California Pest Rating for
Thekopsora minima P. Syd. & Syd. 1915
Former Pest Rating: Q
CURRENT Pest Rating: C
On May 2, 2017, a shipment of blueberry (Vaccinium corymbosum) plants showing symptoms of rust were intercepted in San Francisco by San Francisco County Agricultural Officers. The shipment had originated in Oregon and was destined to a wholesale garden store in San Francisco. A sample of symptomatic leaves was collected by the County and sent to the CDFA Plant Pathology Lab for diagnosis. On May 22, 2017, Suzanne Latham, CDFA plant pathologist, identified the fungal pathogen associated with the diseased leaf tissue as Thekopsora minima. The pathogen was assigned a temporary Q rating. Subsequently, the consequences of introduction and establishment of T. minima in California are assessed and a permanent rating is proposed herein.
History & Status:
Background: Thekopsora minima is a fungal pathogen that causes rust disease in blueberries, cranberries, rhododendrons, and other plants in the Ericaceae family. The pathogen completes its life cycle on two different hosts (heteroecious), namely, blueberries and hemlock, and rust disease can lead to extensive defoliation of severely infected plants.
The blueberry leaf rust pathogen was first recorded as endemic in Northeastern America and Japan. During the past decade, it was introduced on infested Vaccinium corymbosum to other countries including South Africa, Mexico, Australia and Colombia (EPPO, 2016). In the USA, it has been reported mainly from northeastern states and, more recently, from the Western Pacific states of Oregon and California (Wiseman et al., 2016; Shands et al., 2017).
Prior to 1993, taxonomically, Thekopsora minima was generally accepted as a member of a species complex known as Pucciniastrum vaccinii, which was considered the causal agent of blueberry rust. However, Sato et al., (1993) identified three distinct rust fungi species on Vaccinium spp., of which one of them, namely, T. minina, is pathogenic on blueberry, while the other two species, Naohidemyces vaccinii (formerly P. vaccinii) and N. fujisanensis, were not regarded as pathogens of blueberry, although they infected other Vaccinium species. Sato et al., (1993) also noted that at that time, T. minima, occurred, in eastern North America and Japan. Nevertheless, because of the past taxonomic confusion of the species complex, the true global distribution of T. minima may be uncertain as some records attributed to Pucciniastrum vaccinii in Argentina, Hawaii (USA), and Spain may be misidentifications of T. minima (Schrader & Maier, 2015). Thekopsora minima is also known by its synonyms: Peridermium peckii Thüm, 1880, Uredo minima Schwein, 1922, and Pucciniastrum minimum (Schwein.) Arthur 1906 (Farr & Rossman, 2017).
In California, Naohidemyces vaccinii has been reported on Vaccinium membranaceum (thin leaf huckleberry), V. caespitosum (dwarf bilberry), V. parvifolium (red huckleberry), V. ovatum (California huckleberry), and Vaccinium sp. (French, 1989). However, recent reports from several states in the US (Oregon and Michigan), China, Mexico, and South Africa, have indicated that Thekopsora minima is the primary pathogen on northern and southern highbush blueberries (Rebollar-Alviter et al., 2011; Shilder & Miles, 2011; Wideman et al., 2016; Zheng et al., 2017). Rust symptoms have been occasionally observed on various southern highbush blueberry cultivars (Vaccinium corymbosum) within California’s central coastal area, with particular incidences noted in Santa Barbara County in 2010 and 2006 (personal communications: Dr. Timothy D. Miles, Assistant Professor of Plant Pathology, California State University Monterey Bay, and Dr. Janet C. Broome, Global Plant Healthy Senior Manager, Driscoll’s, 2017). Rust in blueberry was also observed in Ventura County, and has most likely been in the State since the early 2000s (personal communication: Dr. Janet C. Broome, Driscoll’s, 2017). In 2016-2017, rust symptoms, observed on several blueberry plants and cultivars in a field trials in Watsonville, Santa Cruz County, were confirmed by molecular sequencing to be caused by T. minima and marked a first published report of this pathogen in California (Shands, et al., 2017). On August 9, 2017, in order to officially substantiate the presence of blueberry rust in California, official samples of symptomatic blueberry plant tissue were collected from infected plants in Santa Cruz and Ventura Counties, by the respective County Agricultural officials and submitted to the CDFA Plant Pathology Laboratory for identification of the associated pathogen. Following morphological and molecular sequence analysis, Cheryl Blomquist, CDFA plant pathologist, confirmed the pathogen to be T. minima.
Disease development: Teliospores of T. minima hibernate on blueberry leaves on the ground and after germination in late spring, infest the alternate host, Tsuga spp., via basidiospores. Aeciospores are produced and infest Vaccinium and other Ericaceae host plants resulting in the production of urediniospores. The latter ensure disease spread within the crop during the entire growing season. Furthermore, it has been shown that other closely related blueberry rust species are capable of surviving as mycelium in plant buds and directly producing urediniospores in spring, thereby eliminating the need of the alternate host (EPPO, 2016). It is not known if this is the case for T. minima in California where two native host species, Tsuga heterophylla and T. mertensiana can serve as alternate hosts for the pathogen to complete its lifecycle. These two species are also native to the Pacific western states although the fungus has not been recovered from Tsuga (Wiseman et al., 2016; Shands, et al., 2017). The other two hemlocks that are alternate hosts, T. canadensis and T. diversifolia, are not generally cultivated in California but may be present in small areas of private production and nurseries. Pfister et al., 2004, experimentally determined the predicted optimum temperature for urediniospores to be 19.5°C, with a 5% variation in uredinia production between 17.5 and 22°C.
Dispersal and spread: Spores of Thekospora minima are spread over short distances to nearby plants by wind and rain. Spores may also be spread by human contact, clothing, equipment and packaging. Long distance spread occurs mainly through passage of infected plants including fruit to non-infected regions (EPPO, 2016, Tasmania, 2014).
Hosts: The uredinial and telial stages of the pathogen are found on the main hosts in Vaccinium spp., namely, V. angustifolium var. laevifolium (lowbush blueberry), V. corymbosum (highbush blueberry), V. membranaceum (deciduous huckleberry) and V. erythrocarpum (southern mountain cranberry) in the family Ericaceae. Other hosts belong to different genera in the same family: Azalea sp., A. pontica var. daviesii, Gaylussacia sp., G. baccata (black huckleberry), Leucothoe sp., Lyonia nezikii, L. ovalifolia var. elliptica, Menziesia sp., Pernettya sp., Pieris sp., Rhododendron nudiflorum, R. ponticum, and Rhodora canadensis. The aecial stage of the pathogen is found on the alternate host, Tsuga spp., (hemlock; Pinaceae), T. canadensis (eastern hemlock), T. diversifolia (Japanese hemlock), T. heterophylla (western hemlock), T. mertensiana (mountain hemlock) (EPPO, 2016; Farr & Rossman, 2017; Wiseman et al., 2016).
Symptoms: Initial symptoms appear as small yellow, chlorotic leaf spots on upper surfaces of young leaves. As infection progresses these lesions turn rust or brown-colored, enlarge and coalesce covering large areas of a leaf. On the underside of leaves, small flecks surrounded by water-soaked halos develop turning into yellow-orange, powdery pustules containing uredinia with urediniospores. Pustules may also develop on blueberry fruit. In severe infections premature leaf drop and plant defoliation can occur and result in decline in fruit yield and flower production (EPPO, 2016).
Damage Potential: Blueberry rust disease caused by Thekopsora minima may result in plant defoliation and decline in fruit and flower production. Generally, under conditions of high humidity required for rust fungi infection, significant losses in blueberry production and other Ericaceae host plants can be expected. However, in California, such high humidity climates are not anticipated in blueberry cultivated regions and T. minima has not caused significant rust disease in blueberry, even though it has been in the State for over 17 years ((personal communication: Dr. Janet C. Broome, Driscoll’s, 2017). Infected plants do not suffer from leaf drop, which is generally associated with the rust, and the pathogen has not been an issue of concern for blueberry growers to warrant administration of control measures. Some rust disease is apparent on leaves from early spring into summer following periods of significant rain, however, it is difficult to find infected plants later in the season (personal communications: Dr. Janet C. Broome, Driscoll’s, 2017 and Dr. Timothy D. Miles, CSUMB). Similarly, economic damage to other environmental host plants is expected to be minimal as the pathogen has already been in California for several years without any significant increase of its impact.
Worldwide Distribution: Asia: China, Japan; Africa: South Africa; Europe: Netherlands (restricted distribution), Portugal (present, few occurrences); North America: Canada, Mexico, USA; South America: Colombia; Oceania: Australia (New South Wales, Queensland, Victoria) (EPPO, 2016, 2017; Mostert et al., 2010; Zheng et al., 2017).
In Europe, the pathogen is currently regarded as “Transient, under eradication” in Belgium and Germany (EPPO, 2017). In the USA, it has been reported from Delaware, Massachusetts, Michigan, New York and Oregon (EPPO, 2017; Sato et al., 1993; Schilder & Miles, 2011; Wiseman et al., 2016).
Official Control: Thekopsora minima has been on the EPPO Alert List for the European Union since 2016 (EPPO, 2017). Presently, Thekoposora minima is on the ‘Harmful Organism List” for Peru (USDA PCIT, 2017).
California Distribution: Thekopsora minima has officially been detected in Santa Cruz and Ventura Counties. The pathogen has also been reported from Santa Barbara County (Shands et al., 2017).
California Interceptions: Thekopsora minima has only been detected once in a shipment of blueberry plants intercepted in San Francisco in 2017 (see “Initiating Event”).
The risk Thekopsora minima would pose to California is evaluated below.
Consequences of Introduction:
1) Climate/Host Interaction: Main hosts of Thekopsora minima are in the family Ericaceae and include blueberries, rhododendrons and azaleas. Blueberries are grown in northern coastal and southern coastal regions and in the San Joaquin Valley. Rhododendrons, azaleas and other horticultural hosts are grown throughout California particularly in coastal climates. However, because T. minima requires high humidity for infection and development in order to cause significant disease, it would only be likely to establish in very limited areas of the State. The pathogen is already established in several coastal areas, for the past several years, and rust disease appears typically only during early spring to summer following significantly wet periods.
Evaluate if the pest would have suitable hosts and climate to establish in California.
– Low (1) Not likely to establish in California; or likely to establish in very limited areas.
– Medium (2) may be able to establish in a larger but limited part of California.
– High (3) likely to establish a widespread distribution in California.
2) Known Pest Host Range: Thekopsora minima has a moderate host range. Main hosts of the pathogen are in the family Ericaceae and include blueberries, rhododendrons, and azaleas.
Evaluate the host range of the pest.
– Low (1) has a very limited host range.
– Medium (2) has a moderate host range.
– High (3) has a wide host range.
3) Pest Dispersal Potential: Urediniospores are produced in abundance and ensure disease spread within the crop during the entire growing season. Spores are spread over short distances to nearby plants by wind and rain and may also be spread by human contact, clothing, equipment and packaging. Long distance spread occurs mainly through passage of infected plants including fruit to non-infected regions.
Evaluate the natural and artificial dispersal potential of the pest.
– Low (1) does not have high reproductive or dispersal potential.
– Medium (2) has either high reproductive or dispersal potential.
– High (3) has both high reproduction and dispersal potential.
4) Economic Impact: While blueberry rust disease has been reported to cause plant defoliation, this has not been the case in California, even though the fungus has been present in the State for several years. Blueberry growers have noted that some rust disease is apparent on blueberry leaves from early spring into summer following periods of significant rain, however, it is difficult to find infected plants later in the season. Infected plants do not suffer from leaf drop, which is generally associated with the rust, and the pathogen has not been an issue of concern for blueberry growers to warrant administration of control measures. No yield loss due to this rust pathogen in California has been observed or reported (see; ‘Damage Potential’).
Evaluate the economic impact of the pest to California using the criteria below.
Economic Impact: None
A. The pest could lower crop yield.
B. The pest could lower crop value (includes increasing crop production costs).
C. The pest could trigger the loss of markets (includes quarantines).
D. The pest could negatively change normal cultural practices.
E. The pest can vector, or is vectored, by another pestiferous organism.
F. The organism is injurious or poisonous to agriculturally important animals.
G. The organism can interfere with the delivery or supply of water for agricultural uses.
Economic Impact Score: 1
– Low (1) causes 0 or 1 of these impacts.
– Medium (2) causes 2 of these impacts.
– High (3) causes 3 or more of these impacts.
5) Environmental Impact: Although, horticultural and environmental plants, such as azaleas and rhododendrons, are hosts of Thekopsora minima (see: ‘Hosts’), the pathogen has not increased in its spread or impact in cultivated communities over the past several years of its presence in California. Therefore, no significant impact on the environment or home/ornamental plantings is expected.
Evaluate the environmental impact of the pest on California using the criteria below.
Environmental Impact: None
A. The pest could have a significant environmental impact such as lowering biodiversity, disrupting natural communities, or changing ecosystem processes.
B. The pest could directly affect threatened or endangered species.
C. The pest could impact threatened or endangered species by disrupting critical habitats.
D. The pest could trigger additional official or private treatment programs.
E. The pest significantly impacts cultural practices, home/urban gardening or ornamental plantings.
Environmental Impact Score: 1
– Low (1) causes none of the above to occur.
– Medium (2) causes one of the above to occur.
– High (3) causes two or more of the above to occur.
Consequences of Introduction to California for Thekopsora minima: Low (8)
Add up the total score and include it here.
–Low = 5-8 points
-Medium = 9-12 points
-High = 13-15 points
6) Post Entry Distribution and Survey Information: Evaluate the known distribution in California. Only official records identified by a taxonomic expert and supported by voucher specimens deposited in natural history collections should be considered. Pest incursions that have been eradicated, are under eradication, or have been delimited with no further detections should not be included.
Evaluation is Low. Thekopsora minima has officially been detected only in few coastal counties in California.
-Not established (0) Pest never detected in California, or known only from incursions.
–Low (-1) Pest has a localized distribution in California, or is established in one suitable climate/host area (region).
-Medium (-2) Pest is widespread in California but not fully established in the endangered area, or pest established in two contiguous suitable climate/host areas.
-High (-3) Pest has fully established in the endangered area, or pest is reported in more than two contiguous or non-contiguous suitable climate/host areas.
7) The final score is the consequences of introduction score minus the post entry distribution and survey information score: (Score)
Final Score: Score of Consequences of Introduction – Score of Post Entry Distribution and Survey Information = 7
It is not known if the pathogen will infect hemlock (Tsuga spp.) in California, to complete its life cycle. The pathogen was not recovered from hemlock in California and Oregon (Pacific coastal regions). Hemlock species are widespread in California.
Conclusion and Rating Justification:
Based on the evidence provided above the proposed rating for Thekopsora minima is C.
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Schrader, G., and W. Maier. 2015. Express – PRA for Thekopsora minima occurrence. Julius Kühn-Institute, Institute for Plant Health. Translated by Elke Vogt-Amdt. http://pflanzengesundheit.jki.bund.de/dokumente/upload/fee0d_thekopsora-minima_express-pra.pdf
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USDA PCIT. 2017. USDA Phytosanitary Certificate Issuance & Tracking System. Retrieved May 31, 2017. 6:30:49 pm CDT. https://pcit.aphis.usda.gov/PExD/faces/ReportHarmOrgs.jsp.
Wiseman, M. S., M. I. Gordon, M. L. Putnam. 2016. First report of leaf rust caused by Thekopsora minima on Northern highbush blueberry in Oregon. Plant Disease 100: 1949.
Zheng, X., G. Tang, Y. Tian, X. Huang, X. Chang, H. Chen, H. Yang, S. Zhang, and G. Gong. 2017. First report of leaf rust of blueberry caused by Thekopsora minima in China. Plant Disease 101: 835. https://doi.org/10.1094/PDIS-09-16-1379-PDN
John J. Chitambar, Primary Plant Pathologist/Nematologist, California Department of Food and Agriculture, 3294 Meadowview Road, Sacramento, CA 95832. Phone: 916-262-1110, plant.health[@]cdfa.ca.gov.
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Pest Rating: C