Phytophthora quercina T. Jung 1999

California Pest Rating for

Phytophthora quercina T. Jung 1999

Pest Rating: B

PEST RATING PROFILE

Initiating Event:

On April 25, 2016, two soil samples with roots of valley oak (Quercus lobata) trees that showed symptoms of stunting in a restoration site in Santa Clara County, were collected by Santa Clara County Agricultural officials and sent to the CDFA Plant Pathology Laboratory, for diagnosis. DNA was extracted from soil baits and determined to be 100% similar to the pathogen, Phytophthora quercina, by Suzanne Rooney-Latham, CDFA plant pathologist. DNA samples were sent by CDFA to the USDA APHIS PPQ CPHST Laboratory in Beltsville, Maryland, and on June 10, 2016, USDA confirmed the identity of P. quercina. This detection marked the first confirmed presence and new record of the pathogen in the United States (USDA APHIS PPQ, 2016). Currently, P. quercina has a temporary ‘Q’ rating in California. The risk of introduction and establishment of this pathogen in California is assessed and a permanent rating is proposed herein.

History & Status:

Background: Oak decline is a serious and frequently recurring disease in Europe since the beginning of the twentieth century (Jung et al., 1999). During the early 1990s, several Phytophthora spp. including a newly described P. quercina were found to be associated with oak decline and root rot in central and southern Europe. In pathogenicity tests on oak, Quercus robur, P. quercina was found to be most pathogenic in comparison to the other associated Phytophthora species (Jung et al., 1999). Subsequent reports associated P. quercina with oak decline from Turkey, Austria, and Italy (Balcý & Halmschlager, 2002a, 2002b; Vettraino et al., 2002). Phytophthora quercina is an oomycete, and Cooke et al, (1999) provided molecular evidence that verified P. quercina as a distinct species.

Phytophthora quercina was recently detected in soil samples obtained from the root zone area of diseased valley oak trees grown at a California restoration site. The USDA marked this detection as the first known confirmation of the pathogen in the United States. Details are given above in “Initiating Event”. The species was reported in 2007 on being detected in a soil bait around a declining oak tree in Central Missouri (Schwingle et al., 2007), however, the identification was not confirmed by USDA APHIS and there have not been any further publications on the species in the USA (USDA APHIS PPQ, 2016).

Hosts: Quercus spp. (oak): Q. cerris, Q. hartwissiana, Q. frainetto, Q. ilex, Q. robur, Q. petraea, Q. pubescens, Q. suber, and Q. vulcanica (Balcý & Halmschlager, 2002a, 2002b; EPPO, 2016; Farr & Rossman, 2016; NPRG, 2010).

Symptoms: Phytophthora quercina, along with several other Phytophthora species, occur in oak decline stands in Europe (Balcý & Halmschlager, 2002; Jung et al., 2008). Above ground symptoms of oak decline include dieback of branches and parts of the crown, formation of epicormic shoots, high transparency of the crown, yellowing and wilting of leaves and tarry exudates from the bark. These symptoms are indicative of water stress and poor nutrition (Jung et al., 2008). Below ground symptoms in declining European oak species resulted in deterioration of oak fine roots, including a progressive destruction of the fine root system, dieback of long roots, and necrotic lesions on suberized and non-suberized roots. Although these symptoms occur in both healthy and declining oaks, the damage is generally more severe in declining oaks (Jung, et al., 2008). The pathogen also causes abnormal root branching, and produces elicitins, viz. toxic substances that induce wilting and yellowing and leaf necrosis in declining oaks (NPRG, 2010). In pathogenicity test, P. quercina-infected Quercus robur (oak) seedlings with severe root rot showed wilting and necrosis of leaves, root necrosis and dieback of the shoot. Under natural conditions, mature Q. robur trees showed reductions in fine root length (Jung et al., 1999).

Damage Potential: The extent of damage caused by Phytophthora quercina has not been reported. Several Phytophthora species including P. quercina are associated with oak decline disease. However, P. quercina has been shown to be pathogenic to some European Quercus species, such as Q. robur (Jung et al., 1999), and to be one of the most aggressive and most common species found in reported surveys in Europe (Jung et al., 1999, 2008; Balcý and Halmschlager 2002a, 2002b). In Italy, P. quercina was the only species significantly associated with declining oak trees (Vettraino et al., 2002).

Disease Cycle: Although present in roots and rhizosphere soil of oaks exhibiting symptoms of oak decline, the precise role of Phytophthora quercina in this disease is not known and very little is known about its biology. Jung et al. (2008), reported that at least two different complex diseases are referred to as ‘oak decline’. On sites with a mean soil pH 3.5 or greater and sandy-loam to clayey soil texture, Phytophthora species were commonly isolated from rhizosphere soil, and highly significant correlations existed between crown transparency and various root parameters. However, in sites with a mean soil pH less than 3.9 and sandy to sandy-loam soils, Phytophthora species were not found. Biotic and abiotic stress factors such as drought and frost, may often act synergistically and accelerate Phytophthora-mediated decline of oaks.

Generally, species of Phytophthora that cause root and stem rots survive cold winters or hot and dry summers as thick-walled, resting spores (oospores and chlamydospores) or mycelium in infected roots, stems or soil. During spring, the oospores and chlamydospores germinate to produce motile spores (zoospores) that swim around in soil water and roots of susceptible hosts. The pathogen infects the host at the soil line causing water soaking and darkening of the trunk bark. This infected area enlarges and may encircle the entire stem of small plants which wilt and eventually die. On large plants, the infected, necrotic area may be on one side of the stem and become a depressed canker below the level of the healthy bark. Collar rot canker may spread down the root system. Roots are invaded at the crown area or at ground level. Mycelium and zoospores grow in abundance in cool, wet weather causing damage where the soil is too wet for normal growth of susceptible plants and low temperatures (15-23°C) prevail (Agrios, 2005). Phytophthora quercina is homothallic. Optimum growth in culture is at 20°C and 25°C, however, it is able to grow at temperatures as high as 27.5°C (Jung et al., 1999; Barzanti et al., 2001).

Transmission: Like most Phytophthora species, P. quercina is soil-borne and water-borne and may be spread to non-infected sites through infected plants, nursery and planting stock, and seedlings, soil, run-off and splash irrigation and rain water, and contaminated cultivation equipment, tools, and boots.

Worldwide Distribution: Asia: Turkey; Europe: Austria, Belgium, France, Germany, Hungary, Italy, Luxemberg, Montenegro, Serbia, Spain, Sweden, Scotland, United Kingdom: North America: USA (California) (Balcý & Halmschlager, 2002a, 2002b; EPPO, 2016; Farr & Rossman, 2016; Jung et al., 1999; NPRG, 2010).

Official Control: Phytophthora quercina is listed as an exotic forest pathogen in USDA APHIS PPQ Federal New Pest Response Guidelines for Phytophthora species (NPRG, 2010). The species has been on the North American Plant Protection Organization (NAPPO) alert list since 2002. Currently, P. quercina has a temporary ‘Q’ rating in California.

California Distribution: Phytophthora quercina has been detected in a California native plant restoration site in a Santa Clara County.

California Interceptions: None.

The risk that Phytophthora quercina would pose to California is evaluated below.

Consequences of Introduction:

1) Climate/Host Interaction: Evaluate and score the pest for suitability of hosts and climate to establish in California. Score:

– 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.

Risk is High (3) – Although Phytophthora quercina has been reported to be associated primarily with European oak species in Europe, its recent detection in valley oak rhizosphere soil extends the capability of this pathogen to be associated with California native oaks. Valley oak is endemic to California and present throughout the State. Thereby, making it likely for the pathogen to establish a widespread distribution in California. It is not yet known, but probable that other California native oaks may be affected by P. quercina.

2) Pest Host Range: Evaluate and score the pest as it pertains to host range. Score:

– Low (1) has a very limited host range

– Medium (2) has a moderate host range

– High (3) has a wide host range

Risk is Low (1) – Phytophthora quercina has a host range limited to Quercus spp. that includes Q. cerris, Q. hartwissiana, Q. frainetto, Q. ilex, Q. robur, Q. petraea, Q. pubescens, Q. suber, and Q. vulcanica. In California, it was found to be associated with Q. lobata.

3) Pest Dispersal Potential: Evaluate and score the pest for dispersal potential using these criteria. Score:

– 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.

Risk is High (3) – Phytophthora quercina is soil-borne and water-borne and therefore, primarily spread artificially via infested soils, plants, nursery and planting stock, seedlings, run-off and splash irrigation water, cultivation equipment and tools, and boots that may spread contaminated soil and plant materials to non-infected sites.

4) Economic Impact: Evaluate the economic impact of the pest to California using the criteria below. Score:

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.

– 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.

Risk is Medium (2) – The extent of damage caused by Phytophthora quercina has not been reported. Several Phytophthora species including P. quercina are associated with oak decline disease. In Europe, P. quercina was most commonly associated with the disease than were other Phytophthora species. The pathogen could impact nursery-produced oaks thereby triggering possible loss of markets and requiring changes in normal cultural practices to avoid spread of the soil and water-borne pathogen.

5) Environmental Impact: Evaluate the environmental impact of the pest on California using the criteria below. Score:

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 could significantly impact cultural practices, home/urban gardening or ornamental plantings.

Score the pest for Environmental Impact:

– 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

Risk is High (3) – Phytophthora quercina is listed as an exotic forest pathogen in USDA APHIS PPQ Federal New Pest Response Guidelines for Phytophthora species (NPRG, 2010). The species has been on the North American Plant Protection Organization (NAPPO) alert list since 2002. Although the extent of damage potentially caused by this pathogen is not yet known, its spread within California could cause serious impact on native oaks, disrupt critical habitats by killing critical species necessary for species diversity and soil stability, necessitate official or private treatment programs to preserve critical, rare, or endangered species, and significantly impact cultural practices, home/urban and/or ornamental plantings.

**Consequences of Introduction to California for Phytophthora quercina:**

Add up the total score and include it here

Low = 5-8 points

Medium = 9-12 points

High = 13-17 points

Total points obtained on evaluation of consequences of introduction of Phytophthora quercina to California = (12).

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. (Score)

-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.

Evaluation is Low (-1).

Final Score

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 = 11.

Uncertainties:

The extent of economic damage caused by Phytophthora quercina is not known. Also not known is the exact role of the pathogen in oak decline disease, and details of the biology of the pathogen species.

Conclusion and Rating Justification:

Based on the evidence provided above the proposed rating for Phytophthora quercina is B.

References:

Agrios, G. N. 2005. Plant Pathology fifth edition. Elsevier Academic Press, Massachusetts, USA. 922 p.

Balcý, Y. and E. Halmschlager. 2002a. First confirmation of Phytophthora quercina on oaks in Asia. Plant Disease 86:442. http://dx.doi.org/10.1094/PDIS.2002.86.4.442C

Balcý, Y. and E. Halmschlager. 2002b. First report of Phytophthora quercina in Austria. New Disease Reports volume 6, August 2002-January 2003. http://www.bspp.org.uk/ndr/jan2003/2002-28.htm

Barzanti, G. P., P. Capretti, and A. Ragazzi. 2001. Characteristics of some Phytophthora

species isolated from oak forest soils in central and northern Italy.

Phytopathologia Mediterranea 40(2): 149-156.

Cooke, D.E.L., T. Jung, N. A. Williams, R. Schubert, G. Bahnweg, W. Oswald, and J. M. Duncan. 1999. Molecular evidence supports Phytophthora quercina as a distinct species. Mycological Research, 103:799-804.

EPPO. 2016. Phytophthora quercina (PHYTQU). New PQR database. Paris, France: European and Mediterranean Plant Protection Organization. http://newpqr.eppo.int

Farr, D.F., & A. Y. Rossman. Fungal Databases, Systematic Mycology and Microbiology Laboratory, ARS, USDA. Retrieved January 28, 2016, from http://nt.ars-grin.gov/fungaldatabases/

Jung, T., D. E. L. Cooke, H. Blaschke, J. M. Duncan, and W. Oswald. 1999. Phytophthora quercina sp. nov., causing root rot of European oaks. Mycol. Res. 103: 785-798.

Jung, T., H. Blaschke and W. Oßwald. 2008. Involvement of soilborne Phytophthora species in Central European oak decline and the effect of site factors on the disease. Plant Pathology, 49:706-718. DOI: 10.1046/j.1365-3059.2000.00521.x

Schwingle, B. W., J. Juzqik, J. Eggers, and B. Moltzan. 2007. Phytophthora species in soils associated with declining and nondeclining oaks in Missouri Forests. Plant Disease 91:633. http://apsjournals.apsnet.org/doi/abs/10.1094/PDIS-91-5-0633A

NPRG. 2010. New Pest Response Guidelines: Phytophthora species in the Environment and Nursery Settings. USDA MRP APHIS PPQ Cooperating State Departments of Agriculture, July 09 2010. 229 pages.

USDA APHIS PPQ. 2016. Email from J. H. Bowers, National Survey Coordinator National Policy Manager, Cooperative Agricultural Pest Survey, USDA, APHIS, PPQ, PHP, to Nick Condos, Director, CDFA, sent Friday, June 10, 2016, 11:56 am.

Vetrraino, A. M., G. P. Barzanti, M. C. Bianco, A. Ragazzi, P. Capretti, E. Paoletti, N. Luisi, N. Anselmi, and A. Vannini. 2002. Occurrence of Phytophthora species in oak stands in Italy and their association with declining oak trees. Forest Pathology, 32:19-28. DOI: 10.1046/j.1439-0329.2002.00264.x

Responsible Party:

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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