California Pest Rating for
Ustilago esculenta Henn. 1895
PEST RATING: A
PEST RISK PROFILE
On October 19 and 20, 2017, Manchurian wild rice plants with slightly swollen lower stems, were collected by Riverside County Agricultural officials, from a private company, in Riverside County and sent to the CDFA’s Plant Pathology Lab for possible detection of the smut fungus, Ustilago esculenta. On November 20, 2017, Cheryl Blomquist, CDFA plant pathologist, detected U. esculenta, by PCR and sequencing, from the swollen, white interior plant tissue. The current status and risk of U. esculenta to California is assessed here and a permanent rating is proposed.
History & Status:
Background: Ustilago esculenta is a biotrophic (i.e., it has a long-term, non-lethal feeding relationship with an infected plant) smut fungus that incites formation of swollen culms or smut galls in the apical internodal (stem) region of perennial Manchurian wild rice, Zizania latifolia. These swollen culms or smut galls are edible and have unique flavor and delicacy. The swollen culms are consumed as a vegetable in India (Manipur), China, Japan, and Taiwan (Chung & Tzeng, 2004; Jose et al., 2016; Terrell & Batra, 1982). In China and Japan, it is cultivated as a commercial food crop (Jose et al., 2016). Furthermore, in Taiwan, and southern China, the production of galls occurs during the season of tropical storms and provides an alternate food source to consumers when cultivation of other vegetables is negatively affected. Therefore, the fungus is considered highly beneficial and economically important (Chung & Tzeng, 2004). Hennings (1895) originally discovered the pathogen, Ustilago esculenta in its infected host, Zizania latifolia, in China.
In the USA, Manchurian wild rice, Zizania latifolia, is prohibited entry into the country due to the smut fungus, Ustilago esculenta, that it carries (USDA, 2017). Native species of wild rice may be at risk of infection and loss of production particularly since the fungus prevents development of inflorescences, thereby, affecting seed production (Terrell & Batra, 1982; Yamaguchi, 1990).
In 1991, an illegal 0.05-ha planting of Manchurian wild rice infected with Ustilago esculenta was discovered in a field near Modesto, California and marked the first report of the disease in a field situation in North America. The plants had been brought into the USA in violation of federal quarantines and were eradicated (Watson et al., 1991). In 1999, the host and pathogen were discovered in two small grower’s plots (approximately 2-ha total) in Baton Rouge, Louisiana. The plants were eradicated in 2000 (NPAG, 2001).
Disease Development: Ustilago esculenta spends its entire life cycle in the host plant. The fungus grows within and between plant cells in the stem tissues, particularly near the apical meristem. However, the fungus is not systemically distributed throughout the entire plant and does not invade leaf and root tissue (Chen & Tzang, 1999, Jose et al., 2016). Chen and Tzang (1999), using PCR technology, found the fungal DNA in the growth tip of Manchurian wild rice plants and not in leaves and healthy plant tissue. They also detected the fungus in the sheath of infected plants even when there were no outward signs of its presence. The fungus prevents production of inflorescence and galls develop at the internode region beneath the apical meristem. Galls are formed within 10-15 days even though the plants may have been planted in the soil for over 8 months. Internally, gall formation involves hypertrophy (increase in cell size), hyperplasia (increase in cell numbers), and presence of mucilaginous cavities (Chan & Thrower, 1980). At this developmental stage, the inner tissue of a gall appears white and filled with fungal hyphae which later develop to form dark teliospores (sexual spores) within the gall. Teliospore formation is favored at temperatures greater than 28°C (Chung & Tzeng, 2004). In China, the edible galled plants are harvested for consumption prior to the production of teliospores. With time, black longitudinal streaks appear, and eventually, the entire stem turns black and deteriorates. Furthermore, a lack of nutrients in a plant or low water level in a field initiate earlier production of the reproductive stage of the fungus, thereby, reducing quality and yield of the plants (Yamaguchi, 1990). The optimum temperature for fungal growth is 20-28°C and the optimum pH range is 4-7. The fungus may overwinter as mycelium and teliospores in the grass rhizomes and be transmitted into new shoots through asexual propagation of the plant. Alternatively, teliospores from decomposed galls, may survive in soil (Chung & Tzeng, 2004). Jose et al., (2016) detected spores and fragmented hyphae in the rhizomes throughout the year, including the month of January during which the above ground culms degenerated, thereby, suggesting that it may serve as inoculum for infection.
Dispersal and spread: Plant rhizomes, galled stems, and soil (Jose et al., 2016; Chung & Tzeng, 2004).
Hosts: Zizania spp. in the family Poaceae: Z. aquatica, Z. latifolia (syn. Z. caduciflora), and Zizania sp.
Symptoms: Ustilago esculenta stimulates the swelling of the culms of its host grass plants resulting in the formation of edible galls at the internodal region beneath the apical meristem (stem base). The galls are about 3-4 cm in width and 15-20 cm in length (Chung & Tzeng, 2004). Infected plants do not show any typical disease symptoms despite the internal presence of the fungus (Jose et al., 2016). Experimentally, plant infected with U. esculenta showed a decrease in height, but significant increase in above-ground biomass and higher chlorophyll content (Yan et al., 2013).
Damage Potential: Ustilago esculenta prevents the production of inflorescences in host plants thereby, significantly reducing seed production and resulting in great yield loss (Terrell & Batra, 1982; Chen & Tzeng, 1999). Production of wild rice, including near relatives of Zizania latifolia, in California may be significantly reduced by the fungus.
Worldwide Distribution: Asia: Cambodia, China, Hong Kong, India, Japan, Laos, Malaysia, Myanmar, (east and south Asia), Taiwan, Thailand, (former) USSR, Vietnam; North America: USA (District of Columbia) (Farr & Rossman, 2017).
Official Control: Ustilago esculenta, with its host plant, Zizania spp., are prohibited from being imported or offered for entry into the United States by the USDA, and are on the Prohibited Articles List under Federal Regulations 7CFR 319.37-2 (USDA, 2017).
California Distribution: Ustilago esculenta is not established in California.
California Interceptions: In 1998, there was one interception of Manchurian wild rice infested with Ustilago esculenta destined to a private business in San Bernardino County. The shipment was destroyed.
In 1991, a foreign-sourced, illegal planting of Manchurian wild rice infected with Ustilago esculenta was detected in a field near Modesto. The plants were eradicated.
The risk Ustilago esculenta would pose to California is evaluated below.
Consequences of Introduction:
1) Climate/Host Interaction: Ustilago esculenta is likely to establish wherever wild rice, Zizania, is cultivated in California. California wild rice is grown under warm, dry, clear days, and a long growing season; mostly on fine-textured, poorly-drained soils (Farrar, 2000). Since the fungus is limited to Zizania spp., and is likely to establish wherever native species of wild rice are grown in California, its potential distribution is considered widespread and a ‘High” rating is given to this category.
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: The host range is limited to Zizania
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 fungus is biotrophic and is dependent on the spread infested galled plants for long distance spread. It is also transmitted in propagative rhizomes and soil.
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: Ustilago esculenta prevents the production of inflorescences in host plants thereby, drastically reducing seed production and resulting in great yield loss. The fungus and its vectoring host, Zizania latifolia, are prohibited entry in the USA , and would be a threat to native species of wild rice that are grown in California
Evaluate the economic impact of the pest to California using the criteria below.
Economic Impact: A, B, C, D, E
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: Ustilago esculenta, either through the establishment of infected Zizania latifolia or its direct impact on the stand and cultivation of California native wild rice species, can result in reducing native stands of wild rice by reducing seed production, thereby, disrupting aquatic plant and animal communities, critical habitats, and lowering biodiversity. This could result in additional official treatment programs. A “High” rating is given to this category.
Evaluate the environmental impact of the pest on California using the criteria below.
Environmental Impact: A, C, D
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: 3
– 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 Ustilago esculenta: High (13)
Add up the total score and include it here.
-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. Ustilago esculenta is not established in California.
–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 = 13
Conclusion and Rating Justification:
Based on the evidence provided above the proposed rating for Ustilago esculenta is A.
Chan, Y-S., and L. B. Thrower. 1980. The host-parasite relationship between Zizania caduciflora Turcz. and Ustilago esculenta P. Henn. 1. Structure and development of the host and host-parasite combination. New Phytopathology 85: 201-207.
Chen, R-S., and D. D-S. Tzeng. 1999. PCR-mediated detection of Ustilago esculenta in water oat (Zizania latifolia) by ribosomal internal transcribed spacer sequences. Plant Pathology Bulletin 8: 149-156.
Chung, K., and D. D. Tzeng. 2004. Nutritional Requirements of the Edible Gall-producing Fungus Ustilago esculenta. Journal of Biological Sciences, 4(2), 246-252.
Farr, D. F., and A. Y. Rossman. 2017. Ustilago esculenta. Fungal databases, U.S. National Fungus Collections, ARS, USDA. Retrieved November 28, 2017, from https://nt.ars-grin.gov/fungaldatabases/
Farrar, K. 2000. Crop profile for wild rice in California. California Pesticide Impact Assessment Program, University of California, Davis, CA. http://www.ipmcenters.org/CropProfiles/docs/cawildrice.pdf
French, A.M. 1989. California Plant Disease Host Index. California Department of Food and Agriculture, Sacramento (Updated online version by T. Tidwell, May 2, 2017).
Jose, R. C., S. Goyari, B. Louis, S. D. Waikhom, P. J. Handique, and N. C. Talukdar. 2016. Investigation on the biotrophic interaction of Ustilago esculenta on Zizania latifolia found in the Indo-Burma biodiversity hotspot. Microbial Pathogenesis 98: 6-15.
NPAG. 2001. NPAG report sent to Trillium. 20. Ustilago esculenta (Basidiomycota: Ustilaginomycetes: Ustilaginaceae) wild rice smut. New Pest Advisory Group Plant Epidemiology and Risk Analysis Laboratory, Center for Plant Health Science & Technology.
Terrell, E. E., and L. R. Batra. 1982. Zizania latifolia and Ustilago esculenta, a grass-fungus association. Economic Botany 36: 274-285.
USDA. 2017. Plants for plant manual. United States Department of Agriculture. First edition March 2017.
Watson, T., T. E. Tidwell, and D. G. Fogle. 1991. Smut of Manchurian wild rice caused by Ustilago esculenta in California. Plant Disease 95: 1075. DOI: 10.1094/PD-75-1075D.
Yamaguchi, M. (1990). Asian vegetables. In J. Janick & J. E. Simon (Eds.), Advances in new crops, 387-390. Timber Press, Portland, OR.
Yan, N., X-Q. Wang, X-F. Xu, D-P. Guo, Z-D. Wang, J-Z. Zhang, K. D. Hyde, and H-L. Liu. 2013. Plant growth and photosynthetic performance of Zizania latifolia are altered by endophytic Ustilago esculenta infection. https://doi.org/10.1016/j.pmpp.2013.05.005
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: A
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