PHYTOPHTHORA QUERCETORUM Y. BALCI & S. BALCI 2008

Comments from Janice Alexander
From: Phytophthoras in Native Habitats Work Group, http://www.calphytos.org,
Subject: Comments on California Pest Rating Proposal for Phytophthora quercetorum
The Phytophthoras in Native Habitats Work Group is pleased that the CDFA is assessing the pest risk ratings of several Phytophthora species; we appreciate the opportunity to comment as proposed ratings become available. Here we comment on the posted California Pest Rating Proposal for Phytophthora quercetorum which is proposed for a “C” rating.
We see the “C” rating as problematic for this organism. We suggest it be assigned a “B” rating. A “C”-rating is for “pests of the agricultural industry or environment which score medium to low and are of common occurrence and generally distributed in California. Authorized mitigating regulatory actions: Plants and plant products found infested or infected with or exposed to a “C”-rated pest are not subject to any State enforced regulatory actions listed under subsection 3162(e)” (CHAPTER 5B-3 PLANT QUARANTINE).
A “C” rating is inappropriate for P. quercetorum because:
1) Its distribution is not fully understood, there are few reports in California, and it is not known to be generally distributed in the state.

Response: It is in the nursery trades, not under quarantine action, and there are detections in the Bay Area, Sacramento and Fresno, plus in Southern California in Los Angeles and Orange Counties

2) Its impact to restoration activities, rare plants, wildland and nurseries is most likely not medium to low.
Response: there are not many published reports of plant damage. Most detections have been made by baiting and from plants that are co-infected with other pathogens.
A “B” rating would be beneficial to plant health in California because it would allow response action at the discretion of the County Agricultural Commissioner. It would not be onerous, as it would not require action.
In the risk rating proposal, the distribution and known hosts for P. quercetorum are limited. We are concerned since the organism has been found on several oak (Quercus) species that are important components of California ecosystems (e.g., Q. agrifolia, Q. wislizeni). P. quercetorum has been found in several restoration and horticultural nurseries and in soil associated with Q. agrifolia. Balci and others (2008) found some damage to eastern oak species after inoculation with P. quercetorum.
Restoration activities present a direct pathway for Phytophthora and other pathogen introductions into habitat of very high conservation value (Frankel and others 2020a, 2020b). A “B” rating would allow for consideration of response action but not require it; It would provide some protection to California’s biodiversity and ecological resources. To sustain the health of California wildlands and conservation investments, a “B” rating for P. quercetorum is needed.
Thank you for considering these points. Please let us know if we may be of further assistance. For more information on Phytophthoras in California native plant nurseries and restoration sites, see http://www.calphytos.org, or contact Janice Alexander, UC Cooperative Extension, Marin Co. We look forward to continuing to work with you to sustain plant health for California.
References
Balci, Y., Balci, S., MacDonald, W. L., & Gottschalk, K. W. 2008. Relative susceptibility of oaks to seven species of Phytophthora isolated from oak forest soils. Forest Pathology, 38(6), 394-409.
Frankel, S. J.; Alexander, J.; Benner, D.;Hillman, J. and Shor, A. 2020a. Phytophthora pathogens threaten rare habitats and conservation plantings. Sibbaldia: the International Journal of Botanic Garden Horticulture, (18): 53-65.
Frankel, S.J.; Conforti, C.; Hillman, J.; Ingolia, M.; Shor, A.; Benner, B. Alexander, J.A.; Bernhardt, E.; and Swiecki, T.J. 2020b. Phytophthora Pathogen Introductions in California Restoration areas: Protecting California Native Flora from Human-assisted Pathogen Spread. Forests. 11: 1291. doi: 10.3390/f11121291.

Response: Thank you for your comments and for the additional references.

Comments from Pierluigi (Enrico) Bonello
Dear Dr. Scheck,
I tried to leave a comment on the pest rating proposal for Phytophthora quercetorum but could not find a way to register on the site, so I am sending you my comment this way. I hope it is OK.
Although I am based in Ohio I have done a lot of research on the coast live oak-P. ramorum interaction in California (you can check my publications list on my website), so I am well informed on the risks posed by Phytophthoras in CA forests. For this reason I find the proposed rating highly perplexing. Why is it just a C rating? Especially in the face of rather high rankings on most of the objective measures CDFA itself reports? The fact that we do not have as much info about P quercetorum as we do for e.g. P ramorum should not be sufficient reason to give it a low rating. This outome may result in highly problematic delays in dealing with a potentially highly destructive pathogen.
I hope CDFA will consider giving it a rating of at least B.
Thank you for listening.
Pierluigi (Enrico) Bonello
Professor
College of Food, Agricultural, and Environmental Sciences Plant Pathology
201 Kottman Hall, 2021 Coffey Road, Columbus, OH 43210
614-688-5401 Office / 614-292-4455 Fax
bonello.2@osu.edu / https://plantpath.osu.edu/our-people/pierluigi-enrico-bonello
Pronouns: he/him/his

Response: Thank you for your comments

Comments From: Elizabeth Bernhardt, Ph. D. and Tedmund Swiecki, Ph.D.
Re: Review of: California Pest Rating Proposal for Phytophthora quercetorum Y. Balci & S. Balci 2008, dated 11.20.20
We offer the following comments for your consideration as you finalize the pest rating proposal.
Initiating Event: We think many of the finds of P. quercetorum referred to in this paragraph are from us. For clarity, we list the isolations of P. quercetorum in our database that were submitted to CDFA. All our recoveries of P. quercetorum are from nursery origin plants.
PDR number Our isolate number Host Site/County Notes
MVAP06098963 TS140224-QA1a Quercus agrifolia Nursery/Sacramento Abundant sporulation seen on rotted roots growing out of treepot container, direct isolation, submitted to CDFA for identification.
MV6P06458940 PR150923-SY-S1 Quercus agrifolia Transplant in landscape/ Alameda DBH ~ 40 cm, top appears healthy relative to neighbors, large bleeding canker lower bole, detected by pear baiting of roots/soil. Direct isolation from canker margin onto PARP was negative.
MV6P06578761 PR170810-A5-1 Quercus wislizeni Nursery/ Fresno Pear baiting of leachate test of 24 treepots (4×14″), plants variable, with stunting, 2 with recent dead tops
MV6P06578761 PR170810-A7-4 Quercus agrifolia Nursery/ Fresno Pear baiting of leachate test of 24 treepots (4×14″), tall plants, a few stunted, 2 dead
MV6P06578793 PR20190822-AS4- 2-45-QUAG ’12-2A Quercus agrifolia Transplant in restoration site/ Alameda Tree about 3 m tall, split leader, each about 2.5 cm DBH. Sparse and dwarfed relative to other ungirdled neighbors, leaves on plant are rather small, detected by pear baiting of roots/soil
Also collected and submitted to CDFA directly by a client:
MVAP06099050 SF140527-QA01 Quercus agrifolia Transplant in restoration site/ Alameda Tall seedling that has been dead for a while; plant is at least 2 yrs old, CDFA detected by baiting roots with oregano leaves

Response: thank you for the clarification on the Q. agrifolia sample (not from San Francisco Co), I have corrected the document.

History & Status:
Background:
Hosts: Add Rosa californica (Rosaceae) from
Bourret, T.B. Efforts to detect exotic Phytophthora species reveal unexpected diversity. Chapter 2. Restoration outplantings of nursery‐origin Californian flora are heavily infested with Phytophthora. Ph.D. Thesis. University of California, Davis, CA. ProQuest Dissertations Publishing. 2018, 10746957.

Response: thank you for the reference, I have added Rosa californica to the host list.

The fact that oregano leaves and rhododendron leaves have been used to successfully bait P. quercetorum from infected oak roots suggests that these plants and possibly other plants in these families (Lamiaceae, Ericaceae) could also be hosts. Young wounded leaves of Rhododendron maxima developed lesions after artificial inoculation with P. quercetorum on agar plugs as described in:
Balci, Y., Balci, S., MacDonald, W. L., & Gottschalk, K. W. 2008. Foliar susceptibility of Eastern oak species to Phytophthora infection. Forest Pathology, 38(6), 394-409.
Symptoms
The description of disease starting with a canker at the soil line has disease progression backwards. Based on literature noted below, P. quercetorum is typical of many other root-rotting Phytophthora species in that infections are normally initiated on roots and progress upward, sometimes causing basal cankers.
The original description states “P. quercetorum was associated with oak roots and never isolated from aboveground portions of oak”.
Balci, Y., Balci, S., Blair, J.E., Park, S.Y., Kang, S. and Macdonald, W.L., 2008. Phytophthora quercetorum sp. nov., a novel species isolated from eastern and north- central USA oak forest soils. Mycological Research, 112(8), pp.906-916.
No bleeding Phytophthora cankers were reported on any of the trees at the sampling sites in:
McConnell, M.E. and Balci, Y., 2014. Phytophthora cinnamomi as a contributor to white oak decline in mid-Atlantic United States forests. Plant disease, 98(3), pp.319- 327.
which lists recoveries of P. quercetorum from Acer rubrum and Quercus alba.
A clear example of how root rots initiate cankers that can advance up the taproot to the lower stem is shown in Figure 1 in:
Balci, Y., Balci, S., MacDonald, W. L., & Gottschalk, K. W. 2008. Relative susceptibility of oaks to seven species of Phytophthora isolated from oak forest soils. Forest Pathology, 38(6), 394-409.
P. quercetorum is among the species tested in this report.
Based on the literature, it appears P. quercetorum causes fine root rot and can infect taproots of one year old seedlings of various oak species (Balci et al. 2008 Forest Pathology), indicating it is not restricted to fine roots. When enough roots are infected there may be enough inoculum present to initiate cankers at the soil line under flooded conditions, which was perhaps the case for MV6P06458940. No basal canker was associated with infection of MV6P06578793.
The last sentence in this paragraph, related to temperature, in which Agrios is cited, should be replaced by information specific to this species. In the species description paper, Balci et al. Fig.7 (2008 Mycological Research) shows that P. quercetorum grew optimally on media from about 22.5 to 27.5 C, with a minimum growth temperature between 5 and 10 C and a maximum between 30 to 32.5 C, showing that it has wide adaptability to a range of temperatures. Balci et al. 2008 (the Forest Pathology paper) conducted pathogenicity tests in summer and winter in West Virginia. There was no consistent seasonal difference in taproot infections for P. quercetorum across the 6 oak species evaluated (Table 4 in Balci et al. 2008 Forest Pathology).

Response: thank you for those citations, I have amended this section.

California distribution:
If the record for occurrence in San Francisco comes from MV6P06458940, that would be an error. Although the tree owner had a San Francisco address, the tree itself was located in Alameda County.
The record of P. quercetorum on Rosa californica from Bourret 2018 is from Santa Clara County, which should be added to the California distribution.

Response: I have made the county correction and added R. californica and Santa Clara County

Based on the association of this pathogen with nursery stock and the lack of any concerted effort to detect it, it is likely that the CA distribution is wider than these few detections indicate.
As a side note, P. quercetorum seems to be difficult to detect. Balci et al. 2018 Forest Pathology indicate they had difficulty reisolating it from necrotic lesions on stems that resulted from artificial inoculation. Often multiple attempts had to be made before a successful isolation. We found that higher zoospore concentrations of P. quercetorum were needed to infect green pears than was the case for species such as P. cactorum, which are readily detected with pear baiting. Bourret 2018 used both green pears and rhododendron leaves for baiting but detected P. quercetorum on Rosa californica only with rhododendron leaves.
Consequences of introduction
2) Known pest host range. With the addition of Rosa californica to the host list, the known host range appears to be diverse, encompassing multiple unrelated plant families. The description should indicate that information about this pathogen’s host range is incomplete. Based on current data, the medium “2” rating can be justified, but this rating may well underestimate the host range of P. quercetorum.

Response: I agree that a 2 is appropriate now but the host range may increase, so I have that in the uncertainty

3) Pest Reproductive Potential. Assignment of the score 2 is not consistent with what is known about Phytophthora reproduction and dispersal, and the fact that this particular species has apparently spread across the U.S. in a relatively short time. A 3 rating is more appropriate.

Response: usually a 3 is for something that is seed borne or has a flying vector, soil borne pathogens usually gets a 1 or a 2.

4) Economic Impact
Should add criterion B to the list. The pest will lower crop value by both causing disease and death of infected plants and by increasing nursery costs that will be needed to keep it out of nurseries. This would not change the economic impact score of 3.

Response: I added criterion B

5) Environmental impact:
As noted above, P. quercetorum was found on a nursery-grown outplanted Quercus agrifolia container plant used for landscaping and in restoration plantings in Alameda county and in two different nurseries in northern California that supply plants to restoration sites. In nurseries it has been found on Q. agrifolia and Q. wislizeni. The plants from which P. quercetorum was recovered in Fresno county had originally been bought from a nursery in Southern California. It is therefore possible that the plants were infected before they were sold and that P. quercetorum has been circulating in southern California nurseries. Furthermore, it has been detected on Rosa californica planted in a restoration project.
Since this species has been recovered from wildland environments into which it has been introduced on nursery stock, it can clearly survive under these conditions. Hence, potential environmental impacts include B, C, and D as noted below. This would not change the environmental impact score of 3.
B. The pest could directly affect threatened or endangered species.
Phytophthora quercetorum was only described in 2008, but it clearly has been circulating in the nursery trade for a number of years. Although originally isolated from eastern U.S. on Quercus, it is not limited to Quercus. Its occurrence on Rosa californica raises the possibility it could be pathogenic to Rosa minutifolia, listed as a threatened or endangered species in:
California Natural Diversity Database (CNDDB). January 2021. State and Federally Listed Endangered, Threatened, and Rare Plants of California. California Department of Fish and Wildlife. Sacramento, CA.
Furthermore, multiple vertebrate species currently listed as threatened or endangered or proposed for listing utilize or depend upon various oak woodland habitats in California which would be threatened by wider introduction of this pathogen (see https://oaks.cnr.berkeley.edu/wildlife/).
C. The pest could impact threatened or endangered species by disrupting critical habitats.
Given the pathogenicity of this species to oaks, the importance of oak ecosystems throughout California, the stress oaks are already under due to diseases and pests such as polyphagous shothole borers, golden spotted oak borer, and sudden oak death, it is reasonable to expect further spread would disrupt critical habitats. The range of oak woodlands and other habitats containing oaks overlaps extensively with USFWS-designated critical habitat for threatened and endangered species in California. Because oak woodlands are so widely distributed and are tightly linked with many other adjoining and embedded habitats (e.g., riparian), impacts to oak health can disrupt a wide variety of critical habitats.
D. The pest could trigger additional official or private treatment programs.
Agencies that manage restoration plantings have already instituted treatment programs for restoration plantings in which Phytophthora-infested plants have been unwittingly outplanted. This pathogen is likely to trigger further actions of this type if it becomes more widely spread.

Response – I added criteria B, C and D

Consequences of Introduction to California for Phytophthora quercetorum:
This pathogen has potential to have high impact in California. If the above score changes are made, the total score would be 14.
6) Post Entry Distribution and Survey Information:
It is not clear how the medium rating can be supported, particularly given the specified criteria for evaluating the known California distribution. All data on the California distribution that are noted in the PRP and in this response indicate that this pathogen has only been detected in a few discrete areas. No data, including extensive field sampling surveys in oak woodland habitats (e.g., Swiecki, T. J.; Bernhardt, E. A. 2018. Evaluating threats posed by exotic Phytophthora species to endangered Coyote ceanothus and selected natural communities in the Santa Clara NCCP area.
Final report. Prepared for Santa Clara Valley Habitat Agency. 135p.; http://phytosphere.com/publications/Swiecki_Bernhardt_Evaluating_threats_posed_by_exotic_Ph ytophthora_species_3-15-18.pdf) provide any evidence that this pathogen has become “widespread in California”, which is needed to claim a medium rating. The fact that Quercus species are found statewide speaks to the threat that this pathogen poses, but does not in any way imply that the pathogen is widespread. For this pathogen, only a “low” rating can be supported from the available data.
The process for reducing the pest rating based in the “Post Entry Distribution and Survey Information” may be justifiable for some highly mobile pests that are easily spread aerially. However, this process is not scientifically defensible for pathogens such as soilborne Phytophthora species that are primarily moved by human activities such as the use of nursery stock and the movement of plant material or soil from infested areas. These modes of spread are exactly the types that can be targeted through regulatory approaches. Even the most widespread introduced Phytophthora species, e.g., P. cinnamomi, have not become “fully established in the endangered area” and the spread and impact of this and similar pathogens can still be mitigated by regulatory action. Hence, downrating of the California Pest Rating for soilborne Phytophthora species cannot be supported and this criterion should be listed as “not applicable” for these pathogens and others with similar epidemiology.

Response: Thank you for your comments, the criteria have been set by regulation and N/A is not one of my choices

7) The final score
The final score underestimates the risks associated with this pathogen. The overall final score should be 13. The overall rating would be 14 if the unjustified downgrading of the rating using the Post Entry Distribution and Survey Information criterion was not applied.
Conclusion and Rating Justification:
The proposed rating for Phytophthora quercetorum should be B. Although little is known about this pathogen in California, the fact that it has become widely established in forest soils in the eastern United States suggests it could eventually become more widely established in California, where it could impact one of the state’s largest, most biologically diverse, and ecologically critical vegetation types. Data to date indicate that Phytophthora quercetorum is moving in the nursery trade, including in restoration nurseries, which will provide many opportunities for its introduction into California cultivated and wild landscapes.

Comments from Faith Thompson Campbell, Ph.D.
Subject: Comments on California Pest Rating Proposal for Phytophthora quercetorum
The Center for Invasive Species Prevention (CISP) is pleased that the California Department of Food and Agriculture (CDFA) is assessing the pest risk ratings of several Phytophthora species recently determined to be present in California. We appreciate the opportunity at this time to comment on the proposed rating for Phytophthora quercetorum.
We note that the CDFA proposes a “C” rating for Phytophthora quercetorum.
We are troubled by this proposed rating, for the reasons stated below. We consider a “B” rating to be more justified, accurate, and consistent with the State’s goal of protecting California’s flora.
Two Concerns re: the Overall Agency Approach
The data presented in the CDFA proposal clearly demonstrate a troubling delay in responding to this threat. The earliest nursery detection was in 2014 – six years ago. There have since been several more detections in nurseries growing plants for use in restoration projects. The proposal states that infected soils, plants, planting stock, and seedlings, rain and irrigation water, and cultivation equipment and tools might spread P. quercetorum. Under these circumstances, the Center for Invasive species Prevention asks why the agency allowed the continued presence for six years of this potential pathogen in nurseries. That these are nurseries producing plants intended for planting not in horticultural settings but in native ecosystems is makes this question especially serious
We are also troubled by the apparent decision to not evaluate the risk P. quercetorum apparently poses to hosts other than the two native oaks on which it has been detected to date in California. CDFA does not indicate that it doubts the host status of two known hosts. First is Acer rubrum. Admittedly, the known host is a maple native to eastern North America. However, California has several Acer species in both horticultural use and in the wild that might be vulnerable to the pathogen. Second, Hedera helix, a plant widely used in ornamental horticulture and thus a potential source of spread. Nor has CDFA apparently sought to determine possible host status of California oaks in the white oak group (section Quercus) – including blue (Q. douglasii), Garry (Q. garryana), and valley (Q. lobata) oaks. A proposal to rate this disease without recognizing the potential for additional host species is incomplete and warrants a more cautious approach than a “C” rating.
Concerns re Distribution and Consequences
1) The data presented in the CDFA proposal are too limited to determine the species’ true distribution in California.
The decision to accept only official records has forced CDFA to minimize the probable risk of spread of P. quercetorum — and its impact. As the proposal notes, Quercus species are found statewide so there is nothing preventing the pathogen’s spread statewide as well. This flaw might have been mitigated by a broader discussion of uncertainty, i.e., by including uncertainties in the distribution of P. quercetorum. Instead, that discussion is limited to the lack of understanding of the pathogenicity of this species.
Also, the proposal does not discuss the probability of additional hosts, the extent to which infected plants have been placed in the environment, or the possible presence of the pathogen in other parts of the state. It is unfortunate that CDFA has not answered such basic questions in the six years that it has been aware of P. quercetorum’s presence in California.

Response: The use of official records is a requirement of the proposal, but unofficial samples received by our labs and in published literature are mentioned. In the uncertainty section is the of lack of detailed pathogenicity studies and the possibility of expanding host records. Since it has been found in nursery stock and not under quarantine regulation, I agree it’s likely already more widespread than has been documented.

2) Consequences of Introduction/Hosts
We concur that the “Consequences of Introduction to California” for Phytophthora quercetorum is “High”. We further agree that the microorganism is likely to spread throughout the state, wherever hosts grow.
We emphatically do not agree that the impact of P. quercetorum on California oak species and their plant communities should be rated as “medium to low”. The two known hosts – Q. agrifolia and Q. wislizeni – are widespread and ecologically important.

Response: Others have commented similarly, and I have added criteria and now environmental impact and economic impact are both High

Quercus agrifolia (coast live oak) grows along the western coastal range, from central California southward to northern Baja California, on bluffs, gentle slopes, and canyons up to 4,500 feet in elevation. It is particularly well adapted to the fires so common in these ecosystems. Coast live oaks are also found in southern California’s parks, residential landscapes, and streets where they provide shade and aesthetic value. Q. agrifolia trees are already being killed by sudden oak death (SOD), a disease caused by the introduced pathogen Phytophthora ramorum; and goldspotted oak borer (GSOB – Agrilus auroguttatus). It is also sometimes attacked by the polyphagous shot hole borer (PSHB; Euwallacea whitfordiodendrus) and its associated Fusarium fungus).
Interior live oak (Quercus wislizeni) occurs over about 16% of California’s landscape, especially in the Inner Coast Ranges, the foothills of the southern Cascade Range, and the Sierra Nevada. Among California’s red oaks, interior live oak has the highest tolerance for xeric conditions. It usually dominates the “scrub” or “live oak” chaparral vegetation types in the Inner Coast Ranges and the Sierra Nevada.

Response: there are pathogens with hundreds of hosts, these usually get the highest score which is a 3.

Conclusion
As we noted at the beginning of our comments, restoration plantings present a direct pathway for introduction of P. quercetorum into habitats of very high conservation value – habitats where public agencies and private organizations have invested significant resources in conservation. A “B” rating would allow local (county) officials to consider actions aimed at protecting these resources. They would not be required to take such actions, although CISP hopes they would do so. Such actions would provide some protection to the state’s unique biodiversity and ecological resources. Therefore, the Center for Invasive Species Prevention asks that the California Department of Food and Agriculture amend its proposal and assign a risk rating of “B” to Phytophthora quercetorum.
Sincerely,
Faith Thompson Campbell, Ph.D.
Center for Invasive Species Prevention http://www.cisp.us

Response: thank you for your comments

Comments from Susan Frankel
Heather – For the Phytophthora quercetorum pest rating – now out for comment, I checked with Tyler Bourret, UC Davis Plant Pathology since we are about to publish a catalogue of Phytophthora detections in CA.
Below he points out that Genbank has a few more entries for Phytophthora quercetorum and that P. quercina is in Clade 12.
Please see his comment below. The Phytophthoras in Native Habitat Work Group will likely submit a general comment on the P. q. ranking but I thought these technical points could be better addressed in this email.
By the way, I am finding your PRA of Leptosillia pistaciae very helpful as we struggle to figure out why so many Acacias are dying in the Bay Area. Thanks so much for your work on that!
OK back to P. q. – please see Tyler’s note below (slightly edited by SF). If you have any questions, please contact Tyler at tbbourret@ucdavis.edu.

Thanks, Susan Susan Frankel
Plant Pathologist Forest Service
Pacific Southwest Research Station
From: Tyler Bourret “tbbourret@ucdavis.edu”
Sent: Thursday, December 3, 2020 9:00 PM
To: Frankel, Susan -FS “susan.frankel@usda.gov”
Subject: Re: Another CDFA PRA. Phytophthora quercetorum Y. Balci & S. Balci 2008

Just following up, I read the pest rating. My comments:

I noticed that Heather put P. quercina in clade 4, which was the outcome of one early phylogenetic study, but no longer the case (P. quercina is in clade 12). Super minor point, but might confuse people due to the similar names.
All three of those Phytophthora quercetorum GenBank sequences I previously mentioned are not in the CDFA database or mentioned in the report, and add three counties and one associated host (Rosa californica) to the list.
ITS accession Strain / Isolate Location Substrate / Plant Part Host / Associated Host
GU258630.1 P10080 Orange Co. Quercus agrifolia
MG707807.1 SCVWD384 Santa Clara Co. Soil and roots Rosa californica
MW142299.1 LA66_R1 Los Angeles Co. Soil and roots Quercus sp.

-Tyler

Response: thank you for the additional data, I have added the extra host and Counties

One thought on “PHYTOPHTHORA QUERCETORUM Y. BALCI & S. BALCI 2008”

Heather Scheck says:

January 27, 2021 at 2:36 pm

Comments from Janice Alexander
From: Phytophthoras in Native Habitats Work Group, http://www.calphytos.org,
Subject: Comments on California Pest Rating Proposal for Phytophthora quercetorum
The Phytophthoras in Native Habitats Work Group is pleased that the CDFA is assessing the pest risk ratings of several Phytophthora species; we appreciate the opportunity to comment as proposed ratings become available. Here we comment on the posted California Pest Rating Proposal for Phytophthora quercetorum which is proposed for a “C” rating.
We see the “C” rating as problematic for this organism. We suggest it be assigned a “B” rating. A “C”-rating is for “pests of the agricultural industry or environment which score medium to low and are of common occurrence and generally distributed in California. Authorized mitigating regulatory actions: Plants and plant products found infested or infected with or exposed to a “C”-rated pest are not subject to any State enforced regulatory actions listed under subsection 3162(e)” (CHAPTER 5B-3 PLANT QUARANTINE).
A “C” rating is inappropriate for P. quercetorum because:
1) Its distribution is not fully understood, there are few reports in California, and it is not known to be generally distributed in the state.

Response: It is in the nursery trades, not under quarantine action, and there are detections in the Bay Area, Sacramento and Fresno, plus in Southern California in Los Angeles and Orange Counties

2) Its impact to restoration activities, rare plants, wildland and nurseries is most likely not medium to low.
Response: there are not many published reports of plant damage. Most detections have been made by baiting and from plants that are co-infected with other pathogens.
A “B” rating would be beneficial to plant health in California because it would allow response action at the discretion of the County Agricultural Commissioner. It would not be onerous, as it would not require action.
In the risk rating proposal, the distribution and known hosts for P. quercetorum are limited. We are concerned since the organism has been found on several oak (Quercus) species that are important components of California ecosystems (e.g., Q. agrifolia, Q. wislizeni). P. quercetorum has been found in several restoration and horticultural nurseries and in soil associated with Q. agrifolia. Balci and others (2008) found some damage to eastern oak species after inoculation with P. quercetorum.
Restoration activities present a direct pathway for Phytophthora and other pathogen introductions into habitat of very high conservation value (Frankel and others 2020a, 2020b). A “B” rating would allow for consideration of response action but not require it; It would provide some protection to California’s biodiversity and ecological resources. To sustain the health of California wildlands and conservation investments, a “B” rating for P. quercetorum is needed.
Thank you for considering these points. Please let us know if we may be of further assistance. For more information on Phytophthoras in California native plant nurseries and restoration sites, see http://www.calphytos.org, or contact Janice Alexander, UC Cooperative Extension, Marin Co. We look forward to continuing to work with you to sustain plant health for California.
References
Balci, Y., Balci, S., MacDonald, W. L., & Gottschalk, K. W. 2008. Relative susceptibility of oaks to seven species of Phytophthora isolated from oak forest soils. Forest Pathology, 38(6), 394-409.
Frankel, S. J.; Alexander, J.; Benner, D.;Hillman, J. and Shor, A. 2020a. Phytophthora pathogens threaten rare habitats and conservation plantings. Sibbaldia: the International Journal of Botanic Garden Horticulture, (18): 53-65.
Frankel, S.J.; Conforti, C.; Hillman, J.; Ingolia, M.; Shor, A.; Benner, B. Alexander, J.A.; Bernhardt, E.; and Swiecki, T.J. 2020b. Phytophthora Pathogen Introductions in California Restoration areas: Protecting California Native Flora from Human-assisted Pathogen Spread. Forests. 11: 1291. doi: 10.3390/f11121291.

Response: Thank you for your comments and for the additional references.

Comments from Pierluigi (Enrico) Bonello
Dear Dr. Scheck,
I tried to leave a comment on the pest rating proposal for Phytophthora quercetorum but could not find a way to register on the site, so I am sending you my comment this way. I hope it is OK.
Although I am based in Ohio I have done a lot of research on the coast live oak-P. ramorum interaction in California (you can check my publications list on my website), so I am well informed on the risks posed by Phytophthoras in CA forests. For this reason I find the proposed rating highly perplexing. Why is it just a C rating? Especially in the face of rather high rankings on most of the objective measures CDFA itself reports? The fact that we do not have as much info about P quercetorum as we do for e.g. P ramorum should not be sufficient reason to give it a low rating. This outome may result in highly problematic delays in dealing with a potentially highly destructive pathogen.
I hope CDFA will consider giving it a rating of at least B.
Thank you for listening.
Pierluigi (Enrico) Bonello
Professor
College of Food, Agricultural, and Environmental Sciences Plant Pathology
201 Kottman Hall, 2021 Coffey Road, Columbus, OH 43210
614-688-5401 Office / 614-292-4455 Fax
bonello.2@osu.edu / https://plantpath.osu.edu/our-people/pierluigi-enrico-bonello
Pronouns: he/him/his

Response: Thank you for your comments

Comments From: Elizabeth Bernhardt, Ph. D. and Tedmund Swiecki, Ph.D.
Re: Review of: California Pest Rating Proposal for Phytophthora quercetorum Y. Balci & S. Balci 2008, dated 11.20.20
We offer the following comments for your consideration as you finalize the pest rating proposal.
Initiating Event: We think many of the finds of P. quercetorum referred to in this paragraph are from us. For clarity, we list the isolations of P. quercetorum in our database that were submitted to CDFA. All our recoveries of P. quercetorum are from nursery origin plants.
PDR number Our isolate number Host Site/County Notes
MVAP06098963 TS140224-QA1a Quercus agrifolia Nursery/Sacramento Abundant sporulation seen on rotted roots growing out of treepot container, direct isolation, submitted to CDFA for identification.
MV6P06458940 PR150923-SY-S1 Quercus agrifolia Transplant in landscape/ Alameda DBH ~ 40 cm, top appears healthy relative to neighbors, large bleeding canker lower bole, detected by pear baiting of roots/soil. Direct isolation from canker margin onto PARP was negative.
MV6P06578761 PR170810-A5-1 Quercus wislizeni Nursery/ Fresno Pear baiting of leachate test of 24 treepots (4×14″), plants variable, with stunting, 2 with recent dead tops
MV6P06578761 PR170810-A7-4 Quercus agrifolia Nursery/ Fresno Pear baiting of leachate test of 24 treepots (4×14″), tall plants, a few stunted, 2 dead
MV6P06578793 PR20190822-AS4- 2-45-QUAG ’12-2A Quercus agrifolia Transplant in restoration site/ Alameda Tree about 3 m tall, split leader, each about 2.5 cm DBH. Sparse and dwarfed relative to other ungirdled neighbors, leaves on plant are rather small, detected by pear baiting of roots/soil
Also collected and submitted to CDFA directly by a client:
MVAP06099050 SF140527-QA01 Quercus agrifolia Transplant in restoration site/ Alameda Tall seedling that has been dead for a while; plant is at least 2 yrs old, CDFA detected by baiting roots with oregano leaves

Response: thank you for the clarification on the Q. agrifolia sample (not from San Francisco Co), I have corrected the document.

History & Status:
Background:
Hosts: Add Rosa californica (Rosaceae) from
Bourret, T.B. Efforts to detect exotic Phytophthora species reveal unexpected diversity. Chapter 2. Restoration outplantings of nursery‐origin Californian flora are heavily infested with Phytophthora. Ph.D. Thesis. University of California, Davis, CA. ProQuest Dissertations Publishing. 2018, 10746957.

Response: thank you for the reference, I have added Rosa californica to the host list.

The fact that oregano leaves and rhododendron leaves have been used to successfully bait P. quercetorum from infected oak roots suggests that these plants and possibly other plants in these families (Lamiaceae, Ericaceae) could also be hosts. Young wounded leaves of Rhododendron maxima developed lesions after artificial inoculation with P. quercetorum on agar plugs as described in:
Balci, Y., Balci, S., MacDonald, W. L., & Gottschalk, K. W. 2008. Foliar susceptibility of Eastern oak species to Phytophthora infection. Forest Pathology, 38(6), 394-409.
Symptoms
The description of disease starting with a canker at the soil line has disease progression backwards. Based on literature noted below, P. quercetorum is typical of many other root-rotting Phytophthora species in that infections are normally initiated on roots and progress upward, sometimes causing basal cankers.
The original description states “P. quercetorum was associated with oak roots and never isolated from aboveground portions of oak”.
Balci, Y., Balci, S., Blair, J.E., Park, S.Y., Kang, S. and Macdonald, W.L., 2008. Phytophthora quercetorum sp. nov., a novel species isolated from eastern and north- central USA oak forest soils. Mycological Research, 112(8), pp.906-916.
No bleeding Phytophthora cankers were reported on any of the trees at the sampling sites in:
McConnell, M.E. and Balci, Y., 2014. Phytophthora cinnamomi as a contributor to white oak decline in mid-Atlantic United States forests. Plant disease, 98(3), pp.319- 327.
which lists recoveries of P. quercetorum from Acer rubrum and Quercus alba.
A clear example of how root rots initiate cankers that can advance up the taproot to the lower stem is shown in Figure 1 in:
Balci, Y., Balci, S., MacDonald, W. L., & Gottschalk, K. W. 2008. Relative susceptibility of oaks to seven species of Phytophthora isolated from oak forest soils. Forest Pathology, 38(6), 394-409.
P. quercetorum is among the species tested in this report.
Based on the literature, it appears P. quercetorum causes fine root rot and can infect taproots of one year old seedlings of various oak species (Balci et al. 2008 Forest Pathology), indicating it is not restricted to fine roots. When enough roots are infected there may be enough inoculum present to initiate cankers at the soil line under flooded conditions, which was perhaps the case for MV6P06458940. No basal canker was associated with infection of MV6P06578793.
The last sentence in this paragraph, related to temperature, in which Agrios is cited, should be replaced by information specific to this species. In the species description paper, Balci et al. Fig.7 (2008 Mycological Research) shows that P. quercetorum grew optimally on media from about 22.5 to 27.5 C, with a minimum growth temperature between 5 and 10 C and a maximum between 30 to 32.5 C, showing that it has wide adaptability to a range of temperatures. Balci et al. 2008 (the Forest Pathology paper) conducted pathogenicity tests in summer and winter in West Virginia. There was no consistent seasonal difference in taproot infections for P. quercetorum across the 6 oak species evaluated (Table 4 in Balci et al. 2008 Forest Pathology).

Response: thank you for those citations, I have amended this section.

California distribution:
If the record for occurrence in San Francisco comes from MV6P06458940, that would be an error. Although the tree owner had a San Francisco address, the tree itself was located in Alameda County.
The record of P. quercetorum on Rosa californica from Bourret 2018 is from Santa Clara County, which should be added to the California distribution.

Response: I have made the county correction and added R. californica and Santa Clara County

Based on the association of this pathogen with nursery stock and the lack of any concerted effort to detect it, it is likely that the CA distribution is wider than these few detections indicate.
As a side note, P. quercetorum seems to be difficult to detect. Balci et al. 2018 Forest Pathology indicate they had difficulty reisolating it from necrotic lesions on stems that resulted from artificial inoculation. Often multiple attempts had to be made before a successful isolation. We found that higher zoospore concentrations of P. quercetorum were needed to infect green pears than was the case for species such as P. cactorum, which are readily detected with pear baiting. Bourret 2018 used both green pears and rhododendron leaves for baiting but detected P. quercetorum on Rosa californica only with rhododendron leaves.
Consequences of introduction
2) Known pest host range. With the addition of Rosa californica to the host list, the known host range appears to be diverse, encompassing multiple unrelated plant families. The description should indicate that information about this pathogen’s host range is incomplete. Based on current data, the medium “2” rating can be justified, but this rating may well underestimate the host range of P. quercetorum.

Response: I agree that a 2 is appropriate now but the host range may increase, so I have that in the uncertainty

3) Pest Reproductive Potential. Assignment of the score 2 is not consistent with what is known about Phytophthora reproduction and dispersal, and the fact that this particular species has apparently spread across the U.S. in a relatively short time. A 3 rating is more appropriate.

Response: usually a 3 is for something that is seed borne or has a flying vector, soil borne pathogens usually gets a 1 or a 2.

4) Economic Impact
Should add criterion B to the list. The pest will lower crop value by both causing disease and death of infected plants and by increasing nursery costs that will be needed to keep it out of nurseries. This would not change the economic impact score of 3.

Response: I added criterion B

5) Environmental impact:
As noted above, P. quercetorum was found on a nursery-grown outplanted Quercus agrifolia container plant used for landscaping and in restoration plantings in Alameda county and in two different nurseries in northern California that supply plants to restoration sites. In nurseries it has been found on Q. agrifolia and Q. wislizeni. The plants from which P. quercetorum was recovered in Fresno county had originally been bought from a nursery in Southern California. It is therefore possible that the plants were infected before they were sold and that P. quercetorum has been circulating in southern California nurseries. Furthermore, it has been detected on Rosa californica planted in a restoration project.
Since this species has been recovered from wildland environments into which it has been introduced on nursery stock, it can clearly survive under these conditions. Hence, potential environmental impacts include B, C, and D as noted below. This would not change the environmental impact score of 3.
B. The pest could directly affect threatened or endangered species.
Phytophthora quercetorum was only described in 2008, but it clearly has been circulating in the nursery trade for a number of years. Although originally isolated from eastern U.S. on Quercus, it is not limited to Quercus. Its occurrence on Rosa californica raises the possibility it could be pathogenic to Rosa minutifolia, listed as a threatened or endangered species in:
California Natural Diversity Database (CNDDB). January 2021. State and Federally Listed Endangered, Threatened, and Rare Plants of California. California Department of Fish and Wildlife. Sacramento, CA.
Furthermore, multiple vertebrate species currently listed as threatened or endangered or proposed for listing utilize or depend upon various oak woodland habitats in California which would be threatened by wider introduction of this pathogen (see https://oaks.cnr.berkeley.edu/wildlife/).
C. The pest could impact threatened or endangered species by disrupting critical habitats.
Given the pathogenicity of this species to oaks, the importance of oak ecosystems throughout California, the stress oaks are already under due to diseases and pests such as polyphagous shothole borers, golden spotted oak borer, and sudden oak death, it is reasonable to expect further spread would disrupt critical habitats. The range of oak woodlands and other habitats containing oaks overlaps extensively with USFWS-designated critical habitat for threatened and endangered species in California. Because oak woodlands are so widely distributed and are tightly linked with many other adjoining and embedded habitats (e.g., riparian), impacts to oak health can disrupt a wide variety of critical habitats.
D. The pest could trigger additional official or private treatment programs.
Agencies that manage restoration plantings have already instituted treatment programs for restoration plantings in which Phytophthora-infested plants have been unwittingly outplanted. This pathogen is likely to trigger further actions of this type if it becomes more widely spread.

Response – I added criteria B, C and D

Consequences of Introduction to California for Phytophthora quercetorum:
This pathogen has potential to have high impact in California. If the above score changes are made, the total score would be 14.
6) Post Entry Distribution and Survey Information:
It is not clear how the medium rating can be supported, particularly given the specified criteria for evaluating the known California distribution. All data on the California distribution that are noted in the PRP and in this response indicate that this pathogen has only been detected in a few discrete areas. No data, including extensive field sampling surveys in oak woodland habitats (e.g., Swiecki, T. J.; Bernhardt, E. A. 2018. Evaluating threats posed by exotic Phytophthora species to endangered Coyote ceanothus and selected natural communities in the Santa Clara NCCP area.
Final report. Prepared for Santa Clara Valley Habitat Agency. 135p.; http://phytosphere.com/publications/Swiecki_Bernhardt_Evaluating_threats_posed_by_exotic_Ph ytophthora_species_3-15-18.pdf) provide any evidence that this pathogen has become “widespread in California”, which is needed to claim a medium rating. The fact that Quercus species are found statewide speaks to the threat that this pathogen poses, but does not in any way imply that the pathogen is widespread. For this pathogen, only a “low” rating can be supported from the available data.
The process for reducing the pest rating based in the “Post Entry Distribution and Survey Information” may be justifiable for some highly mobile pests that are easily spread aerially. However, this process is not scientifically defensible for pathogens such as soilborne Phytophthora species that are primarily moved by human activities such as the use of nursery stock and the movement of plant material or soil from infested areas. These modes of spread are exactly the types that can be targeted through regulatory approaches. Even the most widespread introduced Phytophthora species, e.g., P. cinnamomi, have not become “fully established in the endangered area” and the spread and impact of this and similar pathogens can still be mitigated by regulatory action. Hence, downrating of the California Pest Rating for soilborne Phytophthora species cannot be supported and this criterion should be listed as “not applicable” for these pathogens and others with similar epidemiology.

Response: Thank you for your comments, the criteria have been set by regulation and N/A is not one of my choices

7) The final score
The final score underestimates the risks associated with this pathogen. The overall final score should be 13. The overall rating would be 14 if the unjustified downgrading of the rating using the Post Entry Distribution and Survey Information criterion was not applied.
Conclusion and Rating Justification:
The proposed rating for Phytophthora quercetorum should be B. Although little is known about this pathogen in California, the fact that it has become widely established in forest soils in the eastern United States suggests it could eventually become more widely established in California, where it could impact one of the state’s largest, most biologically diverse, and ecologically critical vegetation types. Data to date indicate that Phytophthora quercetorum is moving in the nursery trade, including in restoration nurseries, which will provide many opportunities for its introduction into California cultivated and wild landscapes.

Comments from Faith Thompson Campbell, Ph.D.
Subject: Comments on California Pest Rating Proposal for Phytophthora quercetorum
The Center for Invasive Species Prevention (CISP) is pleased that the California Department of Food and Agriculture (CDFA) is assessing the pest risk ratings of several Phytophthora species recently determined to be present in California. We appreciate the opportunity at this time to comment on the proposed rating for Phytophthora quercetorum.
We note that the CDFA proposes a “C” rating for Phytophthora quercetorum.
We are troubled by this proposed rating, for the reasons stated below. We consider a “B” rating to be more justified, accurate, and consistent with the State’s goal of protecting California’s flora.
Two Concerns re: the Overall Agency Approach
The data presented in the CDFA proposal clearly demonstrate a troubling delay in responding to this threat. The earliest nursery detection was in 2014 – six years ago. There have since been several more detections in nurseries growing plants for use in restoration projects. The proposal states that infected soils, plants, planting stock, and seedlings, rain and irrigation water, and cultivation equipment and tools might spread P. quercetorum. Under these circumstances, the Center for Invasive species Prevention asks why the agency allowed the continued presence for six years of this potential pathogen in nurseries. That these are nurseries producing plants intended for planting not in horticultural settings but in native ecosystems is makes this question especially serious
We are also troubled by the apparent decision to not evaluate the risk P. quercetorum apparently poses to hosts other than the two native oaks on which it has been detected to date in California. CDFA does not indicate that it doubts the host status of two known hosts. First is Acer rubrum. Admittedly, the known host is a maple native to eastern North America. However, California has several Acer species in both horticultural use and in the wild that might be vulnerable to the pathogen. Second, Hedera helix, a plant widely used in ornamental horticulture and thus a potential source of spread. Nor has CDFA apparently sought to determine possible host status of California oaks in the white oak group (section Quercus) – including blue (Q. douglasii), Garry (Q. garryana), and valley (Q. lobata) oaks. A proposal to rate this disease without recognizing the potential for additional host species is incomplete and warrants a more cautious approach than a “C” rating.
Concerns re Distribution and Consequences
1) The data presented in the CDFA proposal are too limited to determine the species’ true distribution in California.
The decision to accept only official records has forced CDFA to minimize the probable risk of spread of P. quercetorum — and its impact. As the proposal notes, Quercus species are found statewide so there is nothing preventing the pathogen’s spread statewide as well. This flaw might have been mitigated by a broader discussion of uncertainty, i.e., by including uncertainties in the distribution of P. quercetorum. Instead, that discussion is limited to the lack of understanding of the pathogenicity of this species.
Also, the proposal does not discuss the probability of additional hosts, the extent to which infected plants have been placed in the environment, or the possible presence of the pathogen in other parts of the state. It is unfortunate that CDFA has not answered such basic questions in the six years that it has been aware of P. quercetorum’s presence in California.

Response: The use of official records is a requirement of the proposal, but unofficial samples received by our labs and in published literature are mentioned. In the uncertainty section is the of lack of detailed pathogenicity studies and the possibility of expanding host records. Since it has been found in nursery stock and not under quarantine regulation, I agree it’s likely already more widespread than has been documented.

2) Consequences of Introduction/Hosts
We concur that the “Consequences of Introduction to California” for Phytophthora quercetorum is “High”. We further agree that the microorganism is likely to spread throughout the state, wherever hosts grow.
We emphatically do not agree that the impact of P. quercetorum on California oak species and their plant communities should be rated as “medium to low”. The two known hosts – Q. agrifolia and Q. wislizeni – are widespread and ecologically important.

Response: Others have commented similarly, and I have added criteria and now environmental impact and economic impact are both High

Quercus agrifolia (coast live oak) grows along the western coastal range, from central California southward to northern Baja California, on bluffs, gentle slopes, and canyons up to 4,500 feet in elevation. It is particularly well adapted to the fires so common in these ecosystems. Coast live oaks are also found in southern California’s parks, residential landscapes, and streets where they provide shade and aesthetic value. Q. agrifolia trees are already being killed by sudden oak death (SOD), a disease caused by the introduced pathogen Phytophthora ramorum; and goldspotted oak borer (GSOB – Agrilus auroguttatus). It is also sometimes attacked by the polyphagous shot hole borer (PSHB; Euwallacea whitfordiodendrus) and its associated Fusarium fungus).
Interior live oak (Quercus wislizeni) occurs over about 16% of California’s landscape, especially in the Inner Coast Ranges, the foothills of the southern Cascade Range, and the Sierra Nevada. Among California’s red oaks, interior live oak has the highest tolerance for xeric conditions. It usually dominates the “scrub” or “live oak” chaparral vegetation types in the Inner Coast Ranges and the Sierra Nevada.

Response: there are pathogens with hundreds of hosts, these usually get the highest score which is a 3.

Conclusion
As we noted at the beginning of our comments, restoration plantings present a direct pathway for introduction of P. quercetorum into habitats of very high conservation value – habitats where public agencies and private organizations have invested significant resources in conservation. A “B” rating would allow local (county) officials to consider actions aimed at protecting these resources. They would not be required to take such actions, although CISP hopes they would do so. Such actions would provide some protection to the state’s unique biodiversity and ecological resources. Therefore, the Center for Invasive Species Prevention asks that the California Department of Food and Agriculture amend its proposal and assign a risk rating of “B” to Phytophthora quercetorum.
Sincerely,
Faith Thompson Campbell, Ph.D.
Center for Invasive Species Prevention http://www.cisp.us

Response: thank you for your comments

Comments from Susan Frankel
Heather – For the Phytophthora quercetorum pest rating – now out for comment, I checked with Tyler Bourret, UC Davis Plant Pathology since we are about to publish a catalogue of Phytophthora detections in CA.
Below he points out that Genbank has a few more entries for Phytophthora quercetorum and that P. quercina is in Clade 12.
Please see his comment below. The Phytophthoras in Native Habitat Work Group will likely submit a general comment on the P. q. ranking but I thought these technical points could be better addressed in this email.
By the way, I am finding your PRA of Leptosillia pistaciae very helpful as we struggle to figure out why so many Acacias are dying in the Bay Area. Thanks so much for your work on that!
OK back to P. q. – please see Tyler’s note below (slightly edited by SF). If you have any questions, please contact Tyler at tbbourret@ucdavis.edu.

Thanks, Susan Susan Frankel
Plant Pathologist Forest Service
Pacific Southwest Research Station
From: Tyler Bourret “tbbourret@ucdavis.edu”
Sent: Thursday, December 3, 2020 9:00 PM
To: Frankel, Susan -FS “susan.frankel@usda.gov”
Subject: Re: Another CDFA PRA. Phytophthora quercetorum Y. Balci & S. Balci 2008

Just following up, I read the pest rating. My comments:

I noticed that Heather put P. quercina in clade 4, which was the outcome of one early phylogenetic study, but no longer the case (P. quercina is in clade 12). Super minor point, but might confuse people due to the similar names.
All three of those Phytophthora quercetorum GenBank sequences I previously mentioned are not in the CDFA database or mentioned in the report, and add three counties and one associated host (Rosa californica) to the list.
ITS accession Strain / Isolate Location Substrate / Plant Part Host / Associated Host
GU258630.1 P10080 Orange Co. Quercus agrifolia
MG707807.1 SCVWD384 Santa Clara Co. Soil and roots Rosa californica
MW142299.1 LA66_R1 Los Angeles Co. Soil and roots Quercus sp.

-Tyler

Response: thank you for the additional data, I have added the extra host and Counties