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Candidatus Liberibacter solanacearum Liefting, Perez-Egusquiza & Clover, 2009

December 8, 2016 Admin

California Pest Rating for

Candidatus Liberibacter solanacearum Liefting, Perez-Egusquiza & Clover, 2009

Pest Rating: B

PEST RATING PROFILE

Initiating Event:

None. The risk of entry and establishment of Ca. Liberibacter solanacearum in California is assessed and a permanent rating is proposed.

History & Status:

Background: Candidatus Liberibacter solanacearum was first identified in 2008 simultaneously in the United States and New Zealand. In New Zealand, Liefting et al., (2008, 2009), detected the bacterial pathogen first in tomato and pepper and then in potato and other solanaceous plants. The pathogen was tentatively named Candidatus Liberibacter solanacearum. In the United States, the pathogen was detected in tomato plants and the potato/tomato psyllid Bactericera cockerelli and tentatively named Candidatus Liberibacter psyllaurous because of its association with psyllid yellows (Hansen et al., 2008; CABI, 2016). Ca. L. psyllaurous is now considered a synonym of Ca. L. solanacearum. The pathogen is the cause of ‘Zebra chip disease’ in potatoes, named because of the presence of dark stripes and blotches that develop from the rapid oxidative darkening of freshly cut tubers and become more distinct after frying infected potato chips (Crosslin, 2009). Zebra chip disease of potatoes was first observed in the 1990s in Mexico and parts of Central America. Foliar symptoms resembled those caused by phytoplasmas. The disease is now widespread in south-western, central, and north-western USA, Mexico, Central America, New Zealand and restricted regions within Europe (see “Worldwide Distribution’ below).

In the United States, zebra chip disease of potatoes was first identified in 2000 in commercial potato fields in Texas and by 2004-2005, was reported to cause serious economic damage in parts of Southern Texas. By 2007, zebra chip disease was observed in Nebraska, Colorado, Kansas, New Mexico, Arizona, Nevada, and California causing losses in the millions of dollars to potato producers and processors in affected regions. Infested fields were often abandoned (Munyaneza et al., 2007b).

In California, while potato crops exhibiting symptoms of zebra chip disease were observed previously (Munyaneza et al., 2007b), the bacterium Ca. L. psyllaurous was first identified in 2009 from diseased potatoes grown in commercial fields in Lancaster, Los Angeles County (Crosslin, 2009; Crosslin et al., 2010). Since then, the presence of Ca. L. solanacearum was also detected, in plant tissue and psyllid vector with real time PCR, in Riverside, Santa Barbara, Orange, and San Diego Counties (Trumble, 2015). Substantial crop losses have occurred in southern California that resulted in abandonment of commercial fields, decline in potato and tomato productions, and significant increases in disease control costs (Trumble, 2015). The pathogen is considered to be of rare occurrence and less of a problem in northern California (Nunez, 2015; Davis, 2015). The psyllid can be found throughout southern California, in Kern County, on the coast up to Sacramento, and within the Sacramento Valley. In the Sacramento area, dense psyllid populations have been reported on bell peppers. For reasons not known, the peppers do not show symptoms of Ca. L. solanacearum (unlike peppers infested with psyllids in Utah, Arizona, New Mexico and New Zealand), and therefore, the presence of the bacterial pathogen in the populations cannot be definitely stated (Trumble, 2015). Also, the psyllid vector is kept in control by growers, through routine insecticide applications primarily against aphid-vectored viruses (Nunez, 2015).

Biology: Candidatus Liberibacter solanacearum is a phloem-limited, insect hemolymph-limited, gram-negative, unculturable bacterium that is primarily spread from infected to healthy plants by psyllid insect vectors. Presently, there are five known geographic haplotypes (a specific group of genes that are inherited together from a single parent) designated A, B, C, D, and E. Haplotypes A and B are associated with Bactericera cockerelli and the diseases caused by this bacterium in potatoes and other solanaceous plants. Haplotypes C and D are associated with diseased carrots, and Trioza apicalis and Bactericera trigonica respectively, and haplotype E is associated with diseased celery and carrot. The five haplotypes are not yet known to elicit biological differences in plant or insect hosts. Haplotype A has been found primarily from Central to North America (from Honduras and Guatemala through western Mexico to Arizona, California, the Pacific Northwest) and in New Zealand. Haplotype B has been found in Mexico and North America (from eastern Mexico and northwards through central USA through Texas). Some overlap of haplotypes A and B occurs in Texas, Kansas, and Nebraska. Haplotype C occurs in Finland, Sweden, and Norway and is associated with T. apicalis. Haplotype ‘D’ was found in mainland Spain and the Canary Islands. Haplotype E is present in mainland Spain, France, and Morocco (EPPO, 2013; Tahzima et al., 2014; Teresani et al., 2014, 2015). Teresani et al., (2015) recently reported two additional new psyllid species, Bactericera tremblayi and B. nigricornis, as potential vectors of Ca. L. solanacearum that were detected with B. trigonica during surveys conducted from 2011 to 2014 in carrot, celery and potato plots in mainland Spain and the Canary Islands.

While there is not much known on the effects of environment on Ca. L. solanacearum, temperature is known to have a significant effect on the development of this bacterial pathogen. Compared to the citrus greening Huanglongbing Liberibacter species, Ca. L. solanacearum appears to be heat sensitive and does not tolerate temperatures above 32°C

Dispersal and spread: Ca. L. solanacearum is transmitted by its psyllid insect vector, Bactericera cockerelli, in a persistent (transovarially or vertically) way and during feeding on infected plant hosts (horizontally). However, vertical transmission of the pathogen in the other psyllid species, Bactericera trigonica and Trioza apicalis, is currently not known. The pathogen is also spread by grafting and infected plants, but not true seed (EPPO, 2013). However, Bertolini et al., (2014) reported the detection of Ca. L. solanacearum in carrot seeds using real-time PCR thereby, indicating that seed transmission is involved in the natural spread of the bacterium via carrot seed in distant regions and countries in Europe. Usually infected seed potatoes do not germinate but may occasionally produce infected plants which are often weak and short-lived and therefore, not a significant mode for spreading the disease (EPPO, 2013).

Hosts: Hosts are included in the plant families Apiaceae and Solanaceae. Main hosts include, Capsicum annuum (bell pepper), Solanum lycopersicum (tomato), S. tuberosum (potato), and Datura stramonium (jimsonweed). Other wild and incidental hosts include Solanum melongena (eggplant), S. pseudocapsicum (Jerusalem-cherry), S. dulcamara (climbing nightshade), Cyphomandra betacea (syn. Solanum betacea; tree tomato/tamarillo), Apium graveolens (celery), Daucus carota (carrot), Physalis peruviana (Cape gooseberry/tomatillo), and Nicotiana tabacum (tobacco) (CABI, 2016, EPPO, 2016).

Symptoms: Characteristic above-ground symptoms in potato and other solanaceous host plants include stunting, erectness of new foliage, chlorosis and purpling of foliage with basal cupping of leaves through entire plant, resetting due to shortened and thickened terminal internodes, enlarged nodes, axillary branches or aerial tubers, leaf scorching, disruption of fruit set, and production of numerous small, misshaped and poor quality fruits. Below-ground symptoms in potato include collapsed stolons, browning of vascular tissue concomitant with necrotic flecking of internal tissues and streaking of the medullary ray tissues, all of which can affect the entire tuber. These symptoms become more distinct upon frying and potato chips processed from affected tubers show very dark blotches, stripes or streaks thereby making them unacceptable for marketing. It is due to the symptoms produced in potato tubers that the disease was named ‘zebra chip’ (EPPO, 2013).

Damage Potential: In potato, plant growth is affected. Potato chips produced from zebra ship-infected tubers have dark stipes that are more distinct upon frying and therefore, not commercially acceptable. Infected tubers often do not sprout or produce hairy sprouts and weak plants. Damage is also caused to other economically important solanaceous plants including tomato, pepper, eggplant, tamarillo, and tobacco. Fields with infected crops may be rejected resulting in their abandonment (EPPO, 2013). Ca. Liberibacter solanacearum can cause significant damage to crop quality and yield. In the Americas and New Zealand, losses in millions of dollars have been caused by the pathogen and psyllid complex and to the carrot industry in Europe (Crosslin et al., 2010; Munyaneza 2007a, 2007b). In Texas and New Zealand, annual potato yield losses at approximately US $22 million and US $40 million respectively were due to Ca L. solanacearum (Soliman, 2012 in CABI, 2016). In Europe, up to 100% crop losses in carrot production due to Ca. L solanacearum – infected carrot psyllid were reported (CABI, 2016).

Worldwide Distribution: Africa: Morocco; North America: Mexico, USA; Europe (restricted distributions within): Finland, Germany (few occurrences), Norway, Spain, Spain – Canary Islands, Sweden; Central America: Guatemala, Honduras, Nicaragua; Oceania: New Zealand (CABI, 2016; EPPO, 2013, 2016).

In Europe, Ca. L. solanacearum has not been detected in potato and tomato crops but has been detected mainly in carrot crops and to a lesser extent in celery in association with other psyllid species, Bactericera trigonica and Trioza apicalis (EPPO, 2013). Ca. L. solanacearum is considered “transient, under eradication” in Austria and France.

In the USA, the pathogen is present in Arizona, California, Colorado, Idaho, Kansas, Montana, Nebraska, Nevada, New Mexico, North Dakota, Oregon, Texas, Utah, Washington, and Wyoming (CABI, 2016; EPPO, 2016).

Official Control: Candidatus Liberibacter solanacearum is on the Harmful Organisms Lists for Argentina, Australia, Brazil, Chile, Costa Rica, Guatemala, Honduras, Republic of Korea, Panama, and Taiwan (USDA PCIT, 2016).

California Distribution: Los Angeles, Riverside, Orange, San Diego, and Santa Barbara Counties. The pathogen is considered to be of rare occurrence in northern California.

California Interceptions: There are no reports of the detection of Ca. Liberibacter solanacearum in plant shipments imported to California.

The risk Ca. Liberibacter solanacearum 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: 3

– 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): Ca. L. solanacearum appears to be heat sensitive and does not tolerate temperatures above 32°C. Presently, its distribution has been confirmed in some counties in southern California, while its occurrence in northern California is rare. While the potato/tomato psyllid vector can be found on Ca L. solanacearum host plants throughout southern California, in Kern County, on the coast up to Sacramento, and within the Sacramento Valley, the presence of the bacterial pathogen has only rarely been found in the northern regions. Furthermore psyllid populations are kept in check by growers through insecticides routinely applied primarily to control aphid-vectored viruses. In the absence of vector control measures, the bacterial pathogen is expected to establish a widespread distribution on prime hosts including, tomatoes, potatoes, peppers and eggplant.

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

Score: 2

– 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): The pathogen has a medium host range that includes major host plants such as tomatoes, potatoes, and peppers, cultivated under significant acreage in California.

3) Pest Dispersal Potential: Evaluate the natural and artificial dispersal potential of the pest.

Score: 3

– 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): Ca. L. solanacearum is primarily transmitted by its psyllid insect vector, Bactericera cockerelli. The bacterium has high reproduction and is dependent primarily on its vector for short and long-distance spread. The bacterium is also spread by grafting and infected plants. [Usually infected seed potatoes do not germinate but may occasionally produce infected plants which are often weak and short-lived and therefore, not a significant mode for spreading the disease.]

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): Ca. L. solanacearum causes zebra chip disease of potatoes and has resulted in significant crop damage and economic loss in production and marketability. Significant losses have also been caused in other economic host crops. The pathogen is vectored by the potato/tomato psyllid vector in California.

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

The pest could have a significant environmental impact such as lowering biodiversity, disrupting natural communities, or changing ecosystem processes.

The pest could directly affect threatened or endangered species.

The pest could impact threatened or endangered species by disrupting critical habitats.

The pest could trigger additional official or private treatment programs.

The pest significantly impacts cultural practices, home/urban gardening or ornamental plantings.

Score the pest for Environmental Impact.

Score: 2

– 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): Infestations of the bacterial pathogen could significantly impact home/urban gardening.

**Consequences of Introduction to California for Candidatus Liberibacter solanacearum:**

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 = 13.

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: -1

-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): Presently, Ca. L. solanacearum is distributed within few counties of southern California, namely, Los Angeles, Riverside, Orange, San Diego, and Santa Barbara Counties and is considered to be only of rare occurrence in northern 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.

Uncertainty:

Not much is known on the effects of environment on Ca. L. solanacearum. Also, its presence in vector populations in northern California cannot be definitively stated.

Conclusion and Rating Justification:

Based on the evidence provided above the proposed rating for the zebra chip pathogen, Ca. Liberibacter solanacearum is B.

References:

Bertolini, E., G. R. Teresani, M. Loiseau, F. A. O. Tanaka, S. Barbé, C. Martínez, P. Gentit, M. M. López, and M. Cambra. 2014. Transmission of ‘Candidatus Liberibacter solanacearum’ in carrot seeds. Plant Pathology: http://dx.doi.org/10.1111/ppa.12245 .

Crosslin, J. M. 2009. First report of ‘Candidatus Liberibacter psyllaurous’ in zebra chip symptomatic potatoes from California. Plant Disease 93: 551. http://dx.doi.org/10.1094/PDIS-93-5-0551B .

Crosslin, J. M., J. E. Munyaneza, J. K. Brown, and L. W. Liefting. 2010. Potato zebra chip disease: A phytopathological tale. Online. Plant Health Progress doi: 10.1094/PHP-2010-0317-01-RV.

Davis, M. 2015. Email from M. Davis, Professor Emeritus, Plant Pathology Department, UC Davis, to J. Chitambar, Primary Plant Pathologist/Nematologist, CDFA, sent Wednesday, November 11, 2015, 7:13:45 pm.

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

EPPO. 2013. Candidatus Liberibacter solanacearum. EPPO Data Sheets on pests recommended for regulation, European and Mediterranean Plant Protection Organization. Bulletin OEPP/EPPO Bulletin 43: 197-201. DOI: 10.1111/epp.12043.

EPPO. 2016. Liberibacter solanacearum (LIBEPS). New PQR database. Paris, France: European and Mediterranean Plant Protection Organization. http://newpqr.eppo.int

Hansen, A. K., J. T. Trumble, R. Stouthamer, and T. D. Paine. 2008. A new huanglongbing species, “Candidatus Liberibacter psyllaurous,” found to infect tomato and potato, is vectored by the psyllid Bactericera cockerelli (Sulc). Applied and Environmental Microbiology, 74(18):5862-5865. http://aem.asm.org .

Liefting, L. W., Z. C. Perez-Egusquiza, G. R. G. Clover, and J. A. D. Anderson. 2008. A new ‘Candidatus Liberibacter’ species in Solanum tuberosum in New Zealand. Plant Disease, 92(10):1474.

Liefting, L. W., B. S. Weir, S. R. Pennycook, and G. R. G. Clover. 2009. ‘Candidatus Liberibacter solanacearum’, associated with plants in the family Solanaceae. International Journal of Systematic and Evolutionary Microbiology, 59(9):2274-2276.

Munyaneza, J. E. 2012. Zebra chip disease of potato: biology, epidemiology and management. American Journal of Potato Research 89: 329-350. http://dx.doi.org/10.1007/s12230-012-9262-3.

Munyaneza, J. E., J. M. Crosslin, and J. E. Upton. 2007a. Association of Bactericera cockerelli (Homoptera: Psyllidae) with “zebra chip”, a new potato disease in southwestern United States and Mexico. Journal of Economic Entomology 100, 656–663.

Munyaneza, J.E., J. A. Goolsby, J. M. Crosslin, and J. E. Upton. 2007b. Further evidence that zebra chip potato disease in the lower Rio Grande Valley of Texas is associated with Bactericera cockerelli. Subtropical Plant Science 59, 30–37.

Nunez, J. 2015. Email from J. Nunez, Vegetable/Plant Pathology Farm Advisor, UC Cooperative Extension, to J. Chitambar, Primary Plant Pathologist/Nematologist, CDFA, sent Wednesday, November 11, 2015, 4:35 pm.

Tahzima, R., M. Maes, E. H. Achbani, K. D. Swisher, J. E. Munyaneza, and K. De Jonghe. 2014. First Report of “Candidatus Liberibacter solanacearum’ on carrot in Africa. Plant Disease 98: 1426. http://dx.doi.org/10.1094/PDIS-05-14-0509-PDN .

Teresani, G. R., E. Bertolini, A. Alfaro-Fernández, C. Martinez, F. A. O. Tanaka, E. W. Kitajima, M. Roselló, S. Sanjuán, J. C. Ferrándiz, M. M. López, M. Cambra, and M. I. Font. 2014. Association of ‘Candidatus Liberibacter solanacearum’ with a vegetative disorder of celery in Spain and development of a real-time PCR method for its detection. Phytopathology 104: 804-811.

Teresani, G., R. Hernández, E. Bertolini, F. Siverio, C. Marroquin, J. Molina, A. Hermoso de Mendoza, and M. Cambra. 2015. Search for potential vectors of ‘Candidatus Liberibacter solanacearum’: population dynamics in host crops. Spanish Journal of Agricultural Research, 13 (1): e10-002. http://dx.doi.org/10.5424/sjar/2015131-6551 .

Trumble, J. T. 2015. Email from J. T. Trumble, Distinguished Professor of Entomology, University of California, Riverside, to J. Chitambar, Primary Plant Pathologist/Nematologist, CDFA, sent Thursday, November 12, 2015, 5:28:41 pm.

USDA PCIT. 2016. USDA Phytosanitary Certificate Issuance & Tracking System. https://pcit.aphis.usda.gov/PExD/faces/ReportHarmOrgs.jsp.

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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Pest Rating: B

Posted by ls

Bacteria, Plant Pathogens

Xanthomonas arboricola pv. pruni (Smith) Vauterin, Hoste, Kersters & Swings

June 1, 2015 Admin

California Pest Rating for

Xanthomonas arboricola **pv. pruni (Smith) Vauterin, Hoste, Kersters & Swings**

Pest Rating: B

PEST RATING PROFILE

Initiating Event:

In September 2013, CDFA plant pathologist, Luci Kumagai, identified Xanthomonas arboricola pv. pruni associated with symptomatic almond seedlings that were submitted by Sierra Gold Nursery in Sutter County to the CDFA Plant Pathology Laboratory. David Marion, CDFA environmental scientist, surveyed the nursery shade house where the trees were housed and determined that only Monterey Almond trees exhibited symptoms of bacterial canker. Subsequently, in line with CDFA’s current Q rating of X. arboricola pv. pruni and ‘Nursery Standard of Cleanliness’, the lot of affected almond trees was destroyed and other Prunus spp. in the nursery were protected from further potential infection. Near about that time, the pathogen was found in commercial almond orchards in a few counties in northern California, thereby marking its first non-official detection in the State. The detection of the associated disease was reported by the University of California Cooperative Extension Farm Advisor for Stanislaus County. In view of the recent finds, the current temporary rating is herein assessed for the proposal of a permanent rating.

History & Status:

Background: Xanthomonas arboricola pv. pruni is a bacterial pathogen that attacks only Prunus spp. causing disease commonly known by various names: bacterial canker of stone fruit, bacterial leaf spot of stone fruit, bacterial shot-hole of stone fruit, and black spot of stone fruit. The bacterium belongs to the family Xanthomonadaceae of the order Xanthomonodales. No strains have been reported, however, difference in virulence to peach, plum and apricot have been noted (Du Plessis, 1988). The species was first described in North America (Michigan) in 1903 on Japanese plum, but it not clear if it spread from there throughout the world or if it naturally has a wide geographical range. In California, it is a relatively new disease of almonds (UCIPM, 2013).

Disease cycle: On Prunus species, the pathogen overwinters in plant tissues such as buds, protected areas (cracks in the bark), and in leaf scars. On almonds it overwinters on fruit mummies and twig cankers. On plum and apricot, cankers formed during the preceding season continue to develop in spring and provide a source of inoculum. During late winter as temperatures warm, peach leaf and flower buds swell, and as new tissue growth initiates, bacteria multiply and cause the epidermis to rupture, forming a lesion or spring canker. Bacteria are spread from cankers or mummified fruit to newly emerging leaves by dripping dew and splashing and/or wind-blown rain. Infection takes place through natural openings or wounds. High moisture conditions favor leaf and fruit infections. Severe infection is favored by warm temperatures (19-28°C), light frequent rainfall and fairly heavy winds and dew. Following foliar infection, cankers develop in the green shoot tissue, but usually become sealed off by formation of a periderm barrier layer. Also, cankers tend to dry out during the summer months thereby reducing viability of bacteria. For that reason, twig cankers produced in plum and peach during the summer are not considered important overwintering sites or sources of inoculum for spring infections. Generally, late shoot infections that occur just before leaf fall in autumn provide the primary inoculum source for the following spring (CABI, 2014; UCIPM, 2013).

Hosts: Xanthomonas arboricola pv. pruni attacks only Prunus species, in particular fruit crops such as almonds, peaches, cherries, plums, apricots, P. salicina (Chinese/Japanese plum), and ornamental species of Prunus including P. davidiana (Chinese wild peach), Japanese apricot (P. mume), and P. laurocerasus (cherry laurel). Generally, species of the Sino-Japanese group (P. japonica and P. salicina) are more susceptible than European plums (CABI, 2014; EPPO, 2013)

Symptoms: Symptoms may vary depending on the infected plant host and plant part.

On peach leaves, infection is first apparent on the lower leaf surface as small, pale green to yellow, circular or irregular areas with a light tan center. These spots become apparent on the upper surface as they enlarge, becoming angular and darken to deep-purple, brown or black. Tissue immediately surrounding the diseased spots becomes yellow. The spots may darken before they drop out giving a shot-hole appearance. Usually, spots are concentrated toward the leaf tip as bacteria accumulate in that area with droplets of rain or dew. Bacterial ooze may exude from the spots. In severe infections defoliation may occur. On peach fruit, small, sunken circular spots with frequently water-soaked margins or light green halos appear on the surface. Pitting and cracking occur near the spots as the fruit enlarges. Gum may exude from bacterial wounds, especially after heavy rains. Spring cankers appear on the top part of overwintering twigs before green shoots are produced. These cankers initiate as small, water-soaked slightly darkened superficial blisters that extend 1-10 cm along the length of the twig or girdle it causing tip death or “black tip injury’. The area below the dead tip harbors the bacteria. Twigs that get infected late in season result in ‘summer cankers’ which are dark purple spots surrounding lenticels that later dry out and become limited, dark, sunken, circular to elliptical lesions.

On plum leaves: the shot-hole effect is more pronounced than on peach leaves. On plum fruit symptoms vary from large sunken, black lesions to small pit-like lesions. On plum and apricot, twig cankers are perennial developing on 2-3 year old twigs. As a result, deep-seated cankers are formed in the inner bark thereby deforming and killing twigs.

On cherry leaves symptoms develop similar to peach but are rarely of importance. Fruit may be distorted and bacteria usually internally inhabit fruit pulp.

On almond: In California, damage has been predominant on the ‘Fritz’ variety however similar damage has been observed by researchers on ‘Monterey’, ‘Padre’, and ‘Nonpareil’ varieties (Holtz et al., 2013). Symptoms on leaves, twigs and fruit are similar to those produced on peach. Symptoms on infected almond nuts include the production of amber colored gum from spots on the hull which internally reveals a lesion. Lesions may enlarge, become sunken and orange in color, or exude an orange slime. Furthermore, infected nuts may stick on spurs and be close to mummified, lesion nuts of the previous year. Leaves may have spots, turn yellow and drop prematurely. Twigs may have lesions or cankers.

Damage Potential: The pathogen is capable of causing severe defoliation thereby weakening trees. The leader (i.e., the vertical stem at the top of the trunk) dies and fruit is reduced in size and often not marketable. Serious losses in peach (25-75%), plum and apricot production are reported from Australia, New Zealand, and the USA (CABI, 2014; EPPO, 2014). Damage to stone fruit is more severe where the latter are grown in light, sandy soils than in heavier soils (UCIPM, 2013).

Transmission: Local spread of the bacterial pathogen from cankers and mummified fruit is limited and dependent on dripping dew and splashing and/or wind-blown rain. Long distance spread, as in international trade, is through infected plantings, budwood, and fruit (except seeds).

Worldwide Distribution: Asia (China, India, Iran, Japan, Korea DPR, Korea Republic, Lebanon, Pakistan, Saudi Arabia, Taiwan, Tajikistan); Africa (South Africa, Zimbabwe); Europe (Bulgaria, France, Italy, Moldova, Montenegro, Netherlands, Romania, Russia (Far East, Southern), Slovenia, Spain, Switzerland, Ukraine); North America (Bermuda, Canada, Mexico, USA); South America (Argentina, Brazil, Uruguay); Oceania (Australia, New Zealand).

In the USA it is present in Alabama, Arkansas, California, Connecticut, Florida, Georgia, Idaho, Kentucky, Louisiana, Maryland, Michigan, Mississippi, Missouri, New Jersey, New York, North Carolina, Oregon, Pennsylvania, South Carolina, and Texas.

Official Control: Ten countries list X. arboricola pv. pruni on their “Harmful Organism Lists’ namely, Canada, Chile, Ecuador, Israel, Madagascar, Mexico, Morocco, New Caledonia, Peru, and Turkey. Whereas, 41 countries worldwide list X. campestris pv. pruni (synonym of X. arboricola pv. pruni) on their lists (USDA PCIT, 2014). Xathomonas arboricola pv. pruni is listed as an A2 quarantine pest by EPPO and of little economic importance in EPPO countries where it is present. Also, it is of quarantine significance for the Inter-African Phytosanitary Council/IAPSC (EPPO, 2014).

California Distribution: The bacterial spot pathogen is relatively in California. It has been found on almonds (mainly Fritz cultivar), in Colusa, Merced, Stanislaus, and San Joaquin Counties, as well as sweet cherry and other stone fruit crops in San Joaquin and Stanislaus Counties (UCIPM, 2013).

California Interceptions: The pathogen was recently intercepted in a nursery in Sutter County. The plants were destroyed (see ‘Initiating event’.)

The risk Xanthomonas arboricola pv. pruni 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 High (2): The pathogen is limited to high moisture and warm temperature conditions and regions for establishment.

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 Medium (2): The host range is limited to Prunus spp. stonefruit which is cultivated in vast acreage within California.

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 (2): The pathogen increases and tends to cause infections in spring and its spread to non-infected tissue is dependent on warm temperatures and wet conditions brought about by wind-driven rainfall, water-splash and dripping dew.

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): Infection of Prunus spp. could lower crop yield and value thereby resulting in a loss of market.

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): Infection of ornamental Prunus species, in particular could impact residential and commercial cultivation of ornamental and fruit trees, requiring cultural practices to remove infected plant parts and mummified fruit. In addition, official and private treatment programs may be needed to manage the pathogen.

**Consequences of Introduction to California for Xanthomonas arboricola pv. pruni:**

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 = 12

6) Post Entry Distribution and Survey Information: Evaluate the known distribution in California. Only official records identified by a taxonomic expert and supported by voucher specimens deposited in natural history collections should be considered. Pest incursions that have been eradicated, are under eradication, or have been delimited with no further detections should not be included. (Score)

-Not established (0) Pest never detected in California, or known only from incursions.
–Low (-1) Pest has a localized distribution in California, or is established in one suitable climate/host area (region).
-Medium (-2) Pest is widespread in California but not fully established in the endangered area, or pest established in two contiguous suitable climate/host areas.
-High (-3) Pest has fully established in the endangered area, or pest is reported in more than two contiguous or non-contiguous suitable climate/host areas.

Evaluation Low (-1): Xanthomonas arboricola pv. pruni has been detected on almond, sweet cherry and other stone fruit in four counties within the Central Valley of 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 = 11

Uncertainty:

To date, Xanthomonas arboricola pv. pruni has been detected mainly in almond orchards in four California counties. Targeted surveys for the detection of this relatively new pathogen may result in a wider distribution and range of host plants than currently known for the State. If that occurs, then a lower rating than that proposed here is probable. Therefore, diligent screenings and management of planting stock in nurseries will remain critical to mitigate risk of introduction of the pathogen to new, non-infected commercial production sites.

Conclusion and Rating Justification:

Based on the evidence provided above the proposed rating for Xanthomonas arboricola pv. pruni is B.

References:

CABI. 2014. Xanthomonas arboricola pv. pruni datasheet report. Crop Protection Compendium. www.cabi.org/cpc/

Du Plessis, H. 1988. Differential virulence of Xanthomonas campestris pv. pruni for peach, plum, and apricot cultivars. Phytopathology, 78 (10):1312-1315.

EPPO, 2014. Xanthomonas arboricola pv. pruni (XANTPR). PQR database. Paris, France: European and Mediterranean Plant Protection Organization. http://newpqr.eppo.int

Holtz, B., D. Doll, R. Duncan, J. Edstrom, T. Michailides, and J. Adaskaveg. 2013. http://www.ipm.ucdavis.edu/PDF/MISC/168605.pdf

UCIPM. 2013. Bacterial spot (Xanthomonas arboricola pv. pruni) University of California Agriculture & Natural Resources, UC IPM Online, Statewide Integrated Pest Management Program. http://www.ipm.ucdavis.edu/EXOTIC/bacterialspot.html

USDA PCIT. 2014. USDA Phytosanitary Certificate Issuance and Tracking System. Phytosanitary Export Database. https://pcit.aphis.usda.gov/PExD/faces/ReportHarmOrgs.jsp

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.

PEST RATING: B

Posted by ls

Bacteria, Plant Pathogens

Rhodococcus fascians

April 9, 2015 Admin

California Pest Rating for

Rhodococcus fascians

Pest Rating: C

PEST RATING PROFILE

Initiating Event:

On April 10, 2014, Dr. Jennifer Randall, Associate Research Professor, New Mexico State University, notified Nick Condos, Director, Plant Health and Pest Prevention Services, California Department of Food and Agriculture (CDFA), of her confirmed identification of the plant pathogen, Rhodococcus fascians associated with abnormal pistachio UCB-1 rootstocks from several orchards in California, as well as from a California nursery in Stanislaus County where the rootstocks had originated. Subsequent communications between CDFA and Craig Kallsen, Citrus and Pistachio Farm Advisor for Kern County, indicated that thousands of pistachio rootstocks obtained from the same nursery and planted in the southern San Joaquin Valley since 2011-2014, were performing poorly and exhibiting similar symptoms to those observed and tested positive for R. fascians by Dr. Randall. The Nursery rootstocks were obtained from the University of California Foundation Plant Services. Currently, R. fascians is a C rated pathogen by CDFA. The pest rating for the bacterial pathogen is herein reanalyzed under CDFA’s new pest risk analysis process to reaffirm its permanent rating.

History & Status:

Background: Rhodococcus fascians is a yellow-orange gram positive, aerobic, non-spore forming, non-motile bacteria with cell walls containing mycolic acid. They may have mycelial growth with fragmentation into rods or coccoid forms. The species was previously known as Corynebacterium fascians, but based on cell wall composition and DNA base composition the species was allocated to the genus Rhodococcus as R. fascians (Goodfellow 1984) in the order Actinomycetales and family Norcardiaceae.

Rhodococcus fascians is a plant pathogen that primarily lives on the exterior surfaces of plants but to a lesser degree, can also be found within plant cells. However, it is not considered to be systemic in plants. There are reports of several bacterial isolates identified as R. fascians that were found in various non-plant habitats – including ice and polar seawater, however, none of those isolates have been examined for phytopathogenicity (Putman & Miller, 2007). To cause plant disease, isolates of R. fascians must contain a plasmid with virulence genes for phytopathogenicity. Once R. fascians enters a plant, it can produce cytokinin and auxin and alter the normal ratio between the two hormones. This hormone production can block production of abscisic acid and gibberillic acid in plants.

Hosts: Rhodococcus fascians has a host range that includes 87 genera belonging to 40 plant families (CABI, 2014), however, this is considered a underestimated number. Putnam and Miller (2007) reported that the number of hosts should be expanded to at least 122 taxa. They considered several reported hosts as either unconfirmed, without published reports, of uncertain identity, or not naturally infected. Nevertheless, susceptible hosts include monocots and dicots, woody and herbaceous plants: mostly herbaceous perennial ornamentals, few woody plants, few vegetable crops and strawberry.

In California, detection of Rhodococcus fascians on ornamental plants has been reported (A. M. French: California plant disease host index 2^nd edition, updated January 11, 2014). However recently, Stamler et al., (2014) first reported the association of R. fascians on pistachio rootstocks.

Symptoms: Disease symptoms caused by R. fascians have often been overlooked and attributed to the crown gall bacterium Agrobacterium tumefaciens, viral infection, phytoplasmas, viroids, insect injury, nematodes, genetic causes, chemical substances produced by mixed bacterial populations, hormonal disturbance or crowding of plants in small plants (Putnam & Miller, 2007).

Symptoms caused by R. fascians range from witches’ broom and over-fasciation to leafy gall (Faivre-Amiot, 1967), similar to those caused by growth hormone imbalances. The level of symptom expression is dependent on the host plant genus, species and cultivar, age of the plant at time of infection (young growing tissue is more sensitive than older maturing tissue), bacterial strain (avirulent or virulent), and on plant growth conditions and the mode of infection. Symptoms in naturally infected plants include, proliferation of buds in leaf axils or at the base of stems; bunches of fleshy thick stems with misshapen and aborted leaves that develop at or below the crown of the host plant; proliferation of partially expanded buds called leafy galls; misshapen thickened leaves or shoots, expanded stems in ribbon-like growth or fasciation (formed when several hypertrophied shoots collapse); adventitious, amorphous growth from veins, petioles, or leaf edges; stunting; abnormal scales on bulbs; infrequent inhibition of root growth (Putnam & Miller, 2007). Generally, the root system is not affected, although severe infection can result in the main root becoming thickened with the inhibition of secondary roots (CABI, 2014).

In California, pistachio rootstocks associated with R. fascians exhibited symptoms that included shortened internodes, stunted growth, swollen lateral buds, bushy/bunchy growth pattern, twisted roots with virtually no lateral branching, and stem galls (Stamler et al., 2014).

Wounding of a plant host is not necessary for R. fascians infection and the pathogen does not preferentially enter the plant through natural opening. Symptoms can be produced when the bacteria are on the plant surface (CABI, 2014). However, R. fascians may have a prolonged epiphytic phase prior to symptom expression. As mentioned earlier, the presence of a plasmid with virulence genes is essential for phytopathogenicity (Putnam & Miller, 2007; Stamler et al., 2014). Symptoms are more severe and develop more rapidly when wounding occurs.

In nature, plant diseases caused by R. fascians requires moist conditions and moderate temperatures commonly occurring during late fall, mild winters and early spring, and can occur in acidic to slightly alkaline soils (Faivre-Amiot, 1967).

Transmission: The primary means of introduction of the bacterial pathogen to new, uninfested areas – fields or greenhouses, is most likely through contaminated planting material (Putnam & Miller, 2007; CABI, 2014). Putnam and Miller (2007) isolated pathogenic R. fascians from symptomatic in vitro plant tissue cultures. The pathogen is also known to be externally seed borne in some hosts including pea, nasturtium, greenhouse geranium, Marguerite daisy and carnation. Also, the pathogen is spread by irrigation water, water splash or rain and contaminated soil. The role of insects in natural disease transmission is not known, however under artificial conditions, transmission of R. fascians by aphids (Myzus persicae, M. ascalonicus) leading to disease has been reported (CABI, 2014).

Survival: It is not known if R. fascians truly resides in soil as do other members of the genus. However, it has been reported to survive in soils for 3 months or for longer periods of 4-5 years. Putnam & Miller (2007), hold that R. fascians survives in soil only as long as host tissue remains. Long term survival in natural environments is due to the ability of the pathogen to tolerate prolonged nutrient starvation. The detection of R. fascians in ice and polar seawater indicates that it can survive for very long periods at low temperatures, which further indicates that periods of chilling temperatures that are often required for certain plants will not kill the pathogen. The pathogen is also able to survive on rotation crops (CABI, 2014).

Worldwide Distribution: Rhodococcus facians is distributed in 22 countries in Europe, Asia (India, Iran, Israel), Africa (Egypt), Guatemala, Canada (British Columbia, Manitoba, Ontario, Saskatchewan), Mexico, Australia (New South Wales), New Zealand, and the USA (19 states, including California).

Official Control: R. fascians is a quarantine pest in Japan, Argentina and Peru (CABI, 2014).

California Distribution: While there has not been a statewide survey for R. fascians, early CDFA detection records of 1950-1983 document the pathogen being widespread in northern and southern, coastal counties, and northern mountain and foothill counties of California. The 2014 detection of the pathogen on pistachio includes fields and nursery in the Southern San Joaquin Valley (Kern, Tulare and Stanislaus Counties).

California Interceptions: CDFA records indicate detections of R. fascians in herbaceous ornamental plants grown in nurseries. It is quite likely that disease symptoms induced by R. fascians were either overlooked or attributed to other pathogens, chemical, hormonal or cultural factors and therefore, never recorded or recorded to a lesser extent than the actual impact caused by the pathogen.

The risk Rhodococcus fascians 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 High (3) – Given the already widespread distribution of R. fascians in California.

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 High (3) – R. fascians has a very broad host range of monocots and dicots, woody and herbaceous plants: mostly herbaceous perennial ornamentals, few woody plants, few vegetable crops and strawberry.

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) – As a bacterial pathogen, under optimal growth conditions of high moisture and moderate temperature, R. fascians primarily resides epiphytically on plants, has a high reproduction rate and readily spread through contaminated planting propagative material, seed, soil, and water.

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) – Serious recurring economic losses due to R. fascians can be incurred by the nursery industry. R. fascians infestations could lower crop yield and crop values thereby increasing production costs; infestation of nursery herbaceous plants and field crops could result in great loss in markets and alter normal cultural practices to insure pathogen-free propagative plant material.

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

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) – R. fascians may significantly impact ornamental cultivation and home/urban gardening and cultivation practices.

**Consequences of Introduction to California for Rhodococcus fascians:**

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 R. fascians to California = (14).

-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 (-3). R. fascians is ubiquitous and already established in diverse climate areas throughout 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 = 11

Uncertainty:

While there currently remains much unknown regarding the biology of R. fascians (Putnam & Miller, 2007), as well its pathogenic relationship with several hosts including pistachio (Stamler et al., 2014), it is not likely that additional information will qualify the pathogen for a higher rating. Indeed, revelation of further plant hosts, plasmid-borne virulent strains, and detection localities will only strengthen the C-rating of this already widespread pathogen, nevertheless, emphasizing its importance as a bacterial plant pathogen causing serious economic losses to plant production.

Conclusion and Rating Justification:

Based on the evidence provided above the proposed rating for Rhodococcus fascians is C.

References:

CABI. 2014. Rhodococcus fascians datasheet. http://www.cabi.org/cpc/datasheet/15332

Faivre-Amiot A, 1967. Quelques observations sur la presence de Corynebacterium fascians (Tilford) Dowson dans les cultures maraicheres et florales en France. Phytiatrie-Phytopharmacie, 16:165-176.

Goodfellow M, 1992. The family Nocardiaceae. In: Balows A, Trnper HG, Dworkin M, Harder W, Schleifer KH, eds. The Prokaryotes. Berlin, Germany: Springer-Verlag, 1188-1213.

Kallsen, C. 2014. Rhodococcus fascians associated with some UCB-1 rootstocks. Kern Pistachio News, University of California Cooperative Extension, April, 2014.

Kallsen, Craig, University of California Cooperative Extension Bakersfield: email to Duane Schnabel, California Department of Food and Agriculture, April 22, 2014.

Randall, Jennifer, New Mexico State University: email to Nick Condos, California Department of Food and Agriculture, April 10, 2014.

Putnam, M. 2014. Demystifying Rhodococcus fascians. Digger, February, 2014: 33-37.

Putnam, M. L. and M. L. Miller. 2007. Rhodococcus fascians in herbaceous perennials. Plant Disease, 91 (9): 1064-1076.

Stamler, R. A., J. Kilcrease, R. J. Heerama, C. E. Kallsen, and J. J. Randall. 2014. Rhodococcus sp. associated with Pistachio Bushy Top Syndrome in California and Arizona. Plant Disease (submitted).

Responsible Party:

Dr. 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.

Pest Rating: C

Posted by ls

Bacteria, Plant Pathogens

Acidovorax citrulli (Schaad et al., 1978) Schaad et al., 2008

March 16, 2015 Admin

California Plant Pest Rating for

Acidovorax citrulli (Schaad et al., 1978) Schaad et al., 2008

Pest Rating: A

PEST RATING PROFILE

Initiating Event:

In July 2013, the bacterial fruit blotch pathogen (BFB), Acidovorax citrulli, was detected in a melon field (Cucumis melo) in Yolo County. This detection marked the first official record of the bacterial fruit blotch disease in California. Three contiguous fields planted to cucumber (2 fields) and watermelon (1 field), were also tested, however only melon was found infected with BFB. Subsequent trace back investigations revealed that the source seed for the Yolo County melon site was grown in a seed lot in Sutter County in 2012 and later, was found positive for BFB (and Cucumber green mottle mosaic virus – which is not evaluated in this proposal). The 2013 trace back also revealed that in 2012, two sites in Sutter County produced a total of 6 melon and watermelon seed lots that were positive for BFB. Those two sites are currently planted to non-hosts, and volunteer plants of 2013 tested negative for BFB. Two foreign sources of melon and cucumber seed lots planted in the two Sutter County sites were identified as Chile and Romania. However, no (melon) seed remained for testing from the Chilean source, and the source cucumber seed from Romania was not tested for BFB as the progeny seed tested negative for the pathogen. As for the 2013 Yolo County BFB positive site, County and State approved abatement measures were implemented. Wheat, a non-host, was grown at the site and in 2014, volunteer melon plants tested negative for BFB. To date, additional monitoring and testing of volunteer plants continues and those in the field are treated with herbicide and biodegraded. Furthermore, in 2013, approximately 120 trace forward seed lots were evaluated for risk of potential infection with BFB. Pathways identified as possible risk links for potential BFB infection were source seed, shared irrigation, proximity to a positive detection, mechanical transmission (equipment and workers), and seed processing operational steps. Trace forward investigations revealed that 2012 Sutter County melon seeds had been sent to San Benito County and tested positive for BFB. Also, BFB infested watermelon seed had been sent to San Benito County as well as shipped overseas to Lebanon, Italy and Africa. To date, 34 trace forward and trace back seed lots were sampled and tested for BFB, of which 6 were positive for the pathogen. Any remaining seeds from positive seed lots are currently on hold in Sutter and San Benito Counties pending destruction or CDFA approved treatment and proven freedom from the bacterium. Given this current detection and subsequent actions taken, A. citrulli is presently considered a quarantine, actionable pathogen that is temporary, transitional and under eradication, and therefore, not established within California. A permanent pest rating for the pathogen is herein proposed.

History & Status:

Background: Acidovorax citrulli is the causal agent of bacterial fruit blotch and seedling blight of cucurbit plants. The disease is seed transmitted and is a serious pathogen particularly of watermelon and melon worldwide.

Bacterial fruit blotch of cucurbits was first reported in 1965 causing seedling blight symptoms on watermelon seedlings at the USDA regional plant introduction station in Griffin, Georgia, USA. The causal agent was determined to be seed-borne and seed transmissible with the capability of surviving up to 7.5 years in stored seed. Seedling blight was also observed in squash and melon that were artificially inoculated with the pathogen. In 1969, the disease was observed on watermelon at a research farm in Leesburg, Florida, USA, and in 1978 it was observed in Queensland, Australia. The causal agent was identified as Pseudomonas pseudoalcaligenes subsp. citrulli (Schaad et al., 1978). The first outbreak of BFB in commercial watermelon fields was observed in the Mariana Islands (Guam and Tinian). In 1989, the first outbreak of BFB in the continental USA was in major watermelon producing states including Florida, South Carolina and Indiana. Between 1990 and 1995 sporadic and devastating outbreaks occurred in watermelon production regions of the Midwest, Northeast and Southern USA. Despite the implementation of stringent BFB management guidelines developed by academic and industry professionals, BFB outbreaks were reported in cucurbits other than watermelon in 1999 (Walcott, 2005, 2008). In 2013, BFB was first detected in California and consequently treated as a state actionable pathogen (CDFA-PEA, 2013).

Taxonomically, the pathogen belongs to the family Comamonadaceae in the order Burkholderiales. As a result of further taxonomic studies in 1992, Pseudomonas pseudoalcaligenes subsp. citrulli was found to be molecularly closely related to the genus Acidovorax and was subsequently reassigned (Willems et al., 1992). In 2008, Acidovorax avenae subsp. citrulli was reclassified and elevated to species rank, namely, A. citrulli (Schaad et al., 2008).

Disease cycle: The disease cycle begins with contaminated seed. Seedborne inoculum is the most important source of primary inoculum for BFB development in cucurbit seed and fruit production fields as well as in transplant production houses. Acidovorax citrulli has been detected on the external seed surface as well as internally on the papery perisperm-endosperm layer (Kurowski, 2014). In seed and fruit production fields, other sources of inoculum include infected seedlings, the previous season’s plant debris, and volunteer watermelon seedlings or cucurbitaceous weeds. In the USA watermelon production is mostly from dry seeded plants, although transplants are increasing in popularity (CABI, 2014). Contaminated seed result in infected seedlings. Warm temperatures and high relative humidity are favorable for the development of the disease. Under such conditions, bacteria from infested seed infect emerging and developing cotyledons. Little is known about the epidemiology of BFB in seed production environments. Under cool temperatures and low moisture conditions typical BFB fruit and foliar symptoms may not develop however, even with the lack of symptoms infested seeds are produced (Walcott, 2008).

Under field conditions, high relative humidity and rainfall are critical for the spread of bacterial cells through splash dispersal by wind-driven rain or overhead irrigation to uninfected plants. Bacterial cells are also spread by contact with cultivation equipment, irrigation and human contact. Once deposited on uninfected plants, bacterial cells swim through open stomata and leaf wounds and penetrate intercellular sub-epidermal spaces where they rapidly multiply causing the production of water soaked lesions and secondary inoculum. Acidovorax citrulli does not move systemically through the plant. Under favorable conditions, a few primary infections sites can result in widespread infection of all plants by the time of harvest. Leaf lesions that develop are reservoirs of bacteria for fruit infection. At anthesis (fruit set), bacteria are splashed dispersed by wind-driven rain or irrigation onto the surfaces of immature ovaries which they penetrate through open stomata thereby initiating fruit infection (Walcott, 2008). Watermelon fruit are most vulnerable to bacterial infection 2-3 weeks after anthesis. After this brief infection window a wax layer is deposited over the surface of fruit covering stomata and preventing bacteria from penetrating (Frankle et al., 1993). Once wax is deposited, bacteria are only able to enter mature fruit through wounds. Symptoms of fruit infection do not usually develop until about 2 weeks before harvest maturity. The exact reason for this latency period is unknown but may be influenced by fruit physiology (ASTA, 2009). Debris or seed from infested and rotten fruit, cucurbitaceous weeds, and volunteer cucurbit plants may allow the pathogen to over-season and perpetuate the disease cycle in the next cropping cycle.

Typical transplant house conditions favor development of Bacterial fruit blotch. Those conditions include high watermelon seedling populations, high temperatures high relative humidity and overhead irrigation. Infected seeds serve as the source of primary inoculum and bacterial cells from a few infected seedlings can rapidly spread throughout a greenhouse by splash dispersal and production of aerosols. As in field conditions, dispersed bacterial cells are deposited on uninfected seedlings which are penetrated through open stomata to intercellular spaces eventually leading to numerous secondary infection cycles. Asymptomatic plants with epiphytic A. citrulli cells can cause disease outbreaks under field conditions. Infected seedlings produced in transplant greenhouses can result in introduction and widespread development of BFB in the field.

Hosts: Acidovorax citrulli are pathogenic to various species of the Cucurbitaceae family. The most susceptible hosts are watermelon (Citrullus lanatus) and melons (Cucumis melo) including cantaloupe and honeydew melons which develop symptoms on fruit and leaves. Other cucurbits include cucumber (Cucumis sativus), squash (Cucurbita pepo), and Cucurbita moschata which only develop symptoms on foliage and not on fruit. Wild cucurbits are also hosts, such as, wild Citron (Citrullus lanatus var. citroides) that develops symptoms on leaves and fruit with seed transmission. Host range studies using artificial inoculations of the bacteria have resulted in symptoms on several solanaceous hosts including tomato, eggplant and pepper foliage, but not on fruit. Bacteria have been isolated from tomato seeds and foliage of betel pepper (Piper betle).

Symptoms: Acidovorax citrulli can attack all stages of cucurbit plants. Initial symptoms are water-soaked areas along the edges or the midveins on the undersides of cotyledons. In time the water-soaked lesions dry and become reddish to dark brown along the length of the midrib. In severe situations lesions coalesce on cotyledons, hypocotyls and stems and cause seedling collapse. On true leaves water-soaked lesions and reddish-brown to dark brown water soaked lesions are present along the leaf veins. Leaf symptoms may become inconspicuous over time.

Symptoms on fruit may be conspicuous or inconspicuous. Symptoms on watermelon fruit characteristically appear as small, dark olive, greasy irregularly shaped, blotch-like water-soaked spots on the rind of the upper surface of infected fruit. The lesions may rapidly enlarge from a few millimeters in diameter to cover the entire upper surface of the fruit leaving only the ground spot symptomless. In advance stages, the infected site becomes necrotic, cracks develop from which sticky, amber-colored ooze may exude. Internally, the lesions may penetrate into the flesh of the fruit causing rot. On fruit with netting, such as melon, symptoms initiate as small water-soaked spots. In muskmelons, netting does not form over lesions and the lesions do not expand on the rind surface but appears a small inconspicuous pits which extend into the flesh of the fruit forming rotten cavities (Walcott, 2008). In honeydew, initial water-soaked spots over time become brown and cracked with a water-soaked margin.

Damage Potential: Bacterial fruit blotch is the most economically important bacterial disease of cucurbits worldwide (Walcott, 2008). With its outbreak in 1989 in commercial watermelon fields in the continental USA, losses of more than 90% if the total marketable fruit occurred in some affected fields. Since then, although in most years BFB has occurred in relatively few fields, it has continued to be a threat to the watermelon industry and cucurbit seed, transplant and fruit producers, resulting in marketable watermelon fruit losses of over $100,000 to individual growers. In 1992, in Georgia thousands of hectares were lost to the disease (CABI, 2014).

Under favorable environmental conditions fruit losses of 90-100% have been observed in commercial watermelon fields in the USA. In 2000 estimated losses of 40-50% to 100% occurred in melon fields. A survey of 18 melon fields resulted in the detection of 4% to 47% of the disease in all fields (EPPO, 2014).

Transmission: Infested seed is the main mode of transmission of Acidovorax citrulli. The bacteria is also spread through infested seedlings, host crop debris, cucurbitaceous weeds, volunteer cucurbit plants, overhead irrigation, wind driven rain, contaminated cultivation equipment and tools, and human contact.

In field experiments, honey bees were shown to transmit the pathogen to female watermelon blossoms resulting in infection of 25% of seedlots although no fruit symptoms were observed (Fessehaie et al., 2005). Honey bees are not used for pollination in commercial seed production.

Worldwide Distribution: The geographical origin of Acidovorax citrulli is not known, however, the disease has spread to many regions of the world mainly through the passage of contaminated seeds.

Bacterial fruit blotch is distributed in Asia (China, Japan, Republic of Korea, Taiwan, Thailand, Turkey, Iran, Israel, and Malaysia), Europe (Greece, Hungary, Italy), Oceania (Queensland: Australia, Guam, Northern Mariana Islands), South America (Brazil), Central America and Caribbean (Costa Rica, Trinidad and Tobago), and North America (Canada, USA).

Within USA it is distributed in Alabama, Arkansas, Delaware, Florida, Georgia, Iowa, Illinois, Indiana, Maryland, Mississippi, Missouri, North Carolina, Oklahoma, Oregon, South Carolina, and Texas. The disease was detected in 1989 in Delaware, Iowa and Maryland but has not been reported since then (CABI, 2014; EPPO, 2014). The detection in California is considered transient, actionable and under eradication.

Official Control: Presently, 16 countries have included A. avenae subsp. citrulli (syn. of A. citrulli) on their ‘Harmful Organism Lists’. Those countries are; Chile, China, Colombia, Costa Rica, Ecuador, Guatemala, Honduras, India, Israel, Japan, Mexico, Nicaragua, Panama, Peru, Taiwan, and Turkey. Acidovorax citrulli is a quarantine pathogen in California, USA.

California Distribution: There are no official reports of BFB being established in field or natural environments within California – that would indicate an established distribution. The 2013 field detection in Yolo County, California is considered transient, actionable and under eradication.

California Interceptions: There are no state reports of Acidovorax citrulli detections in plant materials intercepted within or at points of entry in California.

The risk Bacterial fruit blotch 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): Although California climate is not considered conducive for the establishment (development and increase) of A. citrulli, the presence of suitable microenvironments and macro/micro climate changes enable establishment and perpetuation of pathogenic strains within California as evidence by the 2013 field outbreak in Yolo County, California.

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 medium (2). The host range is mainly limited to various species of the Cucurbitaceae family. Nevertheless, Cucurbitaceous hosts, including watermelon, melon, squash and cucumber, are widely grown commercially within California to warrant of establishment and spread of this pathogen.

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): Under favorable environmental conditions BFB has a high reproductive rate and depends on artificial means for its dispersal. Infested seeds are the main means of long distance dispersal, and in fields and greenhouses, the bacterium is capable of widespread transmission through contaminated plant materials and debris, equipment, water-splash, human contact and possibly insects.

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

– 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): Incidence of the BFB pathogen could result in lowered crop yields, crop value, increased production costs, loss of markets due to the imposition of quarantine rules and regulations, alteration of cultural practices and possible interference with the delivery of irrigation water where a supply is shared between fields.

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

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 High (3): incidence of A. citrulli could result in additional official or private treatment programs as well as significantly impact cultural practices and home/urban gardening.

Consequences of Introduction to California for Acidovorax citrulli:

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 = 13 (High).

– 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: Acidovorax citrulli is not established in California (0). Actions taken subsequent to the detection of the pathogen in Yolo County and detailed in the “Initiating Event” section above, provide evidence of the current ‘non-established’ status of the pathogen.

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 = 13 (High).

Uncertainty:

Information of the source of the Yolo County BFB detection is not known. Infested seeds and transplant are a ready source of introduction of the pathogen to CA fields. Diligent monitoring and testing of seed/plants in greenhouses and fields must be followed to mitigate risk of further field introduction and potential establishment of the pathogen in California soils.

Conclusion and Rating Justification:

Based on the evidence provided above the proposed rating for Acidovorax citrulli is A.

References:

ASTA. 2009. “Bacterial fruit blotch – a commercial grower’s guide” brochure. June 2009.

Burdman S. and R. Walcott. 2012. “Acidovorax citrulli: generating basic and applied knowledge to tackle a global threat to the cucurbit industry.” Molecular Plant Pathology 13(8): 805-15.

CABI. 2014. “Acidovorax citrulli.” Crop Protection Compendium. Wallingford, UK: CAB International. www.cabi.org/cpc.

CDFA-PEA. 2013. Cucumber Green Mottle Mosaic Virus and Bacterial fruit blotch detections in California. California Department of Food and Agriculture, Pest Exclusion Advisory no. 29-2013.

EPPO. 2014. “Acidovorax citrulli Bacterial fruit blotch of cucurbits.” Panel review date 2013-03. http://www.eppo.int/QUARANTINE/Alert_List/bacteria/Acidovorax_citrulli.htm.

Frankle, W. G., D. L. Hopkins and R. E. Stall. 1993. “Ingress of the watermelon fruit blotch bacterium into fruit.” Plant Disease, 77(11):1090-1092.

Kurowski, C. “CGMMV – BFB Training.” Presentation at the ‘Cucumber green mottle mosaic virus and bacterial fruit blotch disease training” California Department of Food and Agriculture, Sacramento, CA on May 1and 2, 2014. Monsanto Vegetables, Woodland, CA.

Schaad, N. W., G. Sowell Jr, R. W. Goth, R. R. Colwell and R. E. Webb. 1978. “Pseudomonas pseudoalcaligenes subsp. citrulli subsp. nov.” International Journal of Systematic Bacteriology, 28(1):117-125.

Schaad, N. W., E. Postnikova, A. Sechler, L. E Claflin, A. K. Vidaver, J. B. Jones, I. Agarkova, A. Ignatov, E. Dickstein and B. A. Ramundo. 2008. “Reclassification of subspecies of Acidovorax avenae as A. avenae (Manns 1905) emend., A. cattleyae (Pavarino, 1911) comb. nov., A. citrulli Schaad et al., 1978) comb. nov., and proposal of A. oryzae sp. nov.” Systematics and Applied Microbiology 31: 434–446.

Walcott, R. R. 2005. “Bacterial fruit blotch of cucurbits.” The Plant Health Instructor. DOI: 10.1094/PHI-I-2005-1025-02.

Walcott, Ron R. 2008. “Integrated pest management of bacterial fruit blotch of cucurbits.” In Integrated Management of Diseases caused by fungi, phytoplasma and bacteria, Eds. A. Ciancio & K. G. Mukerji. 187-205 p.

Willems A., M. Goor, S. Thielemans, M. Gillis, K. Kersters K and Jde Ley. 1992. “Transfer of several phytopathogenic Pseudomonas species to Acidovorax as Acidovorax avenae subsp. avenae subsp. nov., comb. nov., Acidovorax avenae subsp. citrulli, Acidovorax avenae subsp. cattleyae, and Acidovorax konjaci.” International Journal of Systematic Bacteriology, 42(1):107-119.

Zhao, T., J. Feng, A. Sechler, P. Randhawa, J. Li and N. W. Schaad. 2009. “An imporved assay for detection of Acidovorax citrulli in watermelon and melon seed.” Seed Science & Technology, 37: 337-349.