Rhodococcus fascians

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.

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

Score the pest for Environmental Impact. Score:

– Low (1) causes none of the above to occur.
– Medium (2) causes one of the above to occur.
– High (3) causes two or more of the above to occur.

Risk is Medium (2) – 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).

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

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

Evaluation is (-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.