Peronospora belbahrii (Downy mildew of basil)

California Pest Rating for

Peronospora belbahrii

(Downy mildew of basil)

Pest Rating: C

PEST RATING PROFILE

Initiating Event:

During June 2014, Cheryl Blomquist, CDFA Plant Pathologist, detected Peronospora belbahrii in basil plants grown in a Nursery in Alameda County. The plants had been purchased from a different nursery in Sebastopol, Sonoma County. In 2008, the pathogen had been detected in basil plants produced in various nurseries. Trace-back investigation of the 2008 detections revealed that the seeds had originated in Italy. Presently, the origin of seeds cultivated in Sonoma County is not known. Peronospora belbahrii currently has a Q rating that is herein reassessed for the proposal of a permanent rating.

History & Status:

Background: Peronospora belbahrii is a fungal pathogen that causes downy mildew disease of basil (Ocimum spp. of the family Lamiaceae). Traditionally it was believed that the downy mildew disease of Lamiaceae, including the downy mildew of basil, was caused by a single species namely, P. lamii. However, that view has been proven inaccurate by several researchers, and Belbahri et al. (2005) showed through ITS sequencing that a then newly occurring fungal species on basil was different from P. lamii. Later, Thines et al. (2009) formally introduced this fungal species as P. belbahrii and distinguished it from a different closely related species that parasitizes sage (Salvia). They determined that P. belbahrii isolates infected both basil and coleus (Solenostemon sp.), and while those isolates seemed closely related, Thines et al. (2009) refrained from distinguishing them as two separate species until further studies have been conducted (albeit depending on the taxonomical concept taken, downy mildew on basil and coleus may be attributed to one or two different species). Downy mildew of basil was first reported from Africa from where it is assumed to have originated on sweet basil (Ocimum basilicum). Later, it was reported from Europe. It continued to spread globally and is considered a relatively new disease of basil in the United States.

Disease cycle: Peronospora belbahrii is an oomycete belonging to the family Peronosporaceae. Generally, downy mildews overwinter as thick-walled resting spores called oospores that are produced through the fertilization of two mating types. However, currently only one mating type of P. belbahrii has been found in the USA. Consequently, no oospores are formed and the pathogen is unable to survive harsh cold winters (Grabowski, 2014). It is likely that the pathogen survives as mycelium and/or condia (spores) in infected plant buds, plant debris, leaf tissue and shoots. Peronospora belbahrii thrives in warm, humid climates. However, it can tolerate cool weather, infect and produce conidia at temperatures as low as 59°F (Grabowski, 2012). Generally, under favorable weather conditions, condia are carried by wind or water to wet leaves near the ground where they infect through stomata of the lower leaf surface. A conidium germinates via a germ tube that grows through leaf stomata into intercellular spaces within the leaf tissue and eventually penetrates plant cells through special structures called haustoria. Developing hypha that spreads intercellularly forms a cushion of mycelia just below the stomata. From this cushion, conidophores arise and emerge through stomata. At their tips, conidia (sporangia/spores) are produced simultaneously and are carried by wind and rain to new infection sites of the same or different plant.

Dispersal and spread: The pathogen is seed borne and can also be spread through contaminated plant cuttings, transplants, and fresh leaves. Also, it produces airborne conidia (spores) can disperse and be carried by moist winds. It can also be present in soil associated with host and non-host plants and therefore, can spread by any means that aids in the movement of soil and/or water from infected plants to non-infected ones.

Hosts: Ocimum spp. (basil, including culinary and ornamental varieties), Solenostemon sp. coleus (Thines et al., 2009), Agastache sp. hyssop (Henricot et al., 2009).

Symptoms and damage potential: Infection starts on lower leaves and progresses upwards. Initially symptoms appear as yellowing (slightly chlorotic) of affected leaves with the veins remaining green. Following this, the central portion of a chlorotic lesion may become necrotic; slight curvature of leaves occurs followed by premature leaf fall. In some cases entire area of the leaf surface is affected. Grey to brown, furry or downy (conidia) growth is apparent on underside of symptomatic leaves giving the leaves a dirty appearance. These symptoms may sometimes occur on upper surfaces of leaves.

Under cool dry conditions infected transplants and leaves may not exhibit symptoms (Grabowski, 2012). Basil plants not showing symptoms at harvest are capable of developing symptoms during transport (Roberts et al., 2009). Chen et al. (2010) noted that in Taiwan, the pathogen caused chlorosis and leaf shrinkage on basil in the field, but did not cause any symptom on coleus.

Downy mildew is one of the most destructive diseases of sweet basil which is grown as a specialty crop in greenhouses and production fields in several regions of the United States and other countries. Once infected, basil plants are no longer marketable. Under favorable weather conditions complete yield loss can be expected. In Florida, almost 100% incidence of the disease occurred causing complete yield loss in the field for fresh and potted herbs markets (Roberts et al., 2009). The frequency of disease occurrence and the percentage of infected leaf area were 80-90% and 17-20% respectively on full-grown basil leaves grown a greenhouse in Hungary (Nagy & Horvath, 2011).

Worldwide Distribution: Basil downy mildew has been reported from several countries and continents including, Argentina (greenhouse), Belgium, Benin, Cameroon, Canada, Cuba, Cyprus, France, Switzerland, Hungary, Israel, Iran, Italy, New Zealand, South Africa, Taiwan, Tanzania, Uganda, United Kingdom (Zhang et al., 2012; CABI, 2014; EPPO, 2014; Henricot et al., 2009).

In the United States, the pathogen was first discovered in Florida in 2007 (Roberts et al., 2009). Since then, the disease has been found throughout the eastern United Sates and commercial basil production regions in the Midwest and California, namely, Alabama, California, Connecticut, Delaware, Georgia, Hawaiian Islands, Illinois, Indiana, Kansas, Kentucky, Massachusetts, Missouri, Minnesota, New Jersey, New York, North Carolina, Ohio, Oregon, Pennsylvania, South Carolina, Texas, Vermont, Virginia and Wisconsin (Zhang et al., 2012; Grabowski, 2012; PNW, 2014).

Official Control: Currently, the pathogen is not officially controlled in the United States Department of Agriculture.

California Distribution: In California, the pathogen has been found in nursery and/or field environments of Alameda, San Diego, San Joaquin, Ventura, and Southern Valley Counties.

California Interceptions: Recently P. belbahrii was detected in basil plants grown in a nursery in Alameda County. The plants had originated from a different nursery in Sonoma County (see ‘Initiating Event’).

The risk Downy mildew of basil 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 Medium (2): As evident from current distribution records in California, Peronospora belbahrii – causing downy mildew of basil – is able to develop in warm (not hot), humid weather conditions and can tolerate cool climates as well. Interestingly, in San Diego County, basil was drip irrigated and grown in a hot inland valley. Under those conditions the disease still spread, possibly due to the humid microenvironment that developed in a basil field where plants were grown close together so that dew was produced when evening temperatures dropped.

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

– Low (1) has a very limited host range.

– Medium (2) has a moderate host range.

– High (3) has a wide host range.

Risk is Low (1): The host range is limited to basil, coleus and hyssop. Although several species and varieties of basil exist, the host range is thus far limited to three plant genera.

3) Pest Dispersal Potential: Evaluate the natural and artificial dispersal potential of the pest. 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): Conidia are easily produced simultaneously and in abundance. The pathogen is seed borne as well as transmitted via infected plant material; conidia are dispersed by winds, water and associated soil.

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): Presence of the pathogen in field and/or greenhouse environments can significantly lower crop value and yield. Infected, symptomatic plants are not marketable resulting in total loss in recovery of production costs. Markets for crop sale are directly affected. Normal cultivation practices, including delivery and supply of irrigation water, would need to be altered to prevent spread of the pathogen.

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

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. Score:

– 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 Medium (2): Home/urban gardening of basil and cultivation of coleus and hyssop ornamental plants can be significantly impacted if the pathogen is present in private home garden environments.

Consequences of Introduction to California for Downy mildew of basil:

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 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 High (-3): To date, the pathogen has been detected in more than four non contiguous 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 = 8.

Uncertainty:

Surveys for the detection of P. belbahrii have not been conducted to fully establish its presence in field environments within California. Results of future survey may result in further detections of the pathogen in new locations. This will only strengthen the current proposed C rating. However, due to the devastating effects on crop production, direct action is necessary to mitigate risk of establishment and spread of P. belbahrii on host plants particularly grown in nursery environments.

Conclusion and Rating Justification:

Based on the evidence provided above the proposed rating for Downy mildew of basil is C.

References:

Belbahri, L., G. Calmin, J. Pawlowski and F. Lefort. 2005. Phylogenetic analysis and real time PCR detection of a presumbably undescribed Peronospora species on sweet basil and sage. Mycological Research, 109:1276-1287.

Blomquist, C.L., S. Rooney-Latham and P. A. Nolan. 2009. First report of downy mildew on field-grown sweet basil caused by a Peronospora sp. in San Diego County, California. Plant Disease 93:968.

CABI. 2014. Pernospora belbahrii data sheet report (basic). Crop Protection Compendium. http://www.cabi.org/cpc/datasheetreport?dsid=118352.

Chen, C. H., J. H. Huang, J. H. and T. F. Hsieh. 2010. First report of Peronospora belbahrii causing downy mildew on basil. Plant Pathology Bulletin, 17:177-180.

EPPO. 2014. Peronospora belbahrii (PEROBE). PQR database. Paris, France: European and Mediterranean Plant Protection Organization. http://www.newpqr.eppo.int.

Grabowski, M. 2012. Basil Downy Mildew Peronospora belbahrii. Regents of the University of Minnesota. University of Minnesota Extension. http://www.extension.umn.edu/garden/yard-garden/vegetables/basil-downy-mildew/docs/basil-downy-mildew-pub.pdf.

Henricot, B., J. Denton, J. Scarce, A. V. Barnes and C. R. Lane. 2009. Peronospora belbahrii causing downy mildew disease on Agastache in the UK: a new host and location for the pathogen. New Disease Reports, 20:26.

Nagy, G. and A. Horvath. 2011. Occurrence of downy mildew caused by Peronospora belbahrii on sweet basil in Hungary. Plant Disease, 95:1034.1.

PNW. 2014. Basil, Sweet (Ocimum basilicum) – Downy Mildew. Pacific Northwest Plant Disease Management Handbook. http://pnwhandbooks.org/plantdisease/basil-sweet-ocimum-basilicum-downy-mildew.

Roberts, P. D., R. N. Raid, P. F. Harmon, S. A. Jordan and A. J. Palmateer. 2009. First report of Downy Mildew caused by a Peronospora sp. on basil in Florida and the United States. Plant Disease 93: 199.

Thines, M., S. Telle, S. Ploch and F. Runge. 2009. Identity of the downy mildew pathogens of basil, coleus and sage with implications for quarantine measures. Mycological Research 113:532-540.

Wyenandt, C. A., J. E. Simon, M. T. McGrath and D. L. Ward. 2010. Susceptibility of basil cultivars and breeding lines to downy mildew (Peronospora belbahrii). 2010. HortScience 45:1416-1419.

Zhang, S. Z. Mersha, P. D. Roberts and R. Raid. 2012. University of Florida, IFAS Extension Document PP271. http://edis.ifas.ufl.edu/pdffiles/PP/PP27100.pdf.

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.