Skip to main content
. 2022 Feb 8;20(2):e07077. doi: 10.2903/j.efsa.2022.7077
Taxonomic information

1. Cronartium coleosporioides

Current valid scientific name: Cronartium coleosporioides

Synonyms: Uredo coleosporioides, Peridermium stalactiforme, Cronartium stalactiforme, Cronartium coleosporioides f. album

Name used in the EU legislation: Cronartium spp. (non‐European) [1CRONG]

Order: Pucciniales

Family: Cronartiaceae

Common name: pine cow wheat rust

Name used in the Dossier: Cronartium coleosporioides; Cronartium spp. (non‐European)

2. Cronartium orientale

Current valid scientific name: Cronartium orientale

Synonyms: –

Name used in the EU legislation: Cronartium spp. (non‐European) [1CRONG]

Order: Pucciniales

Family: Cronartiaceae

Common name: –

Name used in the Dossier: Cronartium spp. (non‐European)

3. Cronartium quercuum

Current valid scientific name: Cronartium quercuum

Synonyms: Cronartium asclepiadeum var. quercuum, Uredo quercus, Uromyces quercus, Puccinia quercus, Melampsora quercus, Dicaeoma quercus, Cronartium quercus, Peridermium cerebrum, Aecidium cerebrum, Cronartium cerebrum, Aecidium giganteum, Peridermium giganteum, Peridermium mexicanum, Peridermium fusiforme, Cronartium fusiforme

Name used in the EU legislation: Cronartium spp. (non‐European) [1CRONG]

Order: Pucciniales

Family: Cronartiaceae

Common name: eastern gall rust of pine

Name used in the Dossier: Cronartium quercuum

Group Fungi
EPPO code

CRONCL: Cronartium coleosporioides

CRONOR: Cronartium orientale

CRONQU: Cronartium quercuum

Regulated status

Cronartium coleosporioides, C. orientale and C. quercuum are listed in Annex II/A of Commission Implementing Regulation (EU) 2019/2072 as Cronartium spp. (non‐European) [1CRONG], currently not present in the EU territories.

Cronartium orientale is listed in the Commission Implementing Regulation (EU) 2020/1217 as pests of concern for Pinus thunbergii.

Cronartium quercuum is listed in the Commission Implementing Regulation (EU) 2020/1217 as a pest of concern for Pinus parviflora.

Cronartium coleosporioides and C. quercuum are listed in the A1 EPPO list.

Pest status in China

Even though Cronartium coleosporioides is not reported to be present in China according to EPPO (online_a) and GBIF (online), in the USDA Fungal Database there is one report of C. coleosporioides present in China on Pinus tabuliformis (Farr and Rossman, online).

Cronartium orientale is present in China (Farr and Rossman, online).

Cronartium quercuum is present and detected in Anhui, Gansu, Guangxi, Guizhou, Hubei, Heilongjiang, Henan, Jiangsu, Jiangxi, Sichuan, Shaanxi, Yunnan and Zhejiang provinces (Dossier Sections 2.0 and 4.0; EPPO, online_b).

Pest status in the EU Cronartium coleosporioides, C. orientale and C. quercuum are absent in the EU (EPPO, online_a,b; Farr and Rossman, online; GBIF, online).
Host status on Pinus parviflora and P. thunbergii

Pinus thunbergii is reported as a host of C. orientale and C. quercuum (Farr and Rossman, online).

There is no information on whether C. orientale and C. quercuum can also attack P. parviflora.

However, Pinus as a genus is reported as a host of both C. coleosporioides and C. quercuum (EPPO, online_c,d).

PRA information
Pest Risk Assessment currently available:
  • EPPO Data Sheets on Quarantine Pests (EPPO, 1997a,b),
  • Scientific Opinion on the pest categorisation of Cronartium spp. (non‐EU) (EFSA PLH Panel, 2018),
  • Commodity risk assessment of black pine (Pinus thunbergii Parl.) bonsai from Japan (EFSA PLH Panel, 2019),
  • UK Risk Register Details for Cronartium coleosporioides (DEFRA, online_a),
  • UK Risk Register Details for Cronartium quercuum (DEFRA, online_b).
Other relevant information for the assessment
Biology

Cronartium coleosporioides is native to North America and it is present in the USA and Canada (EPPO, online_a), while C. quercuum is widely distributed on the American continent (the southernmost occurrence in Guyana) and in Eastern Asia (including the far East of Russia). Cronartium orientale is a species newly segregated in Japan from C. quercuum (Kaneko, 2000). As there is little information about C. orientale specific biology, in this opinion the lifecycle of this pathogen will be considered the same as C. quercuum.

Cronartium spp. are heteroecious rusts that alternate their lifecycle between Pinus spp. (the aecial hosts) and a wide variety of telial hosts, both trees and grasses.

Once the Pinus needles are infected, the pathogen takes one to several years to produce pycnia and aecia. Pycnospores are not infectious and serve as spermatia. Pycnia and aecia of C. coleosporioides appear in spring the same year, while aecia of C. quercuum appear the year after pycnia. Aecia then produce aeciospores, which are airborne and are able to travel long distances carried by wind.

Once aeciospores reach a suitable telial host, infection occurs and uredinia will appear in about 2 weeks. Uredinia produce urediniospores which are airborne and able to re‐infect telial hosts during summer. In late summer and autumn (but earlier in C. quercuum which starts usually 2 weeks after the appearance of uredinia), telia are produced in which basidiospores are formed. Basidiospore can be carried by wind up to 1.5 km distance. Basidiospores will infect Pinus trees via first year needles. The mycelium will then develop into woody tissues, where it overwinters in bark or in the galls whose development is triggered by the presence of the pathogen (EPPO, 1997a,b).

Symptoms Main type of symptoms

Cronartium coleosporioides is part of the Blister Rust group, while C. quercuum (likely with the almost identical C. orientale) is included in the Gall Rust group (Wijesinghe et al., 2019).

The main symptom of C. coleosporioides is dieback of branches. However, when the pathogen is present in association with the fungus Atropellis piniphila, bark necrosis and cankers may appear yellow/orange blisters form and develop vertically, upward and downward, along the stem from infected branches (EPPO, 1997a). It should be noted that A. piniphila is not reported to be present in China.

Cronartium quercuum develops yellow/brown galls on stem or branches, until aecia develop on the gall in a cerebroid pattern (EPPO, 1997b). Infection of seedlings, results in severe stunting or rapid death.

On telial hosts, Cronartium spp. produce yellow spots (uredinia) on the lower side of leaves.

Once symptomatic, all these Cronartium species are easy to detect.

Presence of asymptomatic plants Infected pines will be asymptomatic for one or more years.
Confusion with other pests

Symptoms are generic and can easily misidentified. The genus Cronartium can be identified by analysis of their spores.

Cronartium coleosporioides can be distinguished from other Cronartium spp., including C. quercuum by sequence analysis of the ITS region (Vogler and Bruns, 1998; Wijesinghe et al., 2019).

Host plant range

Aecial hosts for Cronartium coleosporioides are Pinus as a genus, Pinus attenuate, P. banksiana, P. contorta, P. coulteri, P. densiflora, P. echinata, P. halepensis, P. jeffreyi, P. leiophylla var. chihuahuana, P. mugo, P. nigra, P. ponderosa, P. radiata, P. sabiniana, P. sylvestris and P. tabuliformis. Telial hosts are Castilleja species, Cordylanthus sp., Lamourouxia dependens, L. rhinanthifolia, Melampyrum lineare, Orthocarpus luteus, Pedicularis bracteosa, P. groenlandica, Rhinanthus crista‐galli and R. borealis subsp. kyrollae (Farr and Rossman, online).

Aecial hosts for Cronartium orientale are Pinus banksiana, P. densiflora, P. echinate, P. elliottii, P. kesiya, P. luchuensis, P. massoniana, P. mugo, P. nigra, P. nigra subsp. laricio, P. pinaster, P. ponderosa, P. sylvestris, P. sylvestris var. mongholica, P. tabuliformis, P. taiwanesis, P. thunbergii, P. virginiana and P. yunnanensis. Telial hosts are Castanea crenata, C. dentata, C. koreana, C. mollissima, Castanopsis cuspidata, C. sieboldin, Fagus crenata, Quercus acutissima, Q. aliena, Q. dentata, Q. fabrei, Q. glauca, Q. langbianensis, Q. microphylla, Q. mongolica, Q. mongolica subs. crispula, Q. myrsinifolia, Q. palustris, Q. petraea, Q. phellos, Q. rubra, Q. serrata, Q. spinosa, Q. suber, Q. variabilis, Q. wutaishanica, Q. x major and Q. x mccormickii (Farr and Rossman, online).

Aecial host for Cronartium quercuum is Pinus as a genus, including P. parviflora and P. thunbergii. Telial hosts are Castanea mollissima, C. crenata, C. dentata, C. henryi, C. pumila, C. sativa, Castanopsis cuspidata, C. sieboldii, Fagus japonica, Notholithocarpus densiflorus, Rhus chinensis and a large number of Quercus species (Farr and Rossman, online).

Reported evidence of impact Cronartium coleosporioides, C. orientale and C. quercuum are EU quarantine pests.
Evidence that the commodity is a pathway

Needles, branches and stems of Pinus spp. can be infected and carry overwintering mycelium (EPPO, 1997a), although infection could be asymptomatic.

Cronartium sp. was intercepted in 2000 in the UK on Mahonia plants for planting coming from China (EUROPHYT, online).

Surveillance information

Cronartium quercuum is recorded in Dossier Sections 2.0, 4.0 and 5.0 as a pathogen occurring in Zhejiang.

The nursery and its immediate vicinity areas (at least 2 km) are inspected at least six times a year at appropriate intervals targeting pests of EU concern on their main and secondary hosts (Dossier Section 4.0). The survey shall be carried out at least by visual examination of each row in the field or nursery and by visual examination of all parts of the plant above the growing medium, using a random sample of at least 300 plants from a given genus where the number of plants of that genus is not more than 3,000 plants, or 10% of the plants if there are more than 3,000 plants from that genus (Dossier Section 4.0). Inspection shall be conducted to examine the presence or absence of harmful organisms of EU concern (Dossier Section 4.0).