Preferred name: Puccinia horiana
Authority: Hennings
Taxonomic position: Fungi: Basidiomycota: Pucciniomycotina: Pucciniomycetes: Pucciniales: Pucciniaceae
Common names in English: white rust of chrysanthemum
view more common names online...
Notes on taxonomy and nomenclature EPPO Categorization: A2 list
EU Categorization: RNQP (Annex IV)
view more categorizations online...
EPPO Code: PUCCHN

P. horiana is a pathogen of several chrysanthemum and daisy species. Its most important host plants include Chrysanthemum × morifolium (commonly known as florist's chrysanthemum), C. indicum, C. japonicum, C. nipponicum (nippon daisy), and Ajania pacifica (gold and silver chrysanthemum) (Water, 1981; Alaei et al., 2009; De Backer et al., 2011; EFSA, 2013). However, it is predominantly known as a pathogen of Chrysanthemum × morifolium, due to the economic importance of this hybrid in the cut flower and potted plant industry. The host range of the pest is currently limited to 12 chrysanthemum and daisy species belonging to 5 genera in the plant family Asteraceae (Chrysanthemum, Nipponanthemum, Arctanthemum, Leucanthemella, and Ajania).

Host list: Ajania pacifica, Ajania shiwogiku, Chrysanthemum indicum, Chrysanthemum japonense, Chrysanthemum lavandulifolium, Chrysanthemum makinoi, Chrysanthemum x morifolium, Chrysanthemum zawadskii, Leucanthemella serotina

The disease is indigenous to Japan, where it was first noted in 1895 (Hiratsuka, 1957). It remained confined to Japan until 1963, from where it spread to China and South Africa (De Backer et al., 2011). Since 1963, P. horiana has spread rapidly on infected shipments of cut flowers and has become established in the Russian Far East, Europe, Africa, Australia, Oceania, North and South America (De Backer et al., 2011).

EPPO Region: Austria, Belgium, Bulgaria, Croatia, Czech Republic, Denmark, France (mainland), Germany, Greece (Kriti), Guernsey, Hungary, Italy (mainland, Sicilia), Latvia, Netherlands, Poland, Portugal (mainland, Madeira), Romania, Russia (Far East), Serbia, Slovakia, Slovenia, Sweden, Switzerland, Tunisia, Türkiye, Ukraine, United Kingdom (England, Northern Ireland, Scotland)
Africa: South Africa, Tunisia
Asia: Brunei Darussalam, China (Fujian, Guangdong, Jiangsu, Xianggang (Hong Kong)), India (Tamil Nadu), Japan (Hokkaido, Honshu, Kyushu, Shikoku), Korea Dem. People's Republic, Korea, Republic, Malaysia (Sabah, West), Taiwan, Thailand, Vietnam
North America: Mexico, United States of America (Pennsylvania)
South America: Argentina, Brazil (Sao Paulo), Chile, Colombia, Peru, Uruguay, Venezuela
Oceania: Australia (New South Wales, Northern Territory, Queensland, South Australia, Tasmania, Victoria, Western Australia), New Zealand

P. horiana is an autoecious rust (Pucciniales) that causes chrysanthemum white rust. The bicellular teliospores are normally formed on the lower side of the host’s leaves. These teliospores germinate in situ to form a promycelium produced in the pustules (Wang et al., 2020). Promycelia bear a mean of two infective propagules, unicellular basidiospores that are released and carried to new hosts by wind over a distance of up to 700 m (De Backer et al., 2011; Wang et al., 2020). No other spores are known (Wang et al., 2020). High humidity and a film of moisture appear to be necessary for germination of both teliospores and basidiospores. Teliospores are capable of germination as soon as they are mature; germination and discharge of basidiospores occurs at temperature between 4 and 23°C and the optimal conditions for development of the pathogen are high relative humidity and cool temperatures (17–20°C) (Whipps, 1993; De Backer et al., 2011). Basidiospores can germinate over a wide range of temperature and at 17–24°C either surface of the leaf may be penetrated within 2 h. Thus, 5 h of wetness is sufficient for a new infection to become established (Firman and Martin, 1968). Abundant, hyaline, intercellular hyphae are produced with intracellular haustoria. Under high humidity and mild temperature, symptoms appear 7–10 days post infection as chlorotic spots that develop teliospores within a pustule on the abaxial leaf surface within 14–18 days post infection (De Backer et al., 2011; Wang et al., 2020), but short periods of high temperatures (over 30°C) can apparently prolong the incubation period to 8 weeks (Whipps, 1993). Leaf wetness and a high relative humidity are essential for basidiospore formation, survival, and infection. Light does not affect germination of teliospores or basidiospores (Firman and Martin, 1968). Successful aerial transport needs to occur under conditions of high relative humidity, as basidiospores lose their ability to germinate after 5 min at relative humidity of 80% and after 1 h at relative humidity of 90% (Firman and Martin, 1968).

To establish successful infection, pathogens should gain access to the cells of the host plant. Young leaves are more susceptible than mature leaves. Studies have shown that species in family Asteraceae differed in resistance to the white rust of chrysanthemum due to leaf traits, such as trichomes and cuticular wax layer, acting as a protective barrier against pathogen’s attacks (Zeng et al., 2013; Wang et al., 2020). Some chrysanthemum cultivars appear to be more resistant than others (Kumar et al., 2021; Zeng et al., 2013). Thus, C. indicum, C. yoshinaganthum, C. makinoi var. wakasaense, C. nankingense, C. vestitum, C. lavandulifolium, C. crassum, Ajania tripinnatisecta were shown to be immune, and strong resistance was demonstrated in C. japonense, C. × shimotomaii, A. przewalskii as well as in White Dolly, White Andaman, IIHR6-32, IIHR9-3, IIHR6-41, and other cultivars of C. × morifolium (Kumar et al., 2011; Zeng et al., 2013). Because wide range of crosses are relatively easy to achieve in the Chrysanthemum complex, these immune and highly resistant accessions could be promising for white rust resistance breeding.

For more information, see Water (1981) and De Backer et al. (2011).

Symptoms

The disease affects mainly leaves, but in the case of severe infestation, spread is seen onto the stems, bracts, and the flowers. Initial symptoms appear as numerous, pale green to yellow spots, up to 5 mm in diameter which develop on the upper surface of the infected leaves (Water, 1981; Mondal and Singh, 2019). Pinkish white coloured telia pustules develop mostly on the lower surface of the leaves and rarely on the upper surface (EPPO, 2020). Under a stereo microscope, telia pustules are tan coloured, covered with slimy layer at an early stage and becoming waxy at a later stage (Water, 1981; EFSA, 2013; Mondal and Singh, 2019). As the spots on the upper surface become sunken, so these pustules become quite prominent and turn whitish when basidiospores are produced. In some cases, a secondary ring of small pustules is formed around the initial pustules (EFSA, 2013). Heavily infected leaves wilt, curl and eventually become necrotic, but they remain attached to the plant and gradually dry up completely (Water, 1981; EFSA, 2013; Mondal and Singh, 2019).

On bracts and stems, sori (complex aggregations of sporangia) sometimes develop when crops are heavily affected, while on flowers infection has been recorded as necrotic flecking with occasional pustules (Dickens, 1970).

Teliospores germinate only in situ (on plants, but not on agar medium).

Morphology

Pustules are 2–5 mm, tan to pink, later white, usually on the lower side of the leaves (hypophyllous), rarely on the upper side of the leaves (epiphyllous), stems, bracts or flowers. The teliospores are oblong to oblong-clavate, slightly constricted at the middle, thin walled, bicelled, pedicellate, pale yellow, 32–45 x 12–18 µm, 1–2 µm thick at sides, hyaline (Baker, 1967; De Backer et al., 2011; Mondal and Singh, 2019). The promycelia are tubular, mostly segmented, short, stout, 33 × 8 µm, 1-to-3-celled, the apical cell often with a lobed appearance, and sometimes branched. Usually two basidiospores are formed per promycelium and basidiospores are hyaline, slightly curved, broadly ellipsoid to fusiform, 7–14 × 5–9 µm, with apical scar (Baker, 1967; Kapooria and Zadoks, 1973; De Backer et al., 2011; EFSA, 2013; Mondal and Singh, 2019).

For more details, see Baker (1967) and Kapooria and Zadoks (1973).

Detection and inspection methods

P. horiana can be detected following the EPPO diagnostic protocol PM 7/027 (2): Puccinia horiana (EPPO, 2020). Detection of P. horiana can be based on the presence of clearly visible symptoms on the leaves (and occasionally also on bracts, stems and flowers) and on morphological features of the teliospores following the EPPO diagnostic protocol (EPPO, 2020). If only chlorotic spots are visible, then detection is possible via incubation or real-time polymerase chain reaction (PCR). For asymptomatic plants, detection can also be done with real-time PCR. Numerous other rust fungi have been reported on chrysanthemums, but P. horiana is easily distinguished from other species by its smooth, hyaline teliospores that always germinate in situ on the living leaf (EPPO, 2020).

Identification and verification of P. horiana is based on microscopic verification of the morphological characteristics of the teliospores (EPPO, 1994, 2020) and/or on specific conventional or real-time PCR tests after DNA extraction of excised pustule material (Alaei et al., 2009; EPPO, 2020). The PCR tests are based on the ribosomal DNA internal transcribed spacer regions and allow detection of all P. horiana strains tested so far. The real-time PCR assays are very sensitive and the lowest proportion of infected plant material that can be detected is 0.001 % (Alaei et al., 2009).

For more information, see EPPO (2020).

The fungus may be spread on infected cuttings and plants, including cut flowers, of glasshouse chrysanthemums. Host plants are widespread in the EPPO region and are susceptible to the pest during their whole growing cycle. Climatic conditions are suitable for infection and sporulation of P. horiana over a wide area of the EPPO region. The basidiospores of P. horiana are released and carried to new hosts by wind over a distance of up to 700 m (De Backer et al., 2011; Wang et al., 2020). After establishment, aerial spread is assumed to be the cause of local infection. Owing to the absence of physical barriers, the probability of aerial spread is higher when chrysanthemum and daisy species are grown as multiflora plants (in a specific manner of propagation when several or many plants are grown from a single root). This is shown by a higher level of disease incidence in outdoor-grown crops (EFSA, 2013).

No vectors of P. horiana are known (EFSA, 2013).

Economic impact

P. horiana is a serious pest in nurseries, frequently causing complete loss of glasshouse chrysanthemum crops. The pest can infect 12 chrysanthemum and daisy species, but it is particularly known as a pathogen of the commercially important C. × morifolium which is grown for the production of cut flowers, potted plants, and garden chrysanthemums. The turnover of chrysanthemum on the Dutch flower auctions was 332 million EUR for cut flowers and 30 million EUR for potted plants in 2008 alone, making it one of the most important floral species (Alaei et al., 2009). An important outbreak of white rust disease caused by P. horiana severely damaged the chrysanthemum crops in 12 different glasshouses in Türkiye in 2007, resulting in yield losses of up to 80% (Munilakshmi et al., 2023). India is the second largest world producer of flowers (after China) and this fungus was considered to be the most destructive and devastating pathogen, causing severe yield and quality loss in Himachal Pradesh state of the country (Mondal and Singh, 2019).

Severe outbreaks also occurred in France, England, and Denmark and the pest has since spread rapidly throughout the countries causing extensive losses. At the present time, white rust is established in most western European countries in most chrysanthemum-growing areas (Whipps, 1993; Alaei et al., 2009; EPPO, 2013), where it can cause significant economic loss in the cut flower industry if not controlled properly.

Control

Intensity of disease symptoms depends on susceptibility of cultivars, but temperature and air humidity are also very important factors (Firman and Martin, 1968). Overhead irrigation should be avoided because high humidity stimulates disease (EPPO, 1994). Among the available strategies to control this rust disease, fungicide treatments are a basic method, however, breeding for host-plant resistance is also an effective strategy (Sriram et al., 2020; Munilakshmi et al., 2023).

Studies on the control of P. horiana found high effectiveness of some fungicides (Wojdyła, 2004; Sriram et al., 2020; Munilakshmi et al., 2023), however, considering the rise of resistance to fungicides, there is a necessity of search for alternative management solutions such as biological control (EFSA, 2013; Munilakshmi et al., 2023).

The fungus Verticillium lecanii (Ascomycota: Cordycipitaceae), a hyperparasite of rust fungi, was assessed as a potentially good agent for an integrated pest control program on all-year-round chrysanthemums, but its application is technologically complicated (Whipps, 1993). Cladosporium cladosporioides and C. pseudocladosporioides (Ascomycota: Cladosporiaceae) were also assessed due to their antagonistic and hyperparasitic effects against P. horiana and the results suggested that these fungi have a high potential as biological control agents of chrysanthemum white rust (Torre et al., 2017). Some chrysanthemum cultivars, e.g. national varieties of chrysanthemum (Kusumaswasti, Marimar, and Yulimar) from Central Java and certain Chinese cultivars of C. indicum, C. yoshinaganthum, C. makinoi var. wakasaense, C. nankingense, C. vestitum, C. lavandulifolium, C. crassum, and Ajania tripinnatisecta are resistant or less susceptible to the pest as shown by practical observation and resistance screening (Zeng et al., 2013; Bety and Pangestuti, 2021) and at least seven genes are considered to be linked to resistance against P. horiana (De Backer et al., 2011). Resistance to white rust in chrysanthemum cultivars is primarily governed by monogenic control, with several species exhibiting resistance. Consequently, it is imperative to adopt sustainable strategies that leverage genetically determined resistance to identify potential sources of resistance. Wide range of crosses emerges as a promising approach for breeding white rust-resistant varieties, capitalizing on the genetic diversity available within different chrysanthemum species and cultivars.

For more details, see also Grouet (1984), Wojdyła (2004), Sriram et al. (2020), and Munilakshmi et al. (2023).

Phytosanitary risk

P. horiana is included in the A1 List of quarantine pests of Comunidad Andina (CAN), the A2 List of pests recommended for regulation which are present in the EPPO region (EPPO, 2023), the A2 List of Eurasian Economic Union (EAEU, 2016), as well as quarantine lists of several individual countries of the world.

In the main European chrysanthemums production areas, the incidence of P. horiana infections in cut flowers and potted plants is considered low (EFSA, 2013). The incidence of P. horiana infections in multiflora plants, which are usually grown outside, is considered higher owing to the exposure to outdoor weather conditions, but the incidence is still limited and with only local effects (EFSA, 2013).

Plant material of chrysanthemum cultivars for propagation purposes originating from infested areas may carry P. horiana as teliospores in pustules or as mycelium, both of which are capable of surviving transport and storage conditions and pest management procedures. Moreover, in the main production areas in the EU it is considered that inoculum of the pathogen is generally present (EFSA, 2013) so the intensification of chrysanthemum production with high plant density in humid glasshouses provides an ideal environment for the fungus to develop. In countries in which the pathogen is not established and where no preventive action is taken, the damage could be particularly devastating if the pathogen is unexpectedly introduced and spread with plants for planting (EFSA, 2013).

When P. horiana is not present in a country and where it is regulated as a quarantine pest, appropriate measures may consist of import of plants or cuttings which have come from premises which have been officially inspected at least monthly, during the 3 months prior to dispatch and on which no symptoms of P. horiana have been known to have observed during that period, and in the immediate vicinity of which no symptoms of P. horiana have been known to have occurred during the 3 months prior to export, or when plants or cuttings have undergone appropriate treatment against P. horiana (as it was suggested in the past by the EU Council Directive 2000/29/EC; EU, 2000).

When P. horiana is already present in a country and treated as a regulated non-quarantine pest (RNQP), then the following phytosanitary measures can be recommended: (a) plants intended for planting have been derived from mother plants which have been inspected at least monthly during the previous 3 months and no symptoms seen at the site of production; or (b) mother plants showing symptoms have been removed and destroyed, along with plants within a 1 m radius, and an appropriate physical or chemical treatment has been applied to the plants which have been inspected before dispatch and found free from symptoms (Picard, 2018; RNQP, 2018; EU, 2019).

Alaei H, De Backer M, Nuytinck J, Maes M, Höfte M & Heungens K (2009) Phylogenetic relationships of Puccinia horiana and other rust pathogens of Chrysanthemum × morifolium based on rDNA ITS sequence analysis. Mycological Research 113(6–7), 668–683. https://doi.org/10.1016/j.mycres.2009.02.003

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De Backer M, Alaei H, Van Bockstaele E, Roldan-Ruiz I, van der Lee T, Maes M & Heungens K (2011) Identification and characterization of pathotypes in Puccinia horiana, a rust pathogen of Chrysanthemum × morifolium. European Journal of Plant Pathology 130, 325–338. https://doi.org/10.1007/s10658-011-9756-8

EAEU (2016) Common List of Quarantine Pests of the Eurasian Economic Union approved by Decision No. 158 of the Eurasian Economic Commission of November 30, 2016. Available at: https://www.consultant.ru/document/cons_doc_LAW_213644/

EFSA Panel on Plant Health (PLH) (2013) Scientific Opinion on the risk to plant health posed by Puccinia horiana Hennings for the EU territory, with the identification and evaluation of risk reduction options. EFSA Journal 11(1), 3069. https://doi.org/10.2903/j.efsa.2013.3069

EPPO (1998) EPPO Standard PP 2/13(1) Guideline on good plant protection practice: Ornamental plants under protected cultivation. EPPO Bulletin 28, 363–385. https://onlinelibrary.wiley.com/doi/epdf/10.1111/j.1365-2338.1998.tb00743.x

EPPO (2002) EPPO Standard PM 4/6(2) Certification scheme for chrysanthemum. EPPO Bulletin 32, 105–114. https://doi.org/10.1046/j.1365-2338.2002.d01-223.x

EPPO (2020) EPPO Standard PM 7/027 (2) Puccinia horiana. EPPO Bulletin 50, 207–216. https://doi.org/10.1111/epp.12658

EPPO (2023) EPPO Standard PM 1/2(32) A1 and A2 Lists of pests recommended for regulation as quarantine pests. https://gd.eppo.int/taxon/PUCCHN/documents

EU (2000) Council Directive 2000/29/EC of 8 May 2000 on protective measures against the introduction into the Community of organisms harmful to plants or plant products and against their spread within the Community. Official Journal of the European Union, L 169 (10.07.2000), p. 1–112. Available at: https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX%3A32000L0029&qid=1708597536729 (Note: no longer in force).

EU (2019) Commission Implementing Regulation (EU) 2019/2072 of 28 November 2019 establishing uniform conditions for the implementation of Regulation (EU) 2016/2031 of the European Parliament and the Council, as regards protective measures against pests of plants, and repealing Commission Regulation (EC) No 690/2008 and amending Commission Implementing Regulation (EU) 2018/2019. Official Journal of the European Union, L 319 (10.12.2019), 1–279. Available at: https://eur-lex.europa.eu/eli/reg_impl/2019/2072/oj

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Grouet D (1984) Mise au point sur les possibilités actuelles de lutte contre la rouille blanche du chrysanthème. Revue Horticole 251, 33–36.

Firman ID & Martin PH (1968) White rust of chrysanthemums. Annals of Applied Biology 62, 429–442.

Kapooria RG & Zadoks JC (1973) Morphology and cytology of the promycelium and the basidiospore of Puccinia horiana. Netherlands Journal of Plant Pathology 79, 236–242. https://doi.org/10.1007/BF01976669

Kumar S, Kumar R, Sriram S, Aswath C, Rao TM & Nair SA (2021) Screening of chrysanthemum (Dendranthema grandiflora) genotypes for resistance to white rust (Puccinia horiana Henn.). Journal of Pharmacognosy and Phytochemistry 10(2), 293–297. https://doi.org/10.22271/phyto.2021.v10.i2d.13820

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RNQP (2018) Puccinia horiana (PUCCHN) https://rnqp.eppo.int/recommendations/summarysheet_pest?pest=PUCCHN

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Torres DE, Rojas-Martínez RI, Zavaleta-Mejía E, Guevara-Fefer P, Márquez-Guzmán GJ & Pérez-Martínez C (2017) Cladosporium cladosporioides and Cladosporium pseudocladosporioides as potential new fungal antagonists of Puccinia horiana Henn., the causal agent of chrysanthemum white rust. PloS One 12(1), e0170782. https://doi.org/10.1371/journal.pone.0170782

USDA APHIS PPQ (2005) Chrysanthemum white rust (CWR) eradication protocol for nurseries containing plants infected with Puccinia horiana Henn. (http://www.aphis.usda.gov/plant_health/plant_pest_info/cwr/downloads/cwrplan.pdf)

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This datasheet was extensively revised in 2024 by Kateryna Davydenko, the Ukrainian Research Institute of Forestry and Forest Melioration and the Swedish University of Agricultural Science. Her valuable contribution is gratefully acknowledged.

EPPO (2024) Puccinia horiana. EPPO datasheets on pests recommended for regulation. https://gd.eppo.int (accessed 2024-12-03)

This datasheet was first published in the EPPO Bulletin in 1982 and revised in the two editions of 'Quarantine Pests for Europe' in 1992 and 1997, as well as in 2024. It is now 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.

CABI/EPPO (1992/1997) Quarantine Pests for Europe (1^st and 2^nd edition). CABI, Wallingford (GB).

EPPO (1982) Data sheets on quarantine organisms, Puccinia horiana. EPPO Bulletin 12(1), 113-117. https://onlinelibrary.wiley.com/doi/epdf/10.1111/j.1365-2338.1982.tb01964.x