California Pest Rating for
PEST RATING: B
PEST RATING PROFILE
On September 5, 2017, a melon (Cucumis melo cv. mlada) fruit, showing symptoms of spotting and scabbing, was collected during a phytosanitary field inspection in Glenn County, by Glenn Agricultural County officials and sent to the CDFA Plant Pathology Laboratory for diagnoses. Sebastian Albu, CDFA plant pathologist, identified the pathogen, Erwinia aphidicola, by PCR and DNA sequencing, as the cause of the disease on the exterior surface of the melon sample. As there have been no earlier reports in the USA, the pathogen was sent in culture to the USDA APHIS PPQ CPHST Diagnostic Lab in Beltsville, Maryland, for diagnostic confirmation. On November 20, 2017, the USDA confirmed the identity of E. aphidicola and marked a new record of the pathogen in the U.S. (USDA, 2017). The pathogen was assigned a temporary ‘Q’ rating. The risk of introduction and establishment of this pathogen in California is assessed and a permanent rating is herein proposed.
History & Status:
Background: Erwinia aphidicola (Enterobacteriaceae) was originally discovered as a new species of bacteria that constituted the major flora of the gut of pea aphid, Acyrthosiphon pisum, and caused aphid mortality (Harada et al., 1997). However, in 2009, E. aphidicola was confirmed as a plant pathogen (Santos et al., 2009) that had caused disease of common bean and pea observed during 2003-2004 in southeastern Spain, and, at that time, was attributed to a different bacterial species, E. persicina (González et al., 2005, 2007; Santos et al., 2009). Both E. persicina and E. aphidicola are closely related species that show high similarity (99-100%) in 16S rDNA sequence analysis. However, Santos et al., (2009) confirmed that sequence analysis of 16S rDNA may not provide sufficient resolving power to discriminate these closely related species, but would require a more species-specific set of DNA primers for PCR amplification. Subsequently, Santos and others were able to molecularly discriminate E. aphidicola from E. persicina and show that E. aphidicola was the cause of the related diseases reported from Spain.
Erwinia aphidicola has not been reported in the USA prior to its recent detection in California. However, in the USA, a new species of bacteria, E. nulandii was isolated from bean in 1981 in Nebraska, and was shown to be distinct from all other Erwinia species by biochemical, protein, and DNA analytical tests. (Schuster et al., 1981). In 1994, E. nulandii was determined to be a synonym of E. persicinus (later corrected to E. persicina) – the species that is closely related to E. aphidicola (Brenner et al., 1994). As shown by Santos and others (2009), further sequence analysis of the USA isolate of E. persicina may be necessary to distinguish the possible presence of E. aphidicola.
Hosts: Presently, Phaseolus vulgaris (bean) and Pisum sativum (pea) are reported as natural hosts for Erwinia aphidicola (Santos et al., 2009). Experimentally, cucumber, tomato, pepper, and melon were reported as alternative hosts to green bean for the southeastern Spanish isolate of E. persicina (Diánez et al., 2009) which later was identified as E. aphidicola (Marín et al., 2011). The current detection of E. aphidicola (see ‘Initiating Event’) indicates the infection of melon in a field environment.
Symptoms: Symptoms of chlorotic and necrotic leaf spots in beans and generalized chlorosis as well as necrosis in leaves and tendrils in peas are exhibited when these plants are infected with Erwinia aphidicola (González et al., 2005, 2007). In beans, early symptoms of light, interveinal chlorosis in leaves soon turn into yellowish leaves with green veins. As the disease progresses, necrotic spots develop and completely affected leaves turn brown. Watery spots and very marked grains appear on infected pods, which take on a curved, hook-like appearance. Rough roots along the entire stem are also produced in diseased plants (Marín et al., 2011). Marín and other researchers (2011) observed 13 different symptoms in plants grown from commercial bean seeds and 10 different symptoms in plants grown from replanting bean seeds in a controlled environment bioassay study. Those symptoms included the earlier reported ones in varying intensities, as well as, green wilted and deformed leaves and dwarfed plants.
In experimental trials, tomato, pepper, cucumber, and melon inoculated with E. aphidicola, exhibited symptoms of leaf necrosis, adventitious roots, brown coloration along the stem, interveinal chlorosis, curled, and blistered leaves. In cucurbits, a distinct lesion in some areas of the stem was also exhibited (Diánez et al., 2009).
In California, symptoms of reticulate scabbing with irregular cracks within scabs, and scattered chlorotic spots were observed on the E. aphidicola-infected melon fruit (see ‘Initiating Event’). These symptoms covered most of the surface of the fruit and were not apparent in internal tissue (personal communication: Sebastian Albu, CDFA).
Disease development: While there is no information reported on the pathogenesis and epidemiology of disease caused by Erwinia aphidicola in particular, it is likely that the biology of E. aphidicola is similar to its genetically closely related species E. persicina, for which only scant information is available. In greenhouse studies on the life cycle, host range, and environmental effects of E. persicina infecting forage or grain legumes, including bean and pea, Zhang and Nan (2014) determined that the pathogen was transmitted by seeds, water, and soil. It was present both on the surface and within seeds. Bacteria present on seeds can be internalized within the sprout and become protected from post-harvest sanitation. Bacteria within seeds can remain alive indefinitely thereby, facilitating long distance transmission of the pathogen via movement of seeds. The pathogen was capable of surviving in alfalfa soil for more than 3 months and could invade alfalfa plants through natural opening. Once within a plant, the bacterial pathogen can move from the roots upward to the leaves, inflorescences, and subsequently, the seeds. The pathogen is capable of surviving within a wide range of environmental conditions and can endure arid, saline, and alkaline conditions. The optimum temperature for growth was 28°C within a range of 10-36°C and no growth occurred below 5°C or above 40°C (Zhang & Nan, 2014).
Dispersal and spread: pathogen-infested plants, seeds, soil, and water (Zhang & Nan, 2014).
Damage Potential: In southeastern Spain, Erwinia aphidicola is reported to have caused over 50% decrease in production of commercial beans due to chlorotic and necrotic leaf spotting and deformation of pods (González et al., 2005). The disease affected approximately 12 ha of field-grown peas (González et al., 2007). Similar to south eastern Spain, most of California experiences a Mediterranean climate which is usually characterized by rainy winters and dry, warm to hot summers. Beans and peas are commercially cultivated in such climate in limited regions within the State, and may be at risk of disease caused by E. aphidicola.
Worldwide Distribution: Europe: Spain; North America: USA (California) (Marin et al., 2011).
Official Control: Presently, Erwinia aphidicola has a temporary Q rating in California. No official control has reported by any country for E. aphidicola or E. persicina.
California Distribution: Glenn County (see “Initiating Event”).
California Interceptions: None reported.
The risk Erwinia aphidicola would pose to California is evaluated below.
Consequences of Introduction:
1) Climate/Host Interaction: Erwinia aphidicola is likely to establish in limited parts of California wherever its natural hosts, peas and beans are grown. Its current detection in melon fruit indicates the possible inclusion of an additional host in California. It is capable of surviving under a wide range of environmental conditions.
Evaluate if the pest would have suitable hosts and climate to establish in California.
– 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.
2) Known Pest Host Range: Presently, the natural host range is very limited. Peas and beans are the only natural hosts that have been reported.
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.
3) Pest Dispersal Potential: The bacterial pathogen has high reproduction and is spread by artificial means through infected planting stock, seeds, soil, and water.
Evaluate the natural and artificial 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.
4) Economic Impact: The potential impact of the pathogen on bean and pea production could result in lowered crop yield and value, as well as a loss of marketability of pea and bean pods.
Evaluate the economic impact of the pest to California using the criteria below.
Economic Impact: A, B, C.
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.
Economic Impact Score: 3
– 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.
5) Environmental Impact: Evaluate the environmental impact of the pest on California using the criteria below. No impact to the environment is expected.
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
Environmental Impact Score: 1
– 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.
Consequences of Introduction to California for Erwinia aphidicola:
Add up the total score and include it here. 10
-Low = 5-8 points
–Medium = 9-12 points
-High = 13-15 points
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.
Evaluation is ‘Low’. To date, Erwinia aphidicola has only been detected in a commercial melon field in Glenn County.
-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.
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 = 9
The host range of Erwinia aphidicola, its epidemiology, and damage caused to those hosts is not fully known.
Conclusion and Rating Justification:
Based on the evidence provided above the proposed rating for Erwinia aphidicola is B.
Brenner, D. J., J. Rodrigues Neto, A. G. Steigerwalt, and C. F. Robbs. 1994. “Erwinia nulandii” is a subjective synonym of Erwinia persicina. International Journal of Systematic Bacteriology 44: 282-284.
Diánez, F., Santos, M., Font, I., de Cara, M., & Tello, J. C. (2009). New host for the enterobacterial phytopathogen Erwinia persicina. In A. Mendez-Vilas (Ed.), Current research topics in applied microbiology and microbial biotechnology (pp. 78–82). Singapore: World Scientific Publishing Co. Pte. Ltd. [Abstract only]
González, A. J., J. C. Tello, and M. de Cara. 2005. First report of Erwinia persicina from Phaseolus vulgaris in Spain. Plant Disease 89: 109.
González, A. J., J. C. Tello, and M. R. Rodicio. 2007. Erwinia persicina causing chlorosis and necrotic spots in leaves and tendrils of Pisum sativum in southeastern Spain. Plant Disease 91: 460.
Harada, H., H. Oyaizu, Y. Kosaka, and H. Ishikawa. 1997. Erwinia aphidicola, a new species isolated from pea aphid, Acyrthosiphon pisum. Journal of General and Applied Microbiology 43: 349-354.
Marín, F., M. Santos, F. Carretero, J. A. Yau, and F. Diánez. 2011. Erwinia aphidicola isolated from commercial bean seeds (Phaseolus vulgaris). Phytoparasitica 39: 483-489. https://doi.org/10.1007/s12600-011-0190-4
Schuster, M. L., A. M. Schuster, and D. S. Nuland. 1981. Erwinia nulandii, a new bacterium pathogenic for beans (Phaseolus vulgaris L.). Fitopatologia Brasileira 6: 345.
USDA. 2017. Email from J. H. Bower, USDA APHIS, to S. Brown, CDFA, (and others). Subject: Fw: Positive: two (2) samples for Erwinia aphidicola from CA (new U.S. record). Sent: Monday, November 20, 2017, 10:42 am.
Zhang, A., and Z. Nan. 2014. Erwinia persicina, a possible new necrosis and wilt threat to forage or grain legumes production. European Journal of Plant Pathology 139: 349-358.
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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