and from there to Europe. Walker (1983) critically reviewed the distribution data. Outbreaks of white rust have also been observed in Ontario, Canada (JSW Dickens, Central Science Laboratory, UK, personal communication, 1994).
P. horiana is mostly a greenhouse pest in more temperate areas. It is considered a quarantine pest in many countries and is subject to rigorous eradication programmes when detected. Distributions can therefore vary from year to year and the National Plant Protection Organization should be consulted for the most up-to-date distribution information for a specific region.
See also CABI/EPPO (1998, No. 236).
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|Brunei Darussalam||Present||CABI/EPPO, 2008; EPPO, 2014|
|China||Present||CABI/EPPO, 2008; EPPO, 2014|
|-Fujian||Present||CABI/EPPO, 2008; EPPO, 2014|
|-Guangdong||Present||CABI/EPPO, 2008; EPPO, 2014|
|-Hong Kong||Present, few occurrences||CABI/EPPO, 2008; EPPO, 2014|
|-Jiangsu||Present||CABI/EPPO, 2008; EPPO, 2014|
|India||Restricted distribution||2013||Dheepa et al., 2015; Sriram et al., 2015|
|-Karnataka||Present||2013||Sriram et al., 2015|
|-Tamil Nadu||Present||2013||Dheepa et al., 2015|
|Israel||Eradicated||CABI/EPPO, 2008; EPPO, 2014|
|Japan||Present||CABI/EPPO, 2008; EPPO, 2014|
|-Hokkaido||Present||CABI/EPPO, 2008; EPPO, 2014|
|-Honshu||Present||CABI/EPPO, 2008; EPPO, 2014|
|Kazakhstan||Absent, no pest record||EPPO, 2014|
|Korea, DPR||Present||CABI/EPPO, 2008; EPPO, 2014|
|Korea, Republic of||Present||CABI/EPPO, 2008; EPPO, 2014|
|Malaysia||Widespread||CABI/EPPO, 2008; EPPO, 2014|
|-Peninsular Malaysia||Present||CABI/EPPO, 2008; EPPO, 2014|
|-Sabah||Present||CABI/EPPO, 2008; EPPO, 2014|
|Taiwan||Present, few occurrences||CABI/EPPO, 2008; EPPO, 2014|
|Thailand||Present||CABI/EPPO, 2008; EPPO, 2014|
|Turkey||Restricted distribution||Göre, 2008; EPPO, 2014|
|Uzbekistan||Absent, no pest record||EPPO, 2014|
|Morocco||Absent, intercepted only||CABI/EPPO, 2008; EPPO, 2014|
|South Africa||Restricted distribution||CABI/EPPO, 2008; EPPO, 2014|
|-Canary Islands||Eradicated||CABI/EPPO, 2008; EPPO, 2014|
|Tunisia||Restricted distribution||CABI/EPPO, 2008; EPPO, 2014|
|Canada||Eradicated||CABI/EPPO, 2008; CFIA, 2008; EPPO, 2014|
|-British Columbia||Eradicated||CABI/EPPO, 2008; CFIA, 2008; EPPO, 2014|
|-Ontario||Eradicated||CABI/EPPO, 2008; EPPO, 2014|
|Mexico||Present, few occurrences||CABI/EPPO, 2008; EPPO, 2014|
|USA||Transient: actionable, under eradication||CABI/EPPO, 2008; NAPPO, 2008; EPPO, 2014|
|-California||Eradicated||CABI/EPPO, 2008; EPPO, 2014|
|-Connecticut||Eradicated||CABI/EPPO, 2008; NAPPO, 2008; EPPO, 2014|
|-Massachusetts||Present, few occurrences||Massachusetts Department of Agricultural Resources, 2008|
|-Michigan||Present, few occurrences||NAPPO, 2008|
|-New Jersey||Eradicated||CABI/EPPO, 2008; EPPO, 2014|
|-New York||Eradicated||CABI/EPPO, 2008; EPPO, 2014|
|-Oregon||Eradicated||CABI/EPPO, 2008; EPPO, 2014|
|-Pennsylvania||Transient: actionable, under eradication||CABI/EPPO, 2008; EPPO, 2014|
|-Virginia||Present, few occurrences||Virginia Department of Agriculture and Consumer Services, 2009|
|-Washington||Eradicated||CABI/EPPO, 2008; EPPO, 2014|
|Argentina||Present||CABI/EPPO, 2008; EPPO, 2014|
|Brazil||Present||CABI/EPPO, 2008; EPPO, 2014|
|-Sao Paulo||Present||CABI/EPPO, 2008; EPPO, 2014|
|Chile||Restricted distribution||CABI/EPPO, 2008; EPPO, 2014|
|Colombia||Present||CABI/EPPO, 2008; EPPO, 2014|
|Peru||Present||CABI/EPPO, 2008; EPPO, 2014|
|Uruguay||Present, few occurrences||CABI/EPPO, 2008; EPPO, 2014|
|Venezuela||Present||CABI/EPPO, 2008; EPPO, 2014|
|Austria||Restricted distribution||1964||CABI/EPPO, 2008; EPPO, 2014|
|Belgium||Widespread||1964||CABI/EPPO, 2008; EPPO, 2014|
|Bulgaria||Restricted distribution||CABI/EPPO, 2008; EPPO, 2014|
|Croatia||Widespread||CABI/EPPO, 2008; EPPO, 2014|
|Cyprus||Eradicated||CABI/EPPO, 2008; EPPO, 2014|
|Czech Republic||Restricted distribution||CABI/EPPO, 2008; EPPO, 2014|
|Denmark||Present, few occurrences||Jorgensen, 1964; CABI/EPPO, 2008; EPPO, 2014|
|Finland||Eradicated||1997||CABI/EPPO, 2008; EPPO, 2014|
|France||Widespread||Grouet and Allaire, 1973; CABI/EPPO, 2008; EPPO, 2014|
|-France (mainland)||Widespread||CABI/EPPO, 2008|
|Germany||Widespread||1968||CABI/EPPO, 2008; EPPO, 2014|
|Greece||Restricted distribution||CABI/EPPO, 2008; EPPO, 2014|
|-Crete||Present||CABI/EPPO, 2008; EPPO, 2014|
|Hungary||Present, few occurrences||CABI/EPPO, 2008; EPPO, 2014|
|Ireland||Eradicated||1976||CABI/EPPO, 2008; EPPO, 2014|
|Italy||Restricted distribution||1964||Malta & Gullino, 1974; CABI/EPPO, 2008; EPPO, 2014|
|-Italy (mainland)||Restricted distribution||CABI/EPPO, 2008|
|-Sicily||Present||CABI/EPPO, 2008; EPPO, 2014|
|Latvia||Restricted distribution||CABI/EPPO, 2008; EPPO, 2014|
|Lithuania||Absent, confirmed by survey||CABI/EPPO, 2008; EPPO, 2014; IPPC, 2016|
|Luxembourg||Absent, formerly present||CABI/EPPO, 2008; EPPO, 2014|
|Netherlands||Restricted distribution||1964||NPPO of the Netherlands, 2013; Boerema and Vermeulen, 1964; CABI/EPPO, 2008; EPPO, 2014|
|Norway||Eradicated||CABI/EPPO, 2008; EPPO, 2014|
|Poland||Restricted distribution||Zamorski, 1982; CABI/EPPO, 2008; EPPO, 2014|
|Portugal||Present, few occurrences||EPPO, 2014|
|Romania||Restricted distribution||CABI/EPPO, 2008; EPPO, 2014|
|Russian Federation||Present||CABI/EPPO, 2008; EPPO, 2014|
|-Russian Far East||Present||CABI/EPPO, 2008; EPPO, 2014|
|Serbia||Restricted distribution||CABI/EPPO, 2008; EPPO, 2014|
|Slovakia||Present||CABI/EPPO, 2008; EPPO, 2014|
|Slovenia||Restricted distribution||CABI/EPPO, 2008; EPPO, 2014|
|Spain||Eradicated||CABI/EPPO, 2008; EPPO, 2014|
|Sweden||Present, few occurrences||1960||Akesson, 1983; CABI/EPPO, 2008; EPPO, 2014|
|Switzerland||Restricted distribution||1964||CABI/EPPO, 2008; EPPO, 2014|
|UK||Restricted distribution||1963||CABI/EPPO, 2008; EPPO, 2014|
|-England and Wales||Restricted distribution||CABI/EPPO, 2008; EPPO, 2014|
|-Northern Ireland||Restricted distribution||CABI/EPPO, 2008; EPPO, 2014|
|-Scotland||Restricted distribution||CABI/EPPO, 2008; EPPO, 2014|
|Ukraine||Transient: actionable, under eradication||CABI/EPPO, 2008; EPPO, 2014|
|Yugoslavia (Serbia and Montenegro)||Restricted distribution||1964||Dordevic, 1983|
|Australia||Restricted distribution||CABI/EPPO, 2008; EPPO, 2014|
|-Australian Northern Territory||Present||EPPO, 2014|
|-New South Wales||Present||CABI/EPPO, 2008; EPPO, 2014|
|-Queensland||Present||CABI/EPPO, 2008; EPPO, 2014|
|-South Australia||Present||CABI/EPPO, 2008; EPPO, 2014|
|-Tasmania||Present||CABI/EPPO, 2008; EPPO, 2014|
|-Victoria||Present||Catley, 1987; CABI/EPPO, 2008; EPPO, 2014|
|-Western Australia||Present||CABI/EPPO, 2008; EPPO, 2014|
|New Zealand||Restricted distribution||1965||CABI/EPPO, 2008; EPPO, 2014|
Risk of IntroductionTop of page Until 1963, P. horiana was confined to China and Japan, where it is presumably important, although little seems to be published concerning it (Yamada, 1956). However, it has since spread rapidly on infected imported cuttings and is now a feared and serious disease in nurseries in Europe, frequently causing complete loss of glasshouse chrysanthemum crops. Severe outbreaks occurred in England and Denmark, and these were at first successfully eradicated. The disease was similarly contained in France following an initial outbreak in 1967, but appeared again in 1971, and has since spread rapidly throughout the country causing extensive losses. At the present time, white rust is established in most western European countries, and statutory measures have been abandoned in these.
P. horiana is an EPPO A2 quarantine pest (OEPP/EPPO, 1982) and is also of quarantine significance for IAPSC, JUNAC and NAPPO. Once established, chrysanthemum white rust is extremely difficult and costly to eradicate. The intensification of chrysanthemum production, with high plant densities in humid glasshouses, provides an ideal environment for the fungus. For many years, the UK and Ireland in particular have maintained phytosanitary measures against the disease, subjecting it to statutory control wherever found. The justification for this policy was argued in terms of cost-effectiveness by Lelliott (1984) and Pemberton (1988). Now that the UK has abandoned this policy, it is not clear whether other countries will find it necessary or opportune to maintain measures, especially if they import potted plants or cut flowers of chrysanthemums from infested countries in significant numbers. If importation is limited to planting material, exclusion might be a more realistic policy.
Hosts/Species AffectedTop of page Chrysanthemums are the only host, especially the florists' cultivars; these are widely cultivated in glasshouses.
Host Plants and Other Plants AffectedTop of page
|Chrysanthemum morifolium (chrysanthemum (florists'))||Asteraceae||Main|
Growth StagesTop of page Flowering stage, Post-harvest
SymptomsTop of page On Leaves
Following infection, pale-green to yellow spots, up to 5 mm diameter, develop on the upper surface. The centres of these spots become brown and necrotic with ageing. On the corresponding lower surface, raised, buff or pinkish, waxy pustules (telia) are found. As the spots on the upper surface become sunken, so these pustules become quite prominent and turn whitish when basidiospores are produced. Telia are occasionally found on the upper leaf surface. Severely attacked leaves wilt, hang down the stem and gradually dry up completely.
On Bracts and Stems
Sori sometimes develop when crops are excessively affected.
Infection has been recorded as necrotic flecking with occasional pustules (Dickens, 1970).
List of Symptoms/SignsTop of page
|Inflorescence / lesions; flecking; streaks (not Poaceae)|
|Leaves / fungal growth|
|Leaves / necrotic areas|
|Leaves / wilting|
|Stems / mould growth on lesion|
Biology and EcologyTop of page P. horiana is an autoecious rust. The bicellular teliospores germinate in situ to produce unicellular basidiospores which are dispersed in air currents. No other spores are known. High humidity, and a film of moisture, appear to be necessary for the germination of both teliospores and basidiospores. Teliospores are capable of germination as soon as they are mature; germination and discharge of basidiospores occur between 4 and 23°C and, at the optimum temperature of 17°C, discharge of basidiospores starts within 3 h. Basidiospores can germinate over a wide temperature range and, at 17-24°C, either surface of the leaf may be penetrated within 2 h. Thus, only 5 h of wetness is sufficient for a new infection to become established. Within the leaf, abundant, hyaline, intercellular hyphae are produced with intracellular haustoria. The incubation period is normally 7-10 days, but short periods of high temperatures (over 30°C) can apparently prolong the period to 8 weeks.
The disease is normally carried on infected cuttings and plants (including cut flowers) of glasshouse chrysanthemums.
There are reports that dispersal by wind can occur over distances of 700 m and more but, because the basidiospores are very sensitive to desiccation at less than 90% RH, long-distance spread would only be likely during very wet periods. Natural spread is hence unlikely over long distances; it is limited even between glasshouses (or else it would never have been possible to contain the disease at all).
The ability of the fungus to overwinter outdoors is unknown. In experiments, teliospores in sori on detached leaves survived for 8 weeks at 50% RH but, at higher humidities or when buried in dry or moist compost, they only survived for 3 weeks or less. It would, therefore, appear that infected debris is not likely to be important in the carry-over of the disease.
Some chrysanthemum cultivars appear to be more susceptible than others and there is evidence that there is more than one pathotype of the fungus. For more information, see Water (1981).
Plant TradeTop of page
|Plant parts liable to carry the pest in trade/transport||Pest stages||Borne internally||Borne externally||Visibility of pest or symptoms|
|Flowers/Inflorescences/Cones/Calyx||hyphae; spores||Yes||Yes||Pest or symptoms usually visible to the naked eye|
|Leaves||hyphae; spores||Yes||Yes||Pest or symptoms usually visible to the naked eye|
|Stems (above ground)/Shoots/Trunks/Branches||hyphae; spores||Yes||Yes||Pest or symptoms usually visible to the naked eye|
|Plant parts not known to carry the pest in trade/transport|
|Fruits (inc. pods)|
|Growing medium accompanying plants|
|True seeds (inc. grain)|
ImpactTop of page P. horiana is now a feared and serious disease in nurseries, frequently causing complete loss of glasshouse chrysanthemum crops.
DiagnosisTop of page
Alaei et al. (2009) successfully detected Puccinia horiana using a conventional, nested and real-time polymerase chain reaction (PCR) protocol.
Detection and InspectionTop of page The fungus can be positively identified on the basis of symptoms and morphological features. Numerous other rust fungi have been reported on chrysanthemums, but they can be distinguished by their teliospore shape, size, surface ornamentation and colour (Punithalingam, 1968). For more information see Stahl (1964), Baker (1967) and Firman and Martin (1968).
Prevention and ControlTop of page Chemical Control
Preventive spraying with fungicides is effective but costly (Water, 1981). Active ingredients found useful include oxycarboxin, triforine, benodanil, triadimefon, diclobutrazol, dibitertanol and propiconazole. Rattink et al. (1985) experimented with systemic fungicides in the nutrient recirculating system of chrysanthemums grown on rockwool. Dickens (1990), using a similar set of fungicides, found that only propiconazole had sufficient eradicative activity to be useful in a statutory campaign. However, in subsequent work Dickens (1991) found that myclobutanil and hexaconazole also had good eradicative activity. For more details on fungicidal control also see Zamorski (1982), Dickens and Potter (1983) and Krebs (1985).
Srivastava et al. (1985) suggest that Verticillium lecanii, used for biological control of aphids on glasshouse chrysanthemums, will also control P. horiana.
Some chrysanthemum cultivars are resistant and breeding for resistance continues (Rademaker and de Jong, 1985, 1987). Grouet (1984) has reviewed white rust control in general.
EPPO recommends (OEPP/EPPO, 1990) that planting material of chrysanthemums should come from a place of production regularly inspected and found free of disease for 3 months beforehand. The fungus should also be absent from the immediate vicinity of the place of production. For cut flowers, visual inspection is sufficient. Veenenbos (1984) outlined the pre-export inspection and control system used to provide this guarantee in the Netherlands. Such systems are now viewed in that country as less and less acceptable from an environmental standpoint, because they depend heavily on intensive use of plant protection products and also interfere with biological control systems in glasshouses. For the few countries where the disease is still absent, these arguments tend to support continued exclusion.
ReferencesTop of page
Alaei H; Baeyen S; Maes M; Höfte M; Heungens K, 2009. Molecular detection of Puccinia horiana in Chrysanthemum × morifolium through conventional and real-time PCR. Journal of Microbiological Methods, 76(2):136-145. http://www.sciencedirect.com/science?_ob=ArticleURL&_udi=B6T30-4TNWGRN-1&_user=6686535&_coverDate=02%2F28%2F2009&_rdoc=5&_fmt=high&_orig=browse&_srch=doc-info(%23toc%234932%232009%23999239997%23857268%23FLA%23display%23Volume)&_cdi=4932&_sort=d&_docanchor=&_ct=17&_acct=C000066028&_version=1&_urlVersion=0&_userid=6686535&md5=15d16f4a8f84ccf8a7d85d8c5f67b5e8
Baker JJ, 1967. Chrysanthemum white rust in England and Wales 1963-66. Plant Pathology, 16:162-166.
Boerema GH; Vermeulen H, 1964. Puccinia horiana, the Japanese rust, also in Dutch chrysanthemum houses. Vakblad voor de Bloemisterij, 19:697.
Dickens J; Potter R, 1983. Chrysanthemums: spraying for white rust. Grower, 100:18, 35, 37.
Dickens JSW, 1970. Infection of chrysanthemum flowers by white rust (Puccinia horiana). Plant Pathology, 19:122-124.
Dickens JSW, 1991. Evaluation of some newer fungicides, in comparison with propiconazole, against chrysanthemum white rust (Puccinia horiana). Tests of Agrochemicals and Cultivars 12. Annals of Applied Biology, 118(supplement):32-33.
EPPO, 1990. Specific quarantine requirements. EPPO Technical Documents, No. 1008. Paris, France: European and Mediterranean Plant Protection Organization.
EPPO, 2014. PQR database. Paris, France: European and Mediterranean Plant Protection Organization. http://www.eppo.int/DATABASES/pqr/pqr.htm
Firman ID; Martin PH, 1968. White rust of chrysanthemums. Annals of Applied Biology, 62:429-442.
Grouet D, 1984. Mise au point sur les possibilités actuelles de lutte contre la rouille blanche du chrysanthFme. Revue Horticole, 251:33-36.
Hennings P, 1901. Some new Japanese rusts. Hedwigia, 40:25-26.
IPPC, 2016. Information on Pest Status in the Republic of Lithuania in 2015. IPPC Official Pest Report, No. LTU-01/2. Rome, Italy: FAO. https://www.ippc.int/
Jorgensen HA, 1964. Japanese chrysanthemum rust, a dangerous disease discovered in Denmark. Gartner Tidende, 80:234-235.
Massachusetts Department of Agricultural Resources, 2008. Pathogen Alert: Chrysanthemum White Rust detected in Massachusetts. Massachusetts, USA: Massachusetts Department of Agricultural Resources/UMass Extension Agriculture and Landscape Program. http://www.massnrc.org/PESTS/linkeddocuments/pestalerts/CWR_Sep2008.html
Pemberton AW, 1988. Quarantine: the use of cost/benefit analysis in the development of MAFF plant health policy. In: Clifford BC, Lester E, eds. Control of Plant Diseases: Costs and Benefits. Oxford, UK: Blackwell Scientific Publications, 195-212.
Rademaker W; Jong J de, 1987. Types of resistance to Puccinia horiana in chrysanthemum. Acta Horticulturae, 197:85-88.
Rattink H; Zamorski C; Dil MC, 1985. Spread and control of white rust (Puccinia horiana) on chrysanthemums on artificial substrate. Mededelingen van de Faculteit Landbouwwetenschappen Rijksuniversiteit Gent, 50(3b):1243-1249
Sriram S; Chandran NK; Rajiv Kumar; Reddy MK, 2015. First report of Puccinia horiana causing white rust of chrysanthemum in India. New Disease Reports, 32:8. http://www.ndrs.org.uk/article.php?id=032008
Stahl M, 1964. Puccinia horiana, white rust of chrysanthemum, a new rust fungus in Germany. Nachrichtenblatt des Pflanzenschutzdienstes, 16:180-182.
Veenenbos JAJ, 1984. The "green corner"; a pre-export inspection system for chrysanthemum cut flowers and pot plants in the Netherlands. Bulletin OEPP/EPPO Bulletin, 14:269-371.
Virginia Department of Agriculture and Consumer Services, 2009. Pest Alert: Chrysanthemum White Rust. Virginia, USA: Virginia Cooperative Extension and Virginia Department of Agriculture and Consumer Services. http://www.sepdn.org/DesktopModules/ViewDocument.aspx?DocumentID=3210
Yamada S, 1956. Experiments on the epidemiology and control of chrysanthemum white rust, caused by Puccinia horiana. Annals of the Phytopathological Society of Japan, 20:148-154.
Distribution MapsTop of page
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