California Pest Rating for

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

Pest Rating: B

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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.

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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

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