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Puccinia buxi

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Datasheet

Puccinia buxi

Summary

  • Last modified
  • 27 September 2018
  • Datasheet Type(s)
  • Invasive Species
  • Pest
  • Preferred Scientific Name
  • Puccinia buxi
  • Taxonomic Tree
  • Domain: Eukaryota
  •   Kingdom: Fungi
  •     Phylum: Basidiomycota
  •       Subphylum: Pucciniomycotina
  •         Class: Pucciniomycetes
  • Summary of Invasiveness
  • P. buxi is an autoecious microcyclic rust, completing its life cycle with two spore forms on one host. It is native to parts of Europe and Asia. An introduction to the USA, is evidence that it can be invasive wit...

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Pictures

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PictureTitleCaptionCopyright
Telia of Puccinia buxi on Buxus spp. Original x5.
TitleTelia
CaptionTelia of Puccinia buxi on Buxus spp. Original x5.
CopyrightUSDA-ARS/Systematic Mycology & Microbiology Laboratory
Telia of Puccinia buxi on Buxus spp. Original x5.
TeliaTelia of Puccinia buxi on Buxus spp. Original x5.USDA-ARS/Systematic Mycology & Microbiology Laboratory
Teliospores of Puccinia buxi on Buxus spp.  Original x400. Note scale bar.
TitleTeliospores
CaptionTeliospores of Puccinia buxi on Buxus spp. Original x400. Note scale bar.
CopyrightUSDA-ARS/Systematic Mycology & Microbiology Laboratory
Teliospores of Puccinia buxi on Buxus spp.  Original x400. Note scale bar.
TeliosporesTeliospores of Puccinia buxi on Buxus spp. Original x400. Note scale bar.USDA-ARS/Systematic Mycology & Microbiology Laboratory
Teliospore of Puccinia buxi on Buxus spp. Original x400. Note scale bar.
TitleTeliospore
CaptionTeliospore of Puccinia buxi on Buxus spp. Original x400. Note scale bar.
CopyrightUSDA-ARS/Systematic Mycology & Microbiology Laboratory
Teliospore of Puccinia buxi on Buxus spp. Original x400. Note scale bar.
TeliosporeTeliospore of Puccinia buxi on Buxus spp. Original x400. Note scale bar.USDA-ARS/Systematic Mycology & Microbiology Laboratory
Teliospores of Puccinia buxi on Buxus spp.  Original x400. Note scale bar.
TitleTeliospores
CaptionTeliospores of Puccinia buxi on Buxus spp. Original x400. Note scale bar.
CopyrightUSDA-ARS/Systematic Mycology & Microbiology Laboratory
Teliospores of Puccinia buxi on Buxus spp.  Original x400. Note scale bar.
TeliosporesTeliospores of Puccinia buxi on Buxus spp. Original x400. Note scale bar.USDA-ARS/Systematic Mycology & Microbiology Laboratory

Identity

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Preferred Scientific Name

  • Puccinia buxi Sowerby 1809

Other Scientific Names

  • Dasyspora buxi Arthur 1906
  • Dicaeoma buxi (Sowerby) Gray 1821
  • Micropuccinia buxi (Arthur) Arthur & H.S. Jacks. 1921
  • Puccinia buxi DC. 1815
  • Trailia buxi (Arthur) Syd. 1922

International Common Names

  • English: Boxwood rust

Summary of Invasiveness

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P. buxi is an autoecious microcyclic rust, completing its life cycle with two spore forms on one host. It is native to parts of Europe and Asia. An introduction to the USA, is evidence that it can be invasive with respect to other temperate countries, particularly because its hosts in the genus Buxus are often propagated vegetatively and may carry latent infections. Boxwoods have long been popular as ornamentals, therefore the rust’s current absence from North America and temperate regions of the southern hemisphere is puzzling; in the earliest introductions of the host, the pathogen would probably have been ignored or overlooked. Conditions of boxwood cultivation may discourage the rust’s growth and survival.

Taxonomic Tree

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  • Domain: Eukaryota
  •     Kingdom: Fungi
  •         Phylum: Basidiomycota
  •             Subphylum: Pucciniomycotina
  •                 Class: Pucciniomycetes
  •                     Order: Pucciniales
  •                         Family: Pucciniaceae
  •                             Genus: Puccinia
  •                                 Species: Puccinia buxi

Notes on Taxonomy and Nomenclature

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This species is frequently cited as Puccinia buxi DC., but DeCandolle’s name is an illegitimate homonym of Sowerby’s binomial; Arthur’s binomial is treated as a new name (nomen novum).

Description

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Spermogonia, aecia and uredinia absent. Telia amphigenous, on indefinite spots, scattered or confluent, hemispherical, pulvinate, compact, erumpent, dark chestnut-brown. Teliospores oblong to clavate, rounded above, apex not thickened, rounded or attenuate below, 55-90 x 20-35 µm, up to 100 µm long, walls 2.0-2.5 µm thick, brown, upper cell with apical germ pore, lower cell with superior germ pore; pedicels hyaline, persistent, very long, up to 160 µm.

See Grove (1913) and Hiratsuka et al. (1992)  for more details.

Distribution

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P. buxi has been reported from Europe, North Africa, Iran, Japan, and China (Dennis, 1986). Occurrence in the islands of the Azores, Madeira, and the Ryukyus of Japan (Dennis, 1986) are presumably the result of introductions. Specimens have been collected from other parts of the range of the primary host, Buxus sempervirens (boxwood) (BPI, 2009).

Distribution Table

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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/RegionDistributionLast ReportedOriginFirst ReportedInvasiveReferenceNotes

Asia

ChinaPresentZhuang, 2003
-SichuanRestricted distributionZhang et al., 1997Daba Mountains
IranPresentBPI, US National Fungus Collections; Dennis, 1986
JapanPresentPresent based on regional distribution.
-KyushuPresent, few occurrences
-Ryukyu ArchipelagoPresentDennis, 1986
TurkeyPresentGöbelez, 1963; Huseyin, 2005

North America

USAPresentPresent based on regional distribution.
-GeorgiaPresentBPI, US National Fungus Collections2004
-PennsylvaniaEradicated2006Introduced Invasive NAPPO, 2006One location

Europe

BelgiumPresentBPI, US National Fungus Collections1883
FranceWidespreadNative Not invasive BPI, US National Fungus Collections; Liou, 1929; Durrieu, 2001
GermanyPresentBPI, US National Fungus Collections; Braun, 1982
GreecePresentNativePantidou, 1973
IrelandPresentBPI, US National Fungus Collections1933
ItalyPresent Not invasive BPI, US National Fungus Collections1876, 1882, 1889
PolandPresentMajewski, 1979
PortugalPresentGonzalez Fragoso, 1918
-AzoresPresentGjærum and Sunding, 1986
-MadeiraPresent, few occurrencesBPI, US National Fungus Collections; Gjærum and Sunding, 1986
Russian FederationPresentPresent based on regional distribution.
-Southern RussiaPresentBPI, US National Fungus CollectionsNear Chosta in Caucasus Moutains. 1982
SloveniaPresentHauptman, 2008In arboretum
SpainPresentNativeGonzalez Fragoso, 1918; Llorens i Villagrassa I, 1984
SwitzerlandPresentBPI, US National Fungus Collections1850, 1900, 1927
UKWidespreadGrove, 1913; Foister, 1961; Dennis, 1986; Dennis, 1995

History of Introduction and Spread

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In the summer of 2005, a nursery in Pennsylvania, USA received a shipment of boxwood (Buxus sempervirens) cuttings from various locations in Greece (NAPPO, 2006). Rooted cuttings were found to be infected with P. buxi the next spring. The infected plants were destroyed by autoclaving, and another shipment to an American nursery was quarantined.

Introductions

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Introduced toIntroduced fromYearReasonIntroduced byEstablished in wild throughReferencesNotes
Natural reproductionContinuous restocking
Maryland Greece 2005 Horticulture (pathway cause)NAPPO (2006) Accidental, eradicated

Risk of Introduction

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As the infection can be asymptomatic during the usual growing season, infected plant material or plants can be collected or grown and then transported across borders and oceans. Obviously infected material coming from various European countries to the USA also has been intercepted by the phytosanitary authorities (BPI, 2009). Boxwood (Buxus sempervirens) has long been a popular ornamental plant, thus it is surprising that introduction in earlier times has not resulted in establishment of this pathogen in the USA and other countries in temperate regions outside Europe. The usual conditions of boxwood cultivation and care may prevent the rust from surviving and proliferating (Durrieu, 2001), but the biology of the fungus is not known well enough to explain its low rate of spread.

Habitat List

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CategorySub-CategoryHabitatPresenceStatus
Terrestrial
Terrestrial – ManagedManaged forests, plantations and orchards Present, no further details Natural
Terrestrial ‑ Natural / Semi-naturalNatural forests Present, no further details Natural

Hosts/Species Affected

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The rust has been reported from Buxus sempervirens (boxwood) and Buxus microphylla (littleleaf boxwood), commonly grown ornamentals, as well as from the Asian species, Buxus sinica (Chinese boxwood), a cold-hardy species from Korea (Batdorf, 1995).

Host Plants and Other Plants Affected

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Plant nameFamilyContext
Buxus balearicaBuxaceaeOther
Buxus microphylla (little-leaf box)BuxaceaeOther
Buxus microphylla var. japonicaBuxaceaeOther
Buxus sempervirens (common boxwood)BuxaceaeMain
Buxus sinica (chinese box)BuxaceaeOther

Growth Stages

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Symptoms

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Black telia develop on indefinite spots on thickened areas of the leaves (Grove, 1913). Smith et al. (1988) report hypertrophy and dieback of new growth caused by this rust.

List of Symptoms/Signs

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SignLife StagesType
Leaves / abnormal colours
Leaves / abnormal leaf fall
Leaves / fungal growth
Leaves / leaves rolled or folded
Stems / dieback

Biology and Ecology

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P. buxi is an autoecious microcyclic rust, completing its life cycle on one host. Teliospores develop in the leaves through autumn and winter, emerging through the epidermis in winter or spring. They are not shed, but remain on the leaf and germinate without dormancy (Wilson and Henderson, 1966). The basidiospores produced then infect the new leaves (Grove, 1913). The teliospores have been reported to fall apart easily into their two cells (Grove, 1913), but the possible role of this character in dissemination of the fungus has not been examined.

Preece (2000) reported that the rust is relatively rare in Great Britain, occurring only on old bushes/trees, some hundreds of years old, but the many newer plantings or plants for sale in recent decades have not been infected. When Preece did find rusted leafy material, it had been imported from southern Europe. In response to Preece’s presentation, Durrieu (2001) reported that the rust, though common on wild boxwood in Europe, is absent in areas of the Pyrenees mountains and in Spain where the host grows without tree cover. On the other hand, the rust is prevalent in shady places regardless of plant age; fir [Abies] or beech [Fagus/Nothofagus] forests on northern slopes usually harbour infected boxwood plants. According to Durrieu, the rust appears only on north sides of shaded bushes, not on the sunny sides. Thus the fungus appears to require the shaded, more humid conditions natural to the understory habitat of the wild boxwood (Batdorf, 1995). As in Great Britain, rust is absent from the smaller plants cultivated in French gardens, but is found on larger plants in old gardens where the plants are shaded (Durrieu, 2001). Durrieu further noted that the rust infects only new growth, not older leaves, and suggests that regular pruning of garden plants, removing the newer growth, may restrict the survival and spread of boxwood rust.

Climate

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ClimateStatusDescriptionRemark
Cf - Warm temperate climate, wet all year Preferred Warm average temp. > 10°C, Cold average temp. > 0°C, wet all year
Cs - Warm temperate climate with dry summer Preferred Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers

Means of Movement and Dispersal

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Natural Dispersal (Non-Biotic)

Rust basidiospores are usually wind-disseminated (Alexopoulos et al., 1996). The teliospores are reported to break apart (Grove, 1913); this may be a mechanism for dispersal of the upper cells.

Accidental Introduction

In the summer of 2005, a nursery in Pennsylvania, USA received a shipment of boxwood (Buxus sempervirens) cuttings from various locations in Greece (NAPPO, 2006). Rooted cuttings in the nursery then developed telia of P. buxi in spring 2006.

Preece (2000) observed telia of the rust in England on cuttings in floral bouquets imported from southern Europe.

Pathway Causes

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CauseNotesLong DistanceLocalReferences
Cut flower tradeFoliage used as greenery in bouquets Yes Yes Preece, 2000
Horticulture Yes Yes NAPPO, 2006
Nursery tradeAnticipated possibility Yes Yes NAPPO, 2006

Pathway Vectors

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VectorNotesLong DistanceLocalReferences
Plants or parts of plantslatent or overlooked infections Yes Yes NAPPO, 2006; Preece, 2000
WindBasidiospores Yes Alexopoulos et al., 1996

Plant Trade

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Plant parts liable to carry the pest in trade/transportPest stagesBorne internallyBorne externallyVisibility of pest or symptoms
Leaves hyphae; spores Pest or symptoms not visible to the naked eye but usually visible under light microscope
Plant parts not known to carry the pest in trade/transport
Bark
Bulbs/Tubers/Corms/Rhizomes
Flowers/Inflorescences/Cones/Calyx
Fruits (inc. pods)
Growing medium accompanying plants
Roots
Seedlings/Micropropagated plants
Stems (above ground)/Shoots/Trunks/Branches
True seeds (inc. grain)
Wood

Impact Summary

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CategoryImpact
Cultural/amenity Negative
Economic/livelihood Negative

Economic Impact

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Any losses due to this fungus are likely to result from restriction on exports or imports of Buxus plants or plant material, or from the destruction of infected imported planting material by nurseries or quarantine authorities.

Environmental Impact

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Some Buxus species are endangered or threatened (Batdorf, 2004); introduction of the rust to their native regions could add to the threats to their survival.

Social Impact

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The presence of the pathogen in Europe has not prevented use as an ornamental in new plantings (Preece, 2000; Durrieu, 2001).

Risk and Impact Factors

Top of page Invasiveness
  • Proved invasive outside its native range
  • Has a broad native range
  • Abundant in its native range
  • Tolerant of shade
Impact outcomes
  • Host damage
Impact mechanisms
  • Parasitism (incl. parasitoid)
  • Pathogenic
Likelihood of entry/control
  • Highly likely to be transported internationally accidentally
  • Difficult to identify/detect as a commodity contaminant

Diagnosis

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No DNA sequences of this species that could be used in laboratory identification of the fungus or detection of the fungus in plant tissue have been deposited in the GenBank database (NCBI, 2009) as of September, 2009.

Detection and Inspection

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Both sides of the newest leaves of Buxus plants should be inspected for black pustules containing large, thick-walled, two-celled stalked spores. On plants without pustules, the newest leaves should be examined for spots accompanied by a thickening of the leaves.

Similarities to Other Species/Conditions

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No other rust fungi are reported on Buxus species. The asexual fungus Macrophoma candollei [Dothiorella candollei] also causes leaf spots on boxwood (Buxus sempervirens). Its small black pycnidia develop on the undersides of leaves, but the disease begins and is more severe on the oldest of the bush’s foliage, rather than on the newest leaves. The pycnidia produce tendrils, often called cirrhi, of single-celled spores (Batdorf, 1995).

Prevention and Control

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SPS Measures

The Animal and Plant Health Inspection Service of the US Department of Agriculture (APHIS-USDA) developed rules for permitting the importation of artificially dwarfed or “penjing” plants from China, in pots containing growth media rather than bare-rooted (USDA/APHIS, 2003). Buxus sinica (Chinese boxwood), a host for P. buxi (Zhang et al., 1997), was among the plants governed by the rule. Requirements for production of plants for export that relate to the exclusion of P. buxi include that the plants should be developed from clean inspected “mother” stock, that they should be rooted and grown in approved media in an active condition for at least 4 months before export, and during that time, they are kept in a greenhouse practicing sanitary procedures, including inspections, to exclude pests and pathogens (USDA/APHIS, 2003).
 
After this rust was reported from a nursery in Pennsylvania, USA, a quarantine was placed on rooted cuttings and plants resulting from a shipment of Buxus material from Greece to a nursery in Maryland in the USA (NAPPO, 2006).
 
Fungicide sprays should be prohibited during such post-entry quarantine of Buxus plants because the fungicides can suppress development of the fungus and disease symptoms. The distribution or sale of asymptomatic plants could spread the fungus to other areas (NAPPO, 2006).
 
Cultural Control and Sanitary Measures
 
Planting for sun and air circulation, as well as thinning and pruning for control of other fungal diseases (Batdorf, 1995), may create conditions that retard the growth and spread of P. buxi. The removal of any shed leaves will reduce available inoculum. As Durrieu (2001) indicates, pruning may remove susceptible and/or infected leaves.

Gaps in Knowledge/Research Needs

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More information is needed on the biology and ecology of this rust fungus, including the means and conditions of dispersal and the conditions of temperature and humidity required for germination, infection, growth and sporulation.

References

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Alexopoulos CJ; Mims CW; Blackwell M, 1996. Introductory Mycology. Fourth edition. New York, USA: John Wiley and Sons Inc., 868 pp.

Batdorf LR, 1995. Boxwood handbook : a practical guide to knowing and growing boxwood. Virginia, USA: American Boxwood Society, 123 pp.

Batdorf LR, 2004. Boxwood: An Illustrated Encyclopedia. Virginia, USA: American Boxwood Society, 343 pp.

BPI (US National Fungus Collections), 2009. Fungal Databases - Specimens. Beltsville, USA: Systematic Mycology and Microbiology Laboratory, Agricultural Research Service, USDA. www.nt.ars-grin.gov/fungaldatabases/specimens/specimens.cfm

Braun U, 1982. [English title not available]. (Die Rostpilze (Uredinales) der Deutschen Demokratischen Republik. Feddes Repertorium.) Zeitschrift für Botanische Taxonomie un Geobotanik, 93:213-334.

Dennis RWG, 1986. Fungi of the Hebrides. Kew, UK: Royal Botanic Gardens, 383 pp.

Dennis RWG, 1995. Fungi of South East England. Richmond, UK: Royal Botanic Gardens, 295 pp.

Durrieu G, 2001. More about box rust (Puccinia buxi). Mycologist, 15:144.

Foister CE, 1961. The economic plant diseases of Scotland: a survey and check list covering the years 1924-1957. Tech. Bull. Dep. Agric. Scot, 1:iv + 209 pp.

Gjærum HB; Sunding P, 1986. Flora of Macaronesia. Checklist of rust fungi (Uredinales). Sommerfeltia, 4. 42pp.

Gonzalez Fragoso R, 1918. [English title not available]. (La roya de los vegetales. Enumeracion y distribucion geografica de los Uredales. Conocidos hasta hoy en la Peninsula Iberica e Islas Baleares. Trabajos del Museo Nacional de Ciencias Naturales.) Serie Botanica, 15:1-267.

Grove WB, 1913. The British rust fungi (Uredinales): their biology and classification. Cambridge, UK: Cambridge University Press.

Göbelez M, 1963. [English title not available]. (La mycoflore de Turquie.) Mycopathologia et Mycologia Applicata, 19:296-314.

Hauptman T, 2008. Tree Diseases of Arboretum Volcji Potok. Ljubljani, Slovenia: Univerza v Ljubljani, 69 pp. http://www.digitalna-knjiznica.bf.uni-lj.si/dn_hauptman_tine.pdf

Hiratsuka N; Sato S; Katsuya K; Kakishima M; Hiratsuka Y; Kaneko S; Ono Y; Sato T; Harada Y; Hiratsuka T; Nakayama K, 1992. The Rust Flora of Japan. Takezono, Ibaraki, Japan: Tsukuba Shuppankai, 1205 pp.

Huseyin E, 2005. Materials on the micromycetes of the box tree and rhododendron from Turkey. In: Proceedings of the 16th Symposium of Mycologists and Lichenologists of Baltic States, Cesis (Latvia), 21-25 September 2005. 62-68.

Liou TN, 1929. [English title not available]. (Note sur quelques Uredinees peu communes ou critiques recoltees dans le Midi, le Centre et l'Est de la France.) Bulletin de la Societe Mycologique de France, 45:197-215.

Llorens i Villagrassa I, 1984. Contribution to the knowledge of Uredinales, Ustilaginales and Phragmobasidiomycetes of Spain. I. (Aportación al conocimiento de los Uredinales, Ustilaginales y Fragmobasidiomicetos de España. I.) Anales de Biología, 1(Special Section 1):35-45.

Majewski T, 1979. Grzyby (Mycota). Tom XI. Basidiomycetes. Uredinales II ([English title not available]). Warsaw, Poland: Polska Akademia Naukowe, 462 pp.

NAPPO, 2006. Boxwood Rust (Puccinia buxi) incident in Pennsylvania. Official Pest Reports. Phytosanitary Alert System, North American Plant Protection Organization. Ottawa, Canada: North American Plant Protection Organization. http://www.pestalert.org/oprDetail.cfm?oprID=202&keyword=Puccinia%20buxi

NCBI, 2009. Entrez cross-database search engine. Maryland, USA: National Center for Biotechnology Information. http://www.ncbi.nlm.nih.gov/sites/gquery

Pantidou ME, 1973. Fungus-host index for Greece. Kiphissia, Greece: Benaki Phytopathological Institute, 382 pp.

Preece TF, 2000. The strange story of box rust, Puccinia buxi, in Britain. Mycologist, 14(3):104-106.

Smith IM; Dunez J; Lelliott RA; Phillips DH; Archer SA(Editors), 1988. European handbook of plant diseases. Oxford, UK: Blackwell Scientific Publications.

USDA/APHIS, 2003. Final Rule for the Importation of Artificially Dwarfed Plants in Growing Media From the People's Republic of China. Washington DC, USA: USDA. http://www.aphis.usda.gov/plant_health/ea/downloads/penjingf.pdf

Wilson M; Henderson DM, 1966. British Rust Fungi. Cambridge, UK: The Cambridge University Press, xvii + 384 pp.

Zhang N; Zhuang JY; Wei SX, 1997. Fungal flora of the Daba Mountains: Uredinales. Mycotaxon, 61:49-79.

Zhuang JY, 2003. Flora Fungorum Sinicorum. Volume II Uredinales ([English title not available]). Beijing, China: Science Press, 324 pp.

Contributors

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10/09/09 Original text by:

Systematic Mycology & Microbiology Laboratory, USDA-ARS, 10300 Baltimore Ave., Beltsville, MD 20705, USA

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