Phytophthora tentaculata Kröber & Marwitz 1993

California Pest Rating Proposal for

Phytophthora tentaculata Kröber & Marwitz 1993

Pest Rating: B

PEST RATING PROFILE

Initiating Event:

During January 2016, samples of two diseased Diplacus hybrids (monkey flower hybrid varieties) and one of diseased Artemisia palmeri (Palmer sagewort) were collected by Kathleen Kosta, CDFA, from a nursery in Santa Clara County. The samples were processed and analyzed at the CDFA Plant Pathology Laboratory and Phytophthora tentaculata was tentatively identified as the associated pathogen by Suzanne Rooney-Latham, CDFA plant pathologist. The identity of the pathogen was later confirmed by the USDA APHIS PPQ CPHST Laboratory in Beltsville, Maryland. The three afore mentioned plant varieties are new hosts records for P. tentaculata. Several detections of this pathogen have been made in California during the past few years. Therefore, the current rating for P. tentaculata is reassessed here.

History & Status:

Background: In 1993, Phytophthora tentaculata was first isolated from roots and stems of greenhouse-grown Argyranthemum frutescens (syn. Chrysanthemum frutescens), Leucanthemum vulgare (syn. C. leucanthemum), Delphinium ajacis, and Verbena sp. in nurseries in the Netherlands and Germany in 1993 (Kröber & Marwitz, 1993). Later, the pathogen was also reported from Spain (Moralejo et al., 2004; Álvarez et al., 2006), Italy (Cristinzio et al., 2006; Martini et al., 2009) and China (Meng & Wang, 2006; Wang and Zhao, 2014) after detection in nursery-potted and field-grown plants. In 2012, P. tentaculata was first detected in North America, in sticky monkey flower, Diplacus aurantiacus (syn. Mimulus aurantiacus) growing in a native plant nursery in Monterey County, California. Plant samples collected by Monterey County and CDFA staff were submitted to CDFA for analysis and the pathogen P. tentaculata was identified by Suzanne Rooney-Latham and Cheryl Blomquist, CDFA plant pathologists (Rooney-Latham & Blomquist, 2014), and later confirmed by the USDA APHIS National Identification Services. The source of the Diplacus (Mimulus) plants was traced back to plants that were grown from seed and cuttings from a historical site in Monterey County. No Diplacus (Mimulus) plants had been shipped from the native plant nursery prior to the initial detection. Consequently, all positive Diplacus (Mimulus) plants and materials were destroyed. The California detection marked the first detection on a native host, albeit in a native plant restoration nursery and a host that has a wide geographical native range in California. Since its initial Monterey County find, P. tentaculata has also been detected in native plant nurseries in Placer, Butte, Santa Cruz, San Mateo, Orange, and Santa Clara Counties, and in out-planted nursery stock in habitat restoration sites in Alameda, Monterey, and Santa Clara Counties. The pathogen was detected and reported from several new hosts that are listed below (see ‘Hosts’) and include Artemisia douglasiana, A. californica, A. dranunculus, A. palmeri, Diplacus x “Apricot”, Diplacus x “Red brick”, Monardella villosa, and Salvia sp. Several of these detections were made during a 2014-2015 survey of California native plant nurseries and restoration sites conducted by the collaborative efforts of CDFA, USDA and a private research company. The survey resulted in the detection of P. tentaculata in 8 out of 16 counties. The origin of P. tentaculata is unknown. Presently in California, Phytophthora tentaculata has only been detected in nursery-grown plants that were out-planted in the environment. The pathogen has persisted on those plants in the field for at least 4.5 years. Therefore, it is likely that in California, the pathway of pathogen spread is from infected nurseries to restoration field sites, and that the pathogen has been spread between and within nurseries by the use of infested pots and plants (Rooney-Latham, et al., 2015).

Hosts: The currently known hosts are included in the plant families Asteraceae, Lamiaceae, Phrymaceae, Ranunculaceae, Rhamnaceae, Rosaceae, and Verbenaceae. The host range includes the following plants, diseases and geographical locations:

Apium graveolens (celery); stem and root rot; China (Wang & Zhao, 2014).

Argyranthemum frutescens (syn. Chrysanthemum frutescens) (marguerite daisy); root and stem base rot; Germany & the Netherlands; Root, collar & stalk rot (Kröber & Marwitz 1993).

Artemisia douglasiana (California mugwort); root rot; California, USA (Rooney-Latham, et al., 2015).

Artemisia dracunculus (tarragon); root rot; California, USA (Rooney-Latham et al., 2015). Artemisia californica (California sagebrush); root rot; California, USA (Rooney-Latham et al., 2015).

Artemesia palmeri (Palmer sagewort); root rot; California, USA (see “Initiating Event”).

Aucklandia lappa (rhizomatous medicinal herb); China; stalk rot & wilt (Meng & Wang 2008).

Calendula arvensis (field marigold) (Li et al., 2011).

Ceanothus cuneatus (buckbrush); root rot; California, USA (Rooney-Latham et al., 2015).

Cichorium intybus (chicory, endive); Italy; collar and root rot (Garibaldi et al. 2006).

Delphinium ajacis (nursery stock); Germany & the Netherlands; root, collar & stalk rot (Kröber & Marwitz 1993).

Diplacus aurantiacus (syn Mimulus aurantiacus) (sticky monkey-flower); California, USA. root and collar rot (Rooney-Latham & Blomquist, 2014).

Diplacus x “Apricot” (Diplacus hybrid variety); root and collar rot; California, USA (see “Initiating Event”).

Diplacus x “Red brick” (Diplacus hybrid variety); root and collar rot; California, USA (see “Initiating Event”).

Frangula californica (syn. Rhamnus californica) (coffeeberry); California; root and collar rot (Frankel et al., 2015; NPAG, 2014).

Gerbera jamesonii (African daisy); Italy; Crown & stem rot (Cristinzio et al. 2006).

Heteromeles arbutifolia (toyon) California, USA (Frankel et al., 2015; NPAG, 2014).

Leucanthemum vulgare (syn. Chrysanthemum leucanthemum) Germany & the Netherlands; Root, collar & stalk rot (Kröber & Marwitz 1993).

Monardella villosa (coyote mint); California, USA (Rooney-Latham et al., 2015).

Origanum vulgare (oregano); Italy. Leaf russeting & chlorosis, wilt, defoliation, twig dieback,basal stem rot, root rot, entire plant collapse (Martini et al. 2009).

Salvia spp. (sage) California, USA (Frankel et al., 2015; NPAG, 2014).

Santolina chamaecyparissus (lavender cotton); Spain; Root rot (Alvarez et al. 2004).

Verbena sp. (nursery stock); Germany, Netherlands; nursery potted plant in Spain; root, collar & stalk rot (Moralejo et al. 2004).

Symptoms: Depending on the host species, Phytophthora tentaculata causes moderate to severe root and crown rot, and death in highly infected plants. The symptoms are not unique to P. tentaculata by similar to infections caused by other Phytophthora species, root and stem pathogens and drought. According to Rooney-Latham et al (2015) symptoms can vary in field-planted nursery stock. Infected sticky monkey flower plants are stunted, with dull yellowish leaves that turn red as the disease progresses. Roots and stem collars have necrotic, sunken lesions with few feeder roots and discolored leaves. In some cases, plants may exhibit poor growth and eventually collapse within their first season, while some plants may grow for a year or more before exhibiting severe dieback during hot summers. Transplanted infected Artemisia douglasiana plants did not show dieback, but exhibited stunting and chlorosis more that 4.5 years after being out-planted (Rooney-Latham et al., 2015; Frankel et al., 2015; Kröber & Marwitz 1993).

Damage Potential: Phytophthora tentaculata causes moderate to severe root and crown rot on woody and semi-woody hosts. Introduction of P. tentaculata-infected native plants to restoration sites could negatively impact native plants in their natural environment.

Disease Cycle: 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). Little information is known about the life cycle or biology of Phytophthora tentaculata other than what was provided by the original species description by Kröber and Marwitz. The temperature range of the pathogen is 7°C to 32°C, the optimum temperature being 15°C to 25°C.

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

Worldwide Distribution: Asia: China; Europe: Italy, Germany, the Netherlands, Spain; North America: USA (California).

Official Control: USDA lists Phytophthora tentaculata in the top 5 Phytophthora species of concern and threat to nurseries and forests in Federal New Pest Response Guidelines (USDA APHIS, 2010). USDA APHIS New Pest Advisory Group determined that P. tentatculata is “actionable and reportable.

California Distribution: Phytophthora tentaculata has been detected in native plant nurseries in Monterey, Placer, Butte, Santa Cruz, San Mateo, Orange, and Santa Clara Counties, and in out-planted nursery stock in habitat restoration sites in Alameda, Monterey, and Santa Clara Counties.

California Interceptions: None.

The risk that Phytophthora tentaculata 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) – To date, Phytophthora tentaculata has been detected in native plant nurseries in eight counties and in habitat restoration sites (in out-planted nursery stock) in three of those eight counties. Several native plant hosts are widespread in California. Since the pathogen is known to attack many plants in the nursery trade, it is possible that the pathogen could appear and survive wherever nurseries, including native plant nurseries, are present in California. Therefore, there is the potential for this pathogen to establish a widespread distribution in California.

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 Medium (2) – Presently, 23 plant hosts belonging to 7 families have been reported. Of these, almost half the number of hosts have been reported from California, and are native to the State. While several new hosts have been reported after the initial detection of the pathogen in Monterey County, based on the present known host range, the risk of the pathogen is evaluated as medium.

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 tentaculata 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 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 High (3) – The presence of Phytophthora tentaculata could cause severe economic impacts in nursery trade, impacting a number of nursery-produced native and ornamental plants that are commonly used in California landscapes as well as some of which play a significant role in the State’s florist trade. In addition to lowered crop yields and lowered crop values due to increased need for protective treatments, the management of infestations of a soil- and water-borne pathogen such as Phytophthora spp. in a commercial nursery may be a laborious and expensive problem that would involve alterations in the normal cultural practices such as choice of sites to grow susceptible hosts, and water and growth medium management practices to ensure pathogen propagule-free irrigation water and growth media.

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) – The USDA APHIS lists Phytophthora tentaculata in the top 5 Phytophthora species of concern and threat to nurseries and forests in Federal New Pest Response Guidelines (USDA APHIS, 2010). The presence of P. tentaculata could cause serious impact on native plants, threatened or endangered species, 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 tentaculata:**

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 tentaculata to California = (14).

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 Medium (-2). To date, Phytophthora tentaculata has been detected in native plant nurseries in Monterey, Placer, Butte, Santa Cruz, San Mateo, Orange, and Santa Clara Counties, and in out-planted nursery stock in habitat restoration sites in Alameda, Monterey, and Santa Clara Counties in California.

Final Score:

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 = 12.

Uncertainties:

While more is known about the presence of Phythophthora tentaculata in California since its original detection in Monterey County, more researched information is needed on the distribution, behavior and threat of Phytophthora tentaculata in California’s natural soils and plant communities under diverse climatic environments.

Conclusion and Rating Justification:

Based on the evidence provided above the proposed rating for Phytophthora tentaculata remains B.

References:

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

Álvarez, L. A., A. Pérez-Sierra, M. León, J. Armengol, and J. García-Jiménez. 2006. Lavender cotton root rot: a new host of Phytophthora tentaculata found in Spain. Plant Disease 90:523. http://dx.doi.org/10.1094/pd-90-0523A

Cristinzio, G., I. Camele and C. Marcone. 2006. Phytophthora tentaculata su gerbera in Italia. First report of Phytophthora tentaculata on gerbera in Italy. Informatore Fitopatologico 56:23-25. http://www.cabdirect.org/abstracts/20063066005.html;jsessionid=C23F9F14D93FF641EEE94948EFEB99D5.

Frankel, S., S. Rooney-Latham, C. L. Blomquist, and E. Bernhardt. 2015. Pest Alert: Phytophthora tentaculata. Technical Report, February 2015, United States Department of Agriculture. http://www.suddenoakdeath.org/wp-content/uploads/2015/02/P.tentaculata.

Garibaldi A., G. Gilardi, M. L. Gullino. 2010. First report of collar and root rot caused by Phytophthora tentaculata on witloof chicory (Cichorium intybus) in Italy. Plant Disease 94:1504.

Kröber, H., and R. Marwitz. 1993. Phytophthora tentaculata sp. nov. und Phytophthora cinnamomi var. parvispora var. nov., zwei neue Pilze von Zierpflanzen in Deutschland. Zeitschrift fur Pflanzenkrankheiten und Pflanzenschutz 100, 250-258. [Original Description]

Martini, P., A. Pane, F. Raudino, A. Chimento, S. Scibetta, and S. O. Cacciola. 2009. First report of Phytophthora tentaculata causing root and stem rot of oregano in Italy. 93:843. http://dx.doi.org/10.1094/PDIS-93-8-0843B.

Meng, J., and Y. C. Wang. 2008. First Report of Stalk Rot Caused by Phytophthora tentaculata on Aucklandia lappa in China. Plant Disease 92 (9): 1365.

doi:10.1094/PDIS-92-9-1365B. http://apsjournals.apsnet.org/doi/abs/10.1094/PDIS-92-9-1365B.

Moralejo, E., M. Puig, and W. A. Man in’t Veld. 2004. First report of Phytophthora tentaculata on Verbena sp. in Spain. The British Society for Plant Pathology.

http://www.bspp.org.uk/publications/new-disease-reports/ndr.php?id=009038. May 31, 2009.

USDA APHIS. 2010. New Pest Response Guidelines: Phytophthora species in the Environment and Nursery Settings. 229 pages.

Rooney-Latham, S., and C. L. Blomquist. 2014. First report of root and stem rot caused by Phytophthora tentaculata on Mimulus aurantiacus in North America. Plant Disease 98(7):996.

Rooney-Latham, S., C. L. Blomquist, T. Swiecki, and E. Bernhardt. 2015. Phytophthora tentaculata. Forest Phytophthoras 5(1): doi:10.5399/osu/fp.5.1.3727.

Schwartzburg, K., H. Hartzog, C. Landry, J. Rogers, and B. Randall-Schadel. 2009. Prioritization of Phytophthora of Concern to the United States. USDA APHIS PPQ CPHST PERAL (Plant Epidemiology and Risk Analysis Laboratory), Raleigh, NC. 61 pages.

Wang, T. and W. Zhao. 2014. First report of Phytophthora tentaculata causing stem and root rot on celery in China. http://dx.doi.org/10.1094/PDIS-06-13-0592-PDN.

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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