Cronartium flaccidum (Scots pine blister rust)

Pictures

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Picture	Title	Caption	Copyright
Title Uredinia Caption Uredinia on underside of leaf of Paeonia sp. Original X10. Copyright USDA-ARS/Systematic Mycology & Microbiology Laboratory	Uredinia	Uredinia on underside of leaf of Paeonia sp. Original X10.	USDA-ARS/Systematic Mycology & Microbiology Laboratory
Title Telia Caption Telia on underside of Paeonia officinalis leaf. Original X10. Copyright USDA-ARS/Systematic Mycology & Microbiology Laboratory	Telia	Telia on underside of Paeonia officinalis leaf. Original X10.	USDA-ARS/Systematic Mycology & Microbiology Laboratory
Title Telia Caption Telia on underside of Vincetoxicum hirundinaria leaf. Original X25. Copyright USDA-ARS/Systematic Mycology & Microbiology Laboratory	Telia	Telia on underside of Vincetoxicum hirundinaria leaf. Original X25.	USDA-ARS/Systematic Mycology & Microbiology Laboratory
Title Aecia of Endocronartium pini Caption Aecia of Endocronartium pini on twig of Pinus sylvestris. Original X7.5. Copyright USDA-ARS/Systematic Mycology & Microbiology Laboratory	Aecia of Endocronartium pini	Aecia of Endocronartium pini on twig of Pinus sylvestris. Original X7.5.	USDA-ARS/Systematic Mycology & Microbiology Laboratory
Title Aecia on twig Caption Aecia on twig of Pinus sylvestris. Original X7.5. Copyright USDA-ARS/Systematic Mycology & Microbiology Laboratory	Aecia on twig	Aecia on twig of Pinus sylvestris. Original X7.5.	USDA-ARS/Systematic Mycology & Microbiology Laboratory
Title Teliospores Caption Teliospores in telial column. Original X400. Note scale bar. Copyright USDA-ARS/Systematic Mycology & Microbiology Laboratory	Teliospores	Teliospores in telial column. Original X400. Note scale bar.	USDA-ARS/Systematic Mycology & Microbiology Laboratory
Title Teliospores Caption Teliospores in telial column, with basidiospores. Original X200. Note scale bar. Copyright USDA-ARS/Systematic Mycology & Microbiology Laboratory	Teliospores	Teliospores in telial column, with basidiospores. Original X200. Note scale bar.	USDA-ARS/Systematic Mycology & Microbiology Laboratory
Title Urediniospores Caption Urediniospores. Original X1000. Note scale bar. Copyright USDA-ARS/Systematic Mycology & Microbiology Laboratory	Urediniospores	Urediniospores. Original X1000. Note scale bar.	USDA-ARS/Systematic Mycology & Microbiology Laboratory
Title Urediniospores Caption Urediniospores. Original X400. Note scale bar. Copyright USDA-ARS/Systematic Mycology & Microbiology Laboratory	Urediniospores	Urediniospores. Original X400. Note scale bar.	USDA-ARS/Systematic Mycology & Microbiology Laboratory
Title Aeciospores Caption Aeciospores. Original X400. Note scale bar. Copyright USDA-ARS/Systematic Mycology & Microbiology Laboratory	Aeciospores	Aeciospores. Original X400. Note scale bar.	USDA-ARS/Systematic Mycology & Microbiology Laboratory
Title Aeciospores Caption Aeciospores. Original X1000. Note scale bar. Copyright USDA-ARS/Systematic Mycology & Microbiology Laboratory	Aeciospores	Aeciospores. Original X1000. Note scale bar.	USDA-ARS/Systematic Mycology & Microbiology Laboratory

Identity

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Preferred Scientific Name

• Cronartium flaccidum (Alb. & Schwein.) G. Winter 1880

Preferred Common Name

• Scots pine blister rust

Other Scientific Names

• Cronartium asclepiadeum (Willd.) Fr. 1815
• Cronartium nemesiae Vestergr. 1896
• Cronartium paeoniae Castagne 1845
• Cronartium pedicularis Lindr. 1900
• Erineum asclepiadeum Willd. 1806
• Peridermium cornui Rostr. ex Kleb. 1890
• Sphaeria flaccida Alb. & Schwein. 1805

International Common Names

• English: blister: pine rust; blister: Scotch pine rust; Cronartium rust; pine stem rust; resin canker; resin top disease: pine; resin: pine canker; resin-top; resin-top disease; scotch pine blister rust
• Spanish: roya americana del grosellero; roya vesiculosa del pino
• French: rouille americaine du groseillier; rouille de la pivoine; rouille vesiculeuse de l'ecorce du pin

Local Common Names

• Finland: tervasroso
• Germany: Keinzopt; Kiefernrindenblasenrost
• Norway: tyritopp
• Sweden: törskate

EPPO code

• CRONFL (Cronartium flaccidum)
• ENDCPI (Endocronartium pini)

Summary of Invasiveness

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C. flaccidum is a heteroecious rust fungus, completing different stages of its life cycle on different plants. Mating of haploid strains occurs on species of Pinus, followed by the production of aeciospores, which infect various species of herbaceous dicotyledons. An asexual stage producing urediniospores occurs on the dicotyledonous plants, followed by the production of teliospores, the sexual stage, that germinate to form basidiospores that infect pines thus completing the cycle. A closely-related autoecious rust, Endocronartium (Peridermium) pini, only infects Pinus hosts. C. flaccidum is known from Europe and parts of northern and eastern Asia; it is a Regulated Pest for the USA (USDA/APHIS, 2008). As an invasive in other temperate areas, this rust could be damaging on native and introduced pines or the alternate host species. The infections on pines develop slowly, therefore the fungus might be overlooked, such that accidental introduction of the rust could occur through the importation of conifer [Pinopsida] seedlings or trees.

Taxonomic Tree

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• Domain: Eukaryota
•     Kingdom: Fungi
•         Phylum: Basidiomycota
•             Subphylum: Pucciniomycotina
•                 Class: Pucciniomycetes
•                     Order: Pucciniales
•                         Family: Cronartiaceae
•                             Genus: Cronartium
•                                 Species: Cronartium flaccidum

Notes on Taxonomy and Nomenclature

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The diverse interactions of this heteroecious fungus with its hosts have resulted in a complicated nomenclature. Several species of Cronartium were initially identified for the rust on the various dicotyledons that are primary hosts. An anamorph, Peridermium cornui, was described as the aecial form of one of these species (Cronartium asclepiadeum) that is now synonymized with C. flaccidum (Wilson and Henderson, 1966).

Another Peridermium species, Peridermium pini (Willd.:Pers.) Lev., was found to be autoecious, living only on pines [Pinus]. A separate Cronartium name was established for it, but this species came to be viewed, instead, as a race of C. flaccidum (Wilson and Henderson, 1966; Hiratsuka, 1968). Hiratsuka (1969) created the genus, Endocronartium, for such autoecious forms of Cronartium-related rusts. This genus forms units that are more closely related to distinct species of Cronartium than to each other (Vogler and Bruns, 1998). A number of studies have elucidated the close genetic relationship between the heteroecious C. flaccidum and the autoecious P. pini (Moricca et al., 1996; Moricca and Ragazzi, 1998; Vogler and Bruns, 1998; Kasanen et al., 2000; Hantula et al., 2002) as well as the difficulty of separating them on a morphological basis (Gibbs et al., 1988; Kasanen, 1997; Kaitera et al., 1999b).

Description

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C. flaccidum is a heteroecious rust, the spermogonial and aecial stages occurring on species of “hard” or two-needled pines, and the uredinial and telial stages on the leaves of herbaceous species in dicotyledonous families such as Asclepiadaceae, Paeoniaceae, and Scrophulariaceae.

Spermogonia: caulicolous, on cankers, under bark, flat, yellow, turning brown, exuding spermatia in orange droplets.

Aecia: caulicolous, blister-like, 2-7 mm diameter, single or confluent; peridium several cells thick, white, peridial cells rhomboid-ellipsoid, walls thick, verrucose. Aeciospores in chains, globose, ovoid to ellipsoid, or polygonal, verrucose except for a smooth area, 21-36 x 14-24 µm, orange-yellow; wall hyaline, thick, 2-4 µm; warts 1-2 µm high.

Uredinia: hypophyllous, scattered or in groups, blister-like, 100-300 µm diameter. Peridium hemispherical, opening by a central pore. Urediniospores single on pedicel, ellipsoid to ovoid, sparsely echinulate, 18-30 x 11-22 µm, yellow; wall hyaline, 1.5-2.5 µm thick.

Telia: hypophyllous, often developing in uredinia, erumpent; teliospores in chains, adhering in columns to 2 mm or more long, pale orange to cinnamon-brown. Teliospores ellipsoid to cylindrical, not separating, 20-64 x 6-16 µm, smooth, with yellowish wall 1-3 µm thick.

Basidiospores: globose-subglobose, smooth, 4-12 µm diameter, their production giving a whitish appearance to upper ends of telia.

See also Mordue and Gibson (1978), Ragazzi et al. (1987), and Kaitera et al. (1999b).

Endocronartium pini is an autoecious rust, generally considered a closely related form of C. flaccidum, cycling from pine to pine through the infection of needles by spores produced in aecia. These spores are morphologically aeciospores, but function as teliospores (Hiratsuka, 1969). Wilson and Henderson (1966) do not identify any morphological differences between the aecial stages of the two species. Hiratsuka (1968) reported that aeciospores of European isolates of E. pini germinated to produce, for the most part, determinate, septate, usually binucleate, but frequently uninucleate, germ tubes, whereas the aeciospores of C. flaccidum produced indeterminate, aseptate germ tubes that are more frequently binucleate. Subsequently, Gibbs et al. (1988), Kasanen (1997), and Kaitera et al. (1999b) suggested that these germ tube characteristics were not consistently different between the heteroecious and autoecious rusts, so that the aeciospores cannot be used to distinguished these species morphologically.

See also Kuprevich and Tranzschel (1957), Hiratsuka (1969), and Kasanen (1997).

Distribution

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C. flaccidum occurs in Europe and parts of northern and eastern Asia in the Northern Hemisphere (Smith et al., 1988; CABI, 1989). The autoecious form, Endocronartium pini, only occurs in Europe, according to Hiratsuka (1969), but Tai (1979) and Chen (2002) report it from China. Given the difficulty of distinguishing the two forms on Pinus without molecular examination or inoculation of dicotyledonous hosts (Hantula et al., 2002), some of the Asian reports might be erroneous. Azbukina (2008) expected to find E. pini in Siberia, but did not.

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/Region	Distribution	Last Reported	Origin	First Reported	Invasive	Reference	Notes
Asia
Armenia	Present					CMI, 1989; EPPO, 2014
Azerbaijan	Present					CMI, 1989; EPPO, 2014
China	Restricted distribution					Chen, 2002; EPPO, 2014
-Anhui	Present					Cheng et al., 1998
-Guizhou	Present					Jing and Wang, 1989; Chen, 2002
-Heilongjiang	Present					CMI, 1989; Cheng et al., 1995; EPPO, 2014
-Henan	Present					Chen, 2002
-Hubei	Present					Jing and Wang, 1989; Chen, 2002
-Jiangsu	Present					CMI, 1989; EPPO, 2014
-Jilin	Present					CMI, 1989; EPPO, 2014
-Liaoning	Present					CMI, 1989; EPPO, 2014
-Nei Menggu	Present					Chen, 2002
-Shaanxi	Present					Jing and Wang, 1989; Jing et al., 1995; Cao et al., 2000; Zhuang and Wei, 2005
-Shanxi	Present					Cheng et al., 1998
-Sichuan	Present					CMI, 1989; Jing and Wang, 1989; EPPO, 2014
-Tibet	Present					Chen, 2002
-Yunnan	Present					CMI, 1989; EPPO, 2014
-Zhejiang	Present					CMI, 1989; EPPO, 2014
Georgia (Republic of)	Present					CMI, 1989; EPPO, 2014
India	Absent, invalid record					EPPO, 2014
Japan	Present					CMI, 1989; EPPO, 2014
-Hokkaido	Present				Not invasive	Hiratsuka, 1932
-Honshu	Widespread					Kobayashi, 2007
-Kyushu	Present					Kobayashi, 2007
Kazakhstan	Present					Churakov, 1989
Korea, DPR	Present					EPPO, 2014
Korea, Republic of	Present					Yi et al., 1985; CMI, 1989; Cho and Shin, 2004; EPPO, 2014
Taiwan	Present					Hiratsuka and Chen, 1991
Europe
Austria	Present		Native			Widder, 1941; CMI, 1989; EPPO, 2014
Belgium	Present		Native			CMI, 1989; EPPO, 2014
Bulgaria	Widespread		Native	1960		Widder, 1941; CMI, 1989; Denchev, 1995; EPPO, 2014
Czech Republic	Widespread					EPPO, 2014
Czechoslovakia (former)	Widespread		Native			Klebahn, 1938; CMI, 1989; EPPO, 2014
Denmark	Present		Native			Ferdinandsen and Jørgensen, 1938; Hylander et al., 1953; Buchwald NF et al., 1961; CMI, 1989; EPPO, 2014
Estonia	Present		Native			CMI, 1989; EPPO, 2014
Finland	Widespread		Native		Invasive	Liro, 1907; Liro, 1908; CMI, 1989; Hantula et al., 1998; Kaitera and Hantula, 1998; EPPO, 2014
Former USSR	Present					Rozhkov, 1975; Storozhenko, 1987; Leont'eva and Stenina, 1990
France	Present		Native			Cornu, 1886; CMI, 1989; EPPO, 2014
Germany	Present		Native			Klebahn, 1901; Klebahn, 1938; CMI, 1989; EPPO, 2014
Greece	Present		Native		Invasive	Diamandis & de Kam, 1986; CMI, 1989; EPPO, 2014
Hungary	Widespread		Native			CMI, 1989; Szabo, 1998; EPPO, 2014
Ireland	Absent, invalid record					EPPO, 2014
Italy	Present		Native		Invasive	Morionde, 1975; Raddi et al., 1979; Ragazzi and Moriondo, 1980; CMI, 1989; Moricca et al., 1996; EPPO, 2014
Latvia	Present		Native			Kuprevich and Transchel, 1957
Lithuania	Present					Kuprevich and Transchel, 1957; EPPO, 2014
Montenegro	Present					Karadzic and Vujanovic, 2009
Netherlands	Present		Native			Hiratsuka, 1968; CMI, 1989; EPPO, 2014
Norway	Widespread		Native		Invasive	Jørstad, 1925; Hiratsuka, 1968; Roll-Hansen, 1973; CMI, 1989; EPPO, 2014
Poland	Present		Native			CMI, 1989; Siwecki and Chojnacki, 1989; Mulenko et al., 2004; EPPO, 2014
Portugal	Present, few occurrences					EPPO, 2014
-Azores	Present					EPPO, 2014
-Portugal (mainland)	Present		Native			Gonçalves, 1936; CMI, 1989
Romania	Present		Native			Klebahn, 1938; CMI, 1989; EPPO, 2014
Russian Federation	Restricted distribution					Kuprevich and Transchel, 1957; EPPO, 2014
-Central Russia	Present		Native			Kuprevich and Transchel, 1957
-Eastern Siberia	Present		Native			Kuprevich and Transchel, 1957; EPPO, 2014
-Northern Russia	Present		Native		Invasive	CMI, 1989; Krutov, 1989
-Russia (Europe)	Restricted distribution					EPPO, 2014
-Russian Far East	Present		Native			CMI, 1989; Azbukina, 1995; Kakishima et al., 1995
-Southern Russia	Present		Native			Kuprevich and Transchel, 1957
-Western Siberia	Present		Native			Kuzmina and Kuz'Min, 2008; EPPO, 2014
Serbia	Present					EPPO, 2014
Slovenia	Present					Jurc, 2007
Spain	Present		Native			CMI, 1989; EPPO, 2014
Sweden	Widespread		Native		Invasive	Rennerfelt, 1943; Rennerfelt, 1947; Hiratsuka, 1968; Klingström, 1973; Martinsson and Nilsson, 1987; CMI, 1989; EPPO, 2014
Switzerland	Restricted distribution		Native			Widder, 1941; CMI, 1989; EPPO, 2014
UK	Restricted distribution		Native			Wilson and Henderson, 1966; CMI, 1989; EPPO, 2014
-England and Wales	Restricted distribution					EPPO, 2014
-Scotland	Present					Greig, 1987; Greig and Sharpe, 1991; Pei and Gibbs, 1991
Ukraine	Present		Native			CMI, 1989; Dudka et al., 2004; EPPO, 2014
Yugoslavia (former)	Present		Native			CMI, 1989
Yugoslavia (Serbia and Montenegro)	Present					Widder, 1941

Risk of Introduction

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The risk of introduction of either form of this rust is greater for those temperate parts of the Southern Hemisphere, such as Australia, where introduced Pinus species are grown in plantations (Neumann and Marks, 1996). Single-aged monoculture populations could suffer epidemics, in particular, if trees are at a susceptible age and the autoecious Endocronartium pini form is introduced. In addition, dicotyledonous hosts for the heteroecious C. flaccidum are native to the temperate countries of the Southern Hemisphere (USDA-ARS, 2009). Other alternate hosts (Gentiana spp., Paeonia spp.) may be introduced as ornamentals and be grown near introduced ornamental pines.

North America has a significant number of stem rusts of the genera Cronartium, Endocronartium and Peridermium on its native species of three-needled pines (Sinclair and Lyon, 2005), which are in a different section of the genus Pinus from the European two-needled hosts (USDA-ARS, 2009). The ecological situation into which C.flaccidum might invade is therefore complex. Some evidence exists of resistance in the native pines (Raddi and Fagnini, 1978; Kaitera and Nuorteva, 2008). Nevertheless, native or introduced primary (telial) hosts for C.flaccidum are present in North America (USDA-ARS, 2009). Among the USDA/APHIS Regulated Plant Pests, Rossman et al. (2006) place this species in the category of “Threat to major crop plants and forest trees”. Accidental introduction of the rust as a latent infection in pines or on pine wood, appears more likely than on ornamental dicotyledons, but the continent has no lack of pines for planting and regulatory agencies have established phytosanitary procedures (USDA/APHIS, 2008; Canadian Food Inspection Agency, 2009).

Introduction of E. pini to new temperate regions would require importation of infected seedlings without quarantine or the occurrence of viable aecia on bark-bearing pine wood materials or products. Apparently, due to regulatory vigilance or other circumstances, this has not happened yet.

Habitat

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Moricca and Ragazzi (1996) found that C. flaccidum isolates had different cultural morphologies in different regions of Italy. Likewise, Gibbs et al. (1988) determined that Peridermium pini isolates from different parts of Great Britain have different culture morphologies. Kaitera et al. (1999a; 2005) identify C. flaccidum as occurring in southern Finland, whereas Endocronartium pini is found throughout the country. Nevertheless, the two forms can occur in the same or adjacent stands of P. sylvestris (Kaitera et al., 1999a).

Habitat List

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Category	Habitat	Presence	Status
Terrestrial-managed
	Managed forests, plantations and orchards	Present, no further details	Harmful (pest or invasive)
Terrestrial-natural/semi-natural
	Natural forests	Present, no further details	Harmful (pest or invasive)

Hosts/Species Affected

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The commercially valuable aecial hosts of C. flaccidum, specifically two-needled pines of Europe and Asia, vary in susceptibility (Raddi and Fagnini, 1978;Kaitera and Nuorteva 2008). Scots pine, Pinus sylvestris, is the common host in northern Europe, but appears to be less susceptible than the Mediterranean species when tested in southern Europe (Raddi and Fagnini, 1978). The North American three-needled pines tested were found to be relatively resistant. Less is known about the pine species reported as hosts in China (Tai, 1979; Teng, 1996; Cao et al., 2000; Chen, 2002; Zhuang and Wei, 2005), Japan (Kobayashi et al., 2007), Korea (Cho and Shin, 2004) and Taiwan (Hiratsuka and Chen, 1991). Raddi and Fagnini (1978) did not observe spotting on needles of young plants of the Asian species, Pinus densiflora, Pinusmassoniana and Pinus tabuliformis, which were exposed to natural basidiospore inoculation in Italy; these species appeared to be resistant.

The telial hosts of C. flaccidum are herbaceous dicotyledonous plants in at least 10 families, as demonstrated by inoculation tests (Wilson and Henderson, 1966; USDA/APHIS, 2008; Kaitera et al., 2012). Some of the species are not native to the geographic range of the rust, and infection was observed in gardens (Goncalves da Cunha, 1936; Gjaerum, 1974; BPI, 2009). Specialized forms referred to as formae speciales varying with respect to pathogenicity to various dicotyledonous hosts have been identified in Europe (Smith et al., 1988), but inoculation tests (Kaitera and Hantula, 1998; Kaitera, 1999; Kaitera et al., 1999a) have indicated that C. flaccidum has low host specificity. Although differences in host susceptibility within a plant genus were noted (Kaitera, 1999; Kaitera et al., 1999a), the broad host range of C. flaccidum suggests that additional host species are likely to be susceptible. Thus, the rust was recently reported from Paeonia daurica in Ukraine (Dudka et al., 2004) and Siphonostegia chinensis in China (Zhuang and Wei, 2005).

Growth Stages

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Symptoms

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Infection of pine needles may or may not cause yellow-red spots on needles (Ragazzi et al., 1986; Smith et al., 1988); spots may appear only after some months (Ragazzi, 1989). Spermogonia appear within 1 or 2 years (Ragazzi, 1989) or later on older trees (Smith et al., 1988). The fungus grows into the shoots, which become swollen, and aecia are produced after one or two additional years (Grieg, 1987). Cankers on stems also bear blister-like pustules, containing orange-yellow spores, especially at bases of branch whorls (Butin, 1995), and the perennial growth of the fungus results in concentric zones of sporulation. Stems are flattened and deformed (Butin, 1995). Resin is produced from the cankers and in the wood underlying it. If cankers on the trunk grow large enough or separate cankers meet, girdling of the stem may result in death of the top or of the entire tree (Smith et al., 1988). The “resin top” name of the disease derives from the combined death of the tree top with copious visible resin generation. However, years may be required for infections to have this effect (Grieg, 1987). On Pinus sylvestris in Finland, Kaitera (2000) found that the average size of lesions bearing aecia on three- to twenty-year-old stems was about 4 cm in length.

On primary hosts, scattered, small chlorotic or necrotic spots appear on the upper side of leaves, with orange uredinia and, later, bristle-like yellowish to red-brown telia below (Wilson and Henderson, 1966; Ragazzi et al, 1987; Kaitera, 1999; Kaitera and Nuorteva, 2006). Spots are sometimes limited by veins (Ragazzi et al., 1987).

List of Symptoms/Signs

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Sign	Life Stages	Type
Leaves / abnormal colours
Leaves / fungal growth
Leaves / yellowed or dead
Stems / canker on woody stem
Stems / dieback
Stems / gummosis or resinosis
Stems / mould growth on lesion

Biology and Ecology

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Life Cycle

Teliospores in bristle-like telia on dicotyledonous primary host leaves germinate in spring to early summer and produce basidiospores that infect the young pine needles through stomates (Mordue and Gibson, 1978; Ragazzi et al., 1987). Mycelium grows through the needles into the cambium of stems and into the rays (Butin, 1995). Haploid spermogonia are the mating organs produced on shoots within 1 or 2 years; after fertilization, aecia are produced on the canker tissues during the summer of the next year or the year after that (Smith et al., 1988). Aeciospores are wind-blown to young leaves of herbaceous dicotyledons, where infection requires a film of free moisture; uredinia and telia develop on the lower sides of leaves (Ragazzi, 1983). Urediniospores are a repeating spore form, spreading the organism in multiple cycles to susceptible new leaves of the dicotyledonous hosts during the growing season. Telia develop in uredinia or directly from leaves (Ragazzi et al., 1987).

In the autoecious Endocronartium pini, the spores produced by aecia are capable of infecting pine directly, without an intervening telial stage. When free water is present, aeciospores germinate on needles and infect through stomates (Van der Kamp, 1970). Wounding of the stem can enhance infection (Wilson and Henderson, 1966; Gibbs et al., 1988), and infections through stem wounds are more damaging (Van der Kamp, 1970).

Genetics

Moricca et al. (1996) identified three regions of DNA with high similarity in C. flaccidum and E. pini isolates from Europe. The 5.8s ribosomal gene sequence was highly conserved, but some heterogeneity appeared in the ITS1 and ITS2 regions. Nevertheless, the same sequence variants occurred in isolates of both fungi. Moricca and Ragazzi (1998) observed virtually identical restriction fragment length polymorphism (RFLP) profiles, again, suggesting a high degree of affinity between the two fungi. A diagnostic difference between them, observed in single-strand conformation polymorphism (SSCP) analysis of a highly variable region, was of a type found in genetic analyses of differences within a species.

Hantula et al. (1998) also observed a high degree of similarity in two genetic regions in European C. flaccidum and E. pini. Results of additional tests using the two markers led Hantula et al. (2002) to consider the two forms to be the same species. For one highly variable marker, differentiation was lower between the two rusts than within populations of each form.

Reproductive Biology

The two rusts are separated on the basis of their reproduction, because E. pini is autoecious, lacking the stage of sexual recombination on any primary host (Wilson and Henderson, 1966; Hantula et al., 2002). On the other hand, Gibbs et al. (1988) reported infection of a dicotyledonous host invitro, with production of telia, by isolates considered to be the autoecious form. This suggests that E. pini may be “facultatively heteroecious”, although Hantula et al. (2002) consider this unlikely. Kasanen et al. (2000) found support for E. pini as homothallic, if not clonal, whereas allele distribution among aecia of C. flaccidum provided evidence of both heterothallic and homothallic matings.

The spermogonia of E. pini appear to be self-fertilizing or non-functional (Hantula et al., 2002). Spermogonial fluid was observed on only a few infected plants in tests in Finland (Kaitera and Nuorteva, 2008).

Physiology and Phenology

Three specialized types of C. flaccidum in Europe have been proposed depending on the telial host genera and varying in geographic distribution (Smith et al., 1988). Scientific attention has focused on f. sp. typica in western Europe. Kaitera (1999) identified new primary hosts in the genus Melampyrum (Scrophulariaceae, now Orobanchaceae) infected by C. flaccidum in Finland; their susceptibility to the other two formae speciales was not examined.

The pine blister rust organisms also exhibit variations in morphology in culture. Pei and Gibbs (1991) found two morphological types of colonies derived from aeciospores that corresponded to two regions of E. pini in Great Britain. Likewise, Moricca and Ragazzi (1996) observed two groupings of C. flaccidum isolates with different cultural characters that were correlated to their geographic origins in Italy.

Mittempergher and Raddi (1977) observed differences in regional sources of C. flaccidum in Italy. A montane isolate was more virulent on Pinus nigra from the same region than were isolates from other habitats. E.pini spore collections from different areas of Finland also differ in virulence on the pine host, but no significant differences were observed among three C. flaccidum collections (Kaitera and Nuorteva, 2008).

Associations

Insect may play a role in mating in C. flaccidum based on the similarity of its life cycle to that of Cronartium ribicola (Mordue and Gibson, 1978; Smith et al., 1988). In that species, insects are attracted to sweet liquid produced from spermogonia and appear to promote fertilization by carrying spermatia between them (Hunt, 1997).

Pappinen and von Weissenberg (1994) investigated an interaction between Pissodes piniphilus, the pine top weevil, and E. pini. The weevils fed more often on infected branches than on healthy branches, and the fungus may infect through feeding wounds, but results were inconclusive concerning the role for the insect as vector of the fungus.

E. pini is parasitized by the conidial fungus Tuberculina maxima (Wilson and Henderson, 1966; Gibbs et al., 1987), but that does not substantially affect losses due to rust (Moricca et al., 2001). Growth on the aecia apparently reduces sporulation rather than lesion expansion (Van der Kamp, 1970).

Climate

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Climate	Status	Description	Remark
Cs - Warm temperate climate with dry summer	Preferred	Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers
Cw - Warm temperate climate with dry winter	Preferred	Warm temperate climate with dry winter (Warm average temp. > 10°C, Cold average temp. > 0°C, dry winters)
Ds - Continental climate with dry summer	Preferred	Continental climate with dry summer (Warm average temp. > 10°C, coldest month < 0°C, dry summers)
Dw - Continental climate with dry winter	Preferred	Continental climate with dry winter (Warm average temp. > 10°C, coldest month < 0°C, dry winters)

Natural enemies

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Natural enemy	Type	Life stages	Specificity	References	Biological control in	Biological control on
Cladosporium tenuissimum	Antagonist	Spores
Tuberculina maxima	Hyperparasite	Fruit bodies/Spores

Notes on Natural Enemies

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Tuberculina maxima (van der Kamp, 1970) and Cladosporium tenuissimum (Moricca et al., 1999; 2001) are naturally occurring hyperparasites of C. flaccidum.

T. maxima invades C. flaccidum aecia, which reduces the formation and sporulation of aeciospores (van der Kamp, 1970; Gibbs et al., 1987). The fungus also infects the spermogonia of Cronartium spp. and has been found on Cronartium spp. uredinia and telia (Wicker, 1981). In the UK, T. maxima reduced the aecia production of E. pini by 30% (van der Kamp, 1970).

C. tenuissimum inhibits C. flaccidum aeciospore germination in vitro, parasitizes aeciospores and destroys their cell wall, probably using enzymes (Moricca et al., 2001).

No control measures are available in practice to use T. maxima or C. tenuissimum for reducing Cronartium spp. incidence on Pinus spp. (Wicker, 1981; Moricca et al., 2001).

Means of Movement and Dispersal

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Natural Dispersal

Rust aeciospores, urediniospores and sporidia (basidiospores) are distributed by wind (Alexopoulos et al., 1996; Hunt, 1997). Aeciospores and urediniospores may be disseminated greater distances than the basidiospores, which may be limited to less than 500 metres (Hunt, 1997).

Vector Transmission

An association of Endocronartium pini with pine top weevils may involve transmission, but results were inconclusive (Pappinen and von Weissenberg, 1994).

Accidental Introduction

Introduction of either form of the rust would be possible if seedlings or young trees were transported while the systemic infections were latent (USDA/APHIS, 2008).

Pathway Vectors

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Vector	Notes	Long Distance	Local	References
Plants or parts of plants		Yes		USDA/APHIS, 2008
Wind	aeciospores, urediniospores	Yes	Yes	Smith et al., 1988

Plant Trade

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

Wood Packaging

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Wood Packaging not known to carry the pest in trade/transport
Loose wood packing material
Non-wood
Processed or treated wood
Solid wood packing material with bark
Solid wood packing material without bark

Impact Summary

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Category	Impact
Economic/livelihood	Negative

Impact

Top of page Severe epidemics on Pinus sylvestris caused by C. flaccidum have been reported in Sweden (Rennerfelt, 1943; 1947; Martinsson and Nilsson, 1987), Norway (Jørstad, 1925; Roll-Hansen, 1973), Finland (Kaitera et al., 1994; Kaitera, 2000; Kankaanhuhta et al., 2000), Germany (Klebahn, 1938), Greece (Diamandis and de Kam, 1986), UK (Wilson and Henderson, 1966; Murray et al., 1969; Gibbs et al., 1987; Greig, 1987), Russia (Krutov, 1989; Azbukina, 1995) and China (Jing and Wang, 1989). In Italy, C. flaccidum epidemics on Pinus nigra, Pinus pinea and Pinus pinaster were frequently reported from 1953 to 1972 (Moriondo, 1975).

In Finland, severe C. flaccidum epidemics have been reported in young P. sylvestris stands, with about 70% of trees infected (Kaitera, 2000). In some locations in Germany, 21-28% of P. sylvestris over 40 years of age were infected by C. flaccidum (Mülder, 1953). In northern Norway, Endocronartium pini affected 60% of P. sylvestris in some stands (Jørstad, 1925). In Thetford forest in England, UK, the number of P. sylvestris trees infected by E. pini increased from 1 to 10% from 1964 to 1979 (Greig, 1987). A C. flaccidum epidemic in Greece killed 5000 m³ of Pinus spp. trees over a 1000 ha area (Diamandis and de Kam, 1986).

In Sweden, E. pini and C. flaccidum caused 40-70% losses in radial increment in mature P. sylvestris stands (Martinsson and Nilsson, 1987). In northern Finland, E. pini reduced the volume of saw timber trees in mature P. sylvestris stands by 2% in trees bearing stem lesions and by 10% in trees with dead tops (Kaitera et al., 1994). The corresponding reductions in marketing value of saw timber trees were 18 and 15%, respectively (Kaitera et al., 1994). In Scotland, UK, E. pini occurred most frequently in old trees; over 50% of the stands infected by E. pini were more than 30 years old (Murray et al., 1969) and the annual loss in timber wood was 4500 m³. In Italy, C. flaccidum reduced the annual height increment more in severely affected P. nigra trees than in slightly affected trees in years of severe rust incidence (Mittempergher and Raddi, 1975).

Risk and Impact Factors

Top of page Invasiveness

• Has a broad native range
• Abundant in its native range
• Highly adaptable to different environments
• Highly mobile locally
• Long lived
• Has high reproductive potential
• Reproduces asexually

Impact outcomes

• Host damage
• Negatively impacts forestry
• Negatively impacts livelihoods
• Reduced amenity values

Impact mechanisms

• Pathogenic

Likelihood of entry/control

• Difficult to identify/detect as a commodity contaminant
• Difficult to identify/detect in the field
• Difficult/costly to control

Diagnosis

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Polymerase chain reaction (PCR)-amplified fragments of two regions of rDNA can be used in restriction fragment length polymorphism (RFLP) and single-strand conformation polymorphism (SSCP) analysis to distinguish alternating from non-alternating isolates of pine blister rust (Moricca and Ragazzi, 1998). Sequences for several regions of rDNA, particularly those for the 5.8s rRNA examined by Moricca et al. (1996), are currently available in GenBank for comparison (NCBI, 2009).

Detection and Inspection

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The delay of sporulation for months or years after infection of pines (Wilson and Henderson, 1966) reduces the reliability of single inspections of seedlings and young trees to detect this fungus. Spots may or may not result from infection of needles (Raddi et al., 1979; Ragazzi et al., 1986). Infection through wounded stems is also possible (Wilson and Henderson, 1966). Established infections produce cankers with blister-like aecia on stems or bark-bearing wood. In the field, nearby herbaceous alternate hosts can be examined for the presence of uredinia and/or bristle-like telial columns on the undersides of leaves (Kaitera et al., 2005).

Similarities to Other Species/Conditions

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Hantula et al. (2002) showed that C. flaccidum and the autoecious rust Endocronartium pini are genetically almost indistinguishable despite differences in life cyle. The two cannot be distinguished by aeciospore morphology (Kasanen, 1997; Kaitera et al., 1999b). Inoculation tests on the dicotyledonous alternate hosts should establish the difference (Kaitera, 1999; Kaitera et al., 1999a; Kaitera and Nuorteva, 2008, but see Gibbs et al., 1988). Moricca and Ragazzi (1998) identified a restriction fragment length polymorphism (RFLP) technique that distinguished the two forms on the basis of one electrophoretic band resulting from Hinf1 restriction endonuclease digestion of the IGS1 region of rDNA.

In North America, there are at least 11 species of Cronartium including Cronartium ribicola and six species of Peridermium that infect trees in the genus Pinus (Sinclair and Lyon, 2005). To a certain extent, these can be distinguished by aeciospore and urediniospore morphology, as well as by symptomatology. Some cause stem cankers, and other rusts produce galls or witchs’ brooms in infected stems or branches. Others cause no stem symptoms at all (Sinclair and Lyon, 2005). Although some of the common Eurasian hosts have been naturalized e.g. Pinus sylvestris (USDA-NCRS, 2009), tests indicate that the three-needled pines native to North America are not susceptible to C. flaccidum (Raddi and Fagnini, 1978; Kaitera and Nuorteva, 2008). Cronartium comandrae, a widespread North American pine stem rust that also infects introduced two-needled species, also hosts for C. flaccidum, produces unique tear-drop-shaped aeciospores on pine (Sinclair and Lyon, 2005).

Other European rusts that can attack pines have a heteroecious life cycle similar to that of C. flaccidum, but usually infect different alternate hosts. Coleosporium tussilaginis, the pine needle rust, shares a few telial hosts with the blister rust, but produces its spermogonia and aecia on pine needles, not on stems (Smith et al., 1988). Also, teliospores of this rust on species of Melampyrum are single and cylindrical, produced not in long columns, but in waxy crusts (Wilson and Henderson, 1966). Melampsora populnea infects the shoots of two-needled pines, causing shoot bending and/or tip death (Smith et al., 1988). Its linear aecia lack a peridium and the aeciospores are significantly smaller than those of C. flaccidum (Wilson and Henderson, 1966).

Although their aeciospores cannot be distinguished even at the level of scanning electron microscopy (Kasanen, 1997), the invasive species C. ribicola does not infect the primary hosts of C. flaccidum in Europe (Kaitera and Nuorteva, 2006) or the same species of pines, because it is restricted to five-needled (soft) pines (Sinclair and Lyon, 2005). Butin (1995) notes that C. flaccidum tends to infect at the top of a tree rather than at the base of stems or of lower branches, where C. ribicola infection is usually found.

Prevention and Control

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Prevention

Given the possibility of latent infections in Pinus, phytosanitary post-entry quarantine of any imported plants is necessary (USDA/APHIS, 2008). Accidental introduction would also likely be prevented by controlling bark-bearing wood in shipping materials from areas where the rust occurs (see Canadian Food Inspection Agency, 2009: MAF, 2009).

Eradication

Butin (1995) recommends removal of infected branches or trees in stands where the disease is already present. Pruning of infected branches may or may not prevent development of additional cankers on the trunk, although the general purpose of removing inoculum is achieved (Moricca and Ragazzi, 2008).

Control

Cultural control and sanitary measures

Basidiospores are disseminated only over a short distance (Hunt, 1997), therefore removal of the primary hosts from the vicinity of limited plantings of pine is a measure that can reduce infection by the heteroecious C. flaccidum (Mordue and Gibson, 1978; Butin, 1995). In Italy, the alternate host is too common for this effort to be effective or worthwhile; however, development of a “hazard map” of the known distribution of the alternate host allows for planting of susceptible pines away from sources of inoculum (Moricca and Ragazzi, 2008).

Chemical control

The use of fungicides may be practical for rust control on plantation, nursery and garden trees, but is impractical in forests (Moricca and Raghazzi, 2008).

Biological control

The hyperparasite Cladosporium tenuissimum is proposed by Moricca et al. (2001) as a possible means of control for stem rust. The aeciospores are directly penetrated and parasitized by the conidial fungus. Tests on two-year-old pine seedlings in the greenhouse showed that treatment with the parasite prevented new rust infections by an average of 42%.

Host resistance

Selection of more resistant species or provenances of pines for growing in areas of stem blister rust is a feasible and promising means of control; although Moricca et al. (2001) state that breeding efforts were not successful. The testing methodology may be a major factor in the usefulness of results obtained. Because the fungus develops slowly even in susceptible plants, progress in rating the plants for resistance must be slow.

Raddi and Fagnini (1978) used three methods to inoculate seedlings and young plants of different pine species with basidiospores of C. flaccidum. Species from southern Europe were susceptible whereas North American and Asian species appeared resistant. In later tests, differing levels of susceptibility were found in three of the European species (Raddi et al., 1979) and results indicated that selection for resistance might be possible in Pinus pinaster.

Although P. sylvestris appeared resistant in the limited tests in Italy (Raddi and Fagnani, 1978),it is a major host species in northern Europe, and differences in susceptibility have been observed (Mordue and Gibson, 1978). Over a number of years, Kaitera and Nuorteva (2008) tested seedlings 1-7 years old with aeciospores of E. pini and basidiospores of C. flaccidum. Little disease was obtained and no significant differences among provenances of Finnish trees were observed. The apparent resistance of the introduced American species Pinus contorta in the same tests led the researchers to recommend use of that species as an alternative to Pinus sylvestris in Finland.

Although levels of rust disease caused by both forms were low (10% or less), Kuzmina and Kuz’min (2008) did find variation in the resistance of “climatypes” of P. sylvestris from different parts of Russia in trials in Western Siberia. Soil type and humidity affected the severity of disease as well as the strength of the provenance tests.

Among the several alternate hosts of C. flaccidum, differences in susceptibility would be expected as well. Roll-Hansen (1973) found strong resistance in some Paeonia (ornamental peony) cultivars and suggested that use of those in gardens could assist in control of C. flaccidum. Kaitera et al. (1999a) also observed variation in susceptibility among telial hosts in several genera, including Paeonia, but found the rust to have a low host specificity in general, because infections by Finnish isolates occurred on both native and non-native species.

Gaps in Knowledge/Research Needs

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Additional information is needed on variation within C. flaccidum as well as on its relationship with Endocronartium pini. The existence of specialized forms with respect to pathogenicity on telial hosts and/or on the pine species should be investigated beyond western Europe, particularly in Asia, where available host species differ.

References

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