Podosphaera caricae-papayae

California Pest Rating for

Podosphaera caricae-papayae

Pest Rating: B

PEST RATING PROFILE

Initiating Event:

In March 2014, Podosphaera caricae-papayae, a powdery mildew fungal pathogen, was identified by morphological and sequence analyses by Suzanne Latham, plant pathologist, CDFA. The symptomatic papaya leaf sample was collected from an ornamental container nursery in Santa Barbara County by County Agricultural plant pathologist, Heather Scheck. The identity of the pathogen was confirmed by USDA APHIS PPQ Mycologist, Megan Romberg. Subsequently, the nursery destroyed the infected papaya plants. In May 2014, the same pathogen was detected on papaya plants, grown in a commercial papaya fruit production nursery greenhouse at a different location within Santa Barbara County. The detection of powdery mildew of papaya in Santa Barbara County marks a first record for North America. Initially, the fungal pathogen was assigned a Q rating which is reassessed herein for the proposal of a permanent rating.

History & Status:

Background: Podosphaera caricae-papayae was originally described by Tanda and Braun in 1985 as Sphaerotheca caricae-papayae. However, in 2000 the species was placed in the genus Podosphaera based on molecular sequence analysis by Braun and Takamatsu (Romberg, 2014). Complications in taxonomic classification of the species exist over the accurate linkage of the sexual or teleomorph stage to the asexual or anamorph stage of the pathogen and further molecular and morphological studies are needed to determine the correct taxonomic position of P. caricae-papayae. In the original description of the species, the teleomorph stage, Sphaerotheca, was linked to the anamorph stage, Oidium caricae (Liberato et al., 2004). However, later this linkage was proven inaccurate and O. caricae was rejected as the anamorph stage, thereby leaving the classification of an asexual stage for P. caricae-papayae unresolved. The exact distribution is unknown because it is unclear which records of “O. caricae” actually belong to P. caricae-papayae. In 2012, P. caricae-papayae was synonymized with the morphologically similar species P. xanthii – the pathogen causing powdery mildew on cucurbits (Braun & Cook, 2012). The synonymy of P. xanthii and P. caricae-papayae is in question given recent molecular work (Takamatsu et al., 2010). P. caricae-papayae is only known from infected seedlings of papaya in Australia, China, India, Japan, New Zealand and California (USA). Greenhouse infections of papaya plants in California were reported as being caused by “cucurbit powdery mildew”. Infections of mature papaya plants in the field have never been reported.

The infected papaya plants recently detected in California only bear the anamorph stage which morphologically resembles the anamorph stage of P. caricae-papayae that was described by Tanda and Braun in 1985 (Romberg, 2014). Furthermore, molecular sequence analysis revealed that the sequences from both California detections are identical to a sequence of P. caricae-papayae from Thailand that was used by Takamatsu et al., (2010) in their phylogenetic analyses of the genus Podosphaera (Latham, 2014; Romberg, 2014). Unfortunately, no morphological information of the Thailand isolate is available to compare with the California isolate. The sequence from Thailand is the only P. caricae-papayae sequence deposited in GenBank and therefore, analytical sequence comparisons of isolates of P. caricae-papayae from California and Thailand with those from other reported regions are lacking. Nevertheless, the Thailand sequence is different from other Podosphaera species sequences in Genbank, including the cucurbit powdery mildew, P. xanthii. Further molecular and morphological studies which would include more isolates will help determine the correct taxonomic position of P. caricae-papayae within the genus Podosphaera in the family Erysiphaceae of the order Erysiphales (Takamatsu et al., 2010).

Powdery mildew of papaya is on obligate parasite. The fungus grows on the surface of plant tissue and invades by sending feeding organs (haustoria) into the plants epidermal cells only in order to obtain nutrients. Mycelium produces conidiophores on the plant surface. Each conidiophore produces chains of conidia (spores) that are dispersed by air currents. Powdery mildew thrives in warm and humid environments. Low light levels, high humidity, moderate temperature and rainfall enhance disease development in papaya (Cunningham & Nelson, 2012). Generally, disease can be severe in warm and dry climate as long as the relative humidity is high enough to enable condial germination and infection.

Hosts: Carica papaya (papaya).

Symptoms: Powdery mildew infects papaya plants of all ages however seedlings in greenhouses are more susceptible than field grown plants. The pathogen frequently infects young immature leaves, petioles, pedicels, peduncles, and unripe fruit. Early on, the undersides of leaves become speckled with small water-soaked spots with white to grayish powdery fungal patches usually near the leaf veins. Yellow-green spots develop on the corresponding upper sides. Soon the patches grow in size and coalesce, and fungal growth may grow on the upper leaf surface and veins. In severe infections, leaves become necrotic, curl and drop prematurely. Mildew patches also develop on immature fruit and can cover the entire fruit, eventually resulting in deformed fruit (Cunningham & Nelson, 2012).

Damage Potential: Infections can result in prematurely defoliated trees, mildewed and deformed fruit causing significant if not, total losses in plant growth and crop yield. Deformed fruit is not marketable resulting in lowered sales. Infections occurring in plants grown in greenhouse can result in severe spread and loss in production if left unmanaged.

In California, there is no commercial acreage under cultivation for papaya. Production is limited to ornamental and fruit production nursery greenhouse and residential gardens for ornamental purposes in southern California counties. Under those environments, loss in production is possible if not managed.

Transmission: Conidia (spores) are primarily dispersed by wind currents.

Survival: During cool weather, condia production ceases and powdery mildew fungi overwinter as cleistothecia (a sexually produced, closed, fruiting body) and mycelium in dormant plant tissue. However, only the asexual stage has been found in California greenhouses. Constant greenhouse growth conditions could perpetuate the anamorphic stage of the fungus.

Worldwide Distribution: The true distribution of the California isolate of P. caricae-papayae is currently not known. Molecular sequence analyses remain unknown for reported isolates of P. caricae-papayae from Australia, China, India, Japan, and New Zealand. The sequence of the isolate from Thailand is the only one deposited in GenBank, and is identical to the sequence of the California isolate.

Official Control: There is no record of official control against this pathogen.

California Distribution: The pathogen has only been detected in greenhouses of two nurseries at two different locations in Santa Barbara County.

California Interceptions: There are no records of Podosphaera caricae-papayae having been intercepted in papaya imported to California.

The risk Podosphaera caricae-papayae would pose to California is evaluated below.

Consequences of Introduction:

1) Climate/Host Interaction: Evaluate if the pest would have suitable 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 Low (1) – Of what is currently known, Podosphaera caricae-papayae will only infect papaya and therefore, is limited to wherever papaya is cultivated. In California, where there is no major cultivation of papaya, plants are propagated in greenhouses for fruit production and ornamental plantings in residential and urban environments of southern counties. As evident in the recent detection in Santa Barbara, the pathogen is capable of establishing in nursery grown papaya.

2) Known Pest Host Range: Evaluate the host range of the pest:

– Low (1) has a very limited host range
– Medium (2) has a moderate host range
– High (3) has a wide host range

Risk is Low (1) – The host range is limited to Carica papaya (papaya).

3) Pest Dispersal Potential: Evaluate the dispersal potential of the pest:

– Low (1) does not have high reproductive or dispersal potential
– Medium (2) has either high reproductive or dispersal potential
– High (3) has both high reproduction and dispersal potential

Risk is High (3) – Under suitable climate conditions, airborne conidia are produced in abundance and readily spread by wind currents to non-infected sites. Within and outside greenhouse environments, the pathogen is capable of rapidly spreading to non infested papaya plants as well as other sites where papaya is grown.

4) Economic Impact: Evaluate the economic impact of the pest to California using these criteria:

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 pathogen can potentially cause significant losses in plant growth and crop yield. Powdery mildew infections of papaya fruit could lower crop yield and value causing significant losses in production. This would result in loss of markets, and change in cultivation practices to prevent the spread of inocula to non-infected, healthy plants.

5) Environmental Impact: Evaluate the environmental impact of the pest on California using these criteria:

A. The pest could have a significant environmental impact such as lowering biodiversity, disrupting natural communities, or changing ecosystem processes.
B. The pest could directly affect threatened or endangered species.
C. The pest could impact threatened or endangered species by disrupting critical habitats.
D. The pest could trigger additional official or private treatment programs.
E. The pest significantly impacts cultural practices, home/urban gardening or ornamental plantings.

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) – Although limited to papaya, occurrence of the pathogen in nursery and outside environments could significantly impact home/urban gardening and/or ornamental plantings, as well as result in the imposition of additional official or private treatments to mitigate effects of infection.

Consequences of Introduction to California for Podosphaera caricae-papayae:

Add up the total score and include it here. (Score)

Low = 5-8 points
Medium = 9-12 points
High = 13-15 points

Total points obtained on evaluation of consequences of introduction of P. caricae-papayae to California = (11).

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). The pathogen was only detected within nursery greenhouses in Santa Barbara, California. Measures were taken to destroy infested plants.

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 = 10

Uncertainty:

To date, the detection of P. caricae-papayae in California is limited to two in-greenhouse sites in Santa Barbara County. There have not been any additional detections, surveys or reports of new infestations in papaya production nurseries and/or outside environments to provide further knowledge of the presence of this pathogen. Further comparative molecular analyses against reported international isolates of the pathogen may provide information of its global distribution and clarity of its taxonomic classification, however, it’s separation from P. xanthii (present in California) has already been proven (see ‘Background’).

While the host range and distribution of the pathogen within California is currently known to be limited, the potential of incurring significant damage due to infection by P. caricae-papayae places the limited distribution of instate papaya nursery ornamental and production plants at medium risk and, therefore, warrants assignment of a B rating. Future detections of P. caricae-papayae could indicate a wider distribution than presently known and result in a lower rating.

Conclusion and Rating Justification:

Based on the evidence provided above the proposed rating for Podosphaera caricae-papayae is B.

References:

Braun, U. and R. T. A. Cook. 2012. Taxonomic manual of the Erysiphales (Powdery Mildews). Centraalbureau voor Schimmelcultures, vol. 11, 707 p.

Cunningham, B and S. Nelson. 2012. Powdery mildew of Papaya in Hawai’i. College of Tropical Agriculture and Human Resources University of Hawai’I at Mānoa. Plant disease, PD-90.

Latham, S. 2014. Email to John Chitambar, CDFA: sent July 3, 2014.

Liberato, J. R., R. W. Barreto and R. P. Louro. 2004. Streptopodium caricae sp. nov., with a discussion of powdery mildews on papaya, and emended descriptions of the genius Streptopodium and Oidium caricae. Mycological Research 108:1185-1194.

Romberg, M. K. 2014. Email from M. K. Romberg, APHIS-USDA, to Suzanne Latham, CDFA: sent March 26, 2014.

Takamatsu, S., S. Ninomi, M. Harada and M. Havrylenko. 2010. Molecular phylogenetic analyses reveal a close evolutionary relationship between Podosphaera (Erysiphales: Erysiphaceae) and its rosaceous hosts. Persoonia, 24, 38-48.

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.