Karnal Bunt of Wheat (Triticum Aestivum Wheat Fields in Arizona Because of the Arizona (Fig
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Morris R. Bonde, Gary L. Peterson, and Norman W. Schaad USDA-ARS-FDWSRU, Frederick, Maryland Joseph L. Smilanick USDA-ARS, Horticultural Crops Research Laboratory, Fresno, California a precaution. On 21 March 1996, the Sec- retary of Agriculture announced a “Dec- laration of Extraordinary Emergency” to deal with the disease and set into motion +ARNAL"UNT the mechanism to compensate growers and handlers for losses due to quarantine ac- tions (54). On 25 March, a federal quaran- tine for Karnal bunt was placed on the state of Arizona and parts of Texas and New Mexico where the Karnal bunt–contami- OF7HEAT nated wheat from Arizona had been planted (25). Later, the discovery of Karnal bunt–infected wheat in California extended the quarantine to portions of that state (Fig. 1), and by late summer a national Karnal bunt survey was underway. The efforts of hundreds of state and federal personnel in Karnal bunt of wheat (Triticum aestivum wheat fields in Arizona because of the Arizona (Fig. 2) and California, and of L.), caused by the smut fungus Tilletia discovery of bunted seeds and the confir- many more workers in other states, and indica Mitra (=Neovossia indica (Mitra) mation of T. indica infection by poly- thousands of pages devoted to Karnal bunt Mundkur), was first discovered in 1930 at merase chain reaction (PCR) (17,48). on the Internet underscore the impact of the Botanical Research Station, Karnal, Bunted seeds also were found in remnant the recent discovery of Karnal bunt in the Haryana, in northwest India (29), and now samples of Arizona wheat seed remaining United States. is considered common in the Punjab region in Arizona after a portion of the lots had The main effect of extensive Karnal of India. The disease has been reported been planted in Arizona, Texas, and New bunt is to reduce yield (4) and impart a from Pakistan, Iraq, and Nepal, and is Mexico. Fields in Texas and New Mexico fishy odor and taste to wheat flour, thus found in wheat from Afghanistan (6). It planted with the seed were deep plowed as reducing the quality of the flour (2). Yield was first reported in Mexico in 1972 (16), and since then it has occurred sporadically in localized areas in the states of Sonora and Sinaloa, northwest Mexico. Because the disease was not known in major wheat- producing countries, trade of Karnal bunt– infested wheat grain became highly regu- lated internationally, and the Mexican gov- ernment in 1984 placed an internal quaran- tine on Karnal bunt to prevent disease spread within the country (27). On 8 March 1996, the U.S. Department of Agriculture (USDA) and the Arizona Department of Agriculture announced the discovery of Karnal bunt in Arizona (Release No. 0115.96, Ag News FAX; 56). Efforts were initiated to quarantine suspect Dr. Bonde’s address is: USDA ARS FDWSRU, 1301 Ditto Avenue, Fort Detrick, MD 21702-5023 E-mail: [email protected] Product names are necessary to report factually on available data; however, the USDA neither guar- antees nor warrants the standard of the product, and the use of the name by USDA implies no approval of the product to the exclusion of others that may also be suitable. Publication no. D-1997-1024-01F This article is in the public domain and not copy- rightable. It may be freely reprinted with custom- ary crediting of the source. The American Phyto- Fig. 1. Map of the continental United States showing Karnal bunt–regulated areas in pathological Society, 1997. August 1997. 1370 Plant Disease / Vol. 81 No. 12 and quality losses are considered by many the Department of Defense (DOD) at Fort disease. Only a few kernels of some wheat smut pathologists to be minor (11,51). Detrick (28). The facility is a 12.5 × 53.7 heads are infected, and usually only a por- However, since Karnal bunt is the subject m brick and concrete building with five tion of an infected kernel is replaced with of strict quarantines by several wheat-im- attached 7.6 × 18.3 m glasshouses under fungal sorus (Fig. 3). T. indica is a porting countries, T. indica can profoundly negative air pressure. All waste water is basidiomycetous pathogen belonging to the affect international trade of commercial decontaminated by DOD upon exiting the order Ustilaginales. Black, dusty-appearing grain and the movement of wheat germ- facility. Each glasshouse has double-lay- teliospores give this group of organisms plasm (51). In 1983, the Animal and Plant ered glass panels supported by a steel su- the name “smut.” The life cycle of T. in- Health Inspection Service (APHIS) placed perstructure. With permission of state and dica is depicted in Figure 4. The telio- restrictions on wheat coming from coun- federal regulatory officials, plant patho- spores (Fig. 5) of T. indica are diploid tries with Karnal bunt, recognizing that gens and diseases from anywhere in the (2N), thick walled, globose to subglobose, establishment of Karnal bunt in the United world can be investigated at Bldg. 374 (28). and average 35 µm in diameter (range 22 to States could have major economic ramifi- ARS initiated Karnal bunt research at 49 µm) when mature (27). They are very cations on U.S. wheat exports. The spread Frederick in 1982, after Karnal bunt ap- resistant to adverse environmental condi- of Karnal bunt to the United States and its peared in northwestern Mexico. The Kar- tions, remaining viable for 2 to 5 years in establishment therein could have placed nal bunt research program at Frederick was contaminated soil (27). The pathogen is the country at a marked disadvantage in the the first initiated in the United States and seedborne but is not transmitted directly international wheat market as the first ma- has continued for 15 years. from seed into plant (27). Teliospores of T. jor wheat-exporting country to have Karnal In 1983, ARS initiated cooperative re- indica are considered dormant immediately bunt. As shown by responses following the search projects on Karnal bunt in India and after formation and have poor germination discovery in March 1996 of Karnal bunt in Mexico, and established and maintained a up to approximately 9 months (36). Arizona, and later in California, the disease containment laboratory in Logan, Utah, After a period of dormancy and in the has generated considerable concern and under the direction of James A. Hoffmann. presence of moisture, teliospores at the soil debate both within and outside the country. He and his staff cooperated closely with J. surface germinate (45). During the germi- The American Phytopathological Society Michael Prescott of the International nation process, the nucleus undergoes took the position that Karnal bunt is of Maize and Wheat Improvement Center meiosis followed by several mitotic divi- little agronomic significance and should (CIMMYT), who managed an extensive sions. A promycelium (basidium) grows not be regulated (1). Karnal bunt research program in Mexico. out from the spore, and as many as 180 Since 1972, research on specific foreign This presentation is an overview of Kar- haploid (1N) basidiospores (also known as plant pathogens of major threat to U.S. nal bunt, its importance in international primary sporidia) are produced at the tip agriculture has been a primary objective of agriculture, and past and present research (18,20,36) (Fig. 6). Normally, teliospores the USDA, Agricultural Research Service to better understand and control the disease germinating under 2 mm of soil are inca- (ARS), Foreign Disease-Weed Science and make rational decisions. Recent re- pable of reaching the surface (45). How- Research Unit at Fort Detrick, Frederick, views include Gill et al. (20), Mathur and ever, it is not known whether teliospores Maryland. In 1992, the major objective of Cunfer (27), and Singh (36). A very com- beneath the soil surface germinate. The this program became the development of prehensive literature review was published primary sporidia mean lengths and widths rapid molecular means of detecting and by Warham (51) in 1986. among isolates range from 64 to 79 µm and making accurate, timely identifications of from 1.6 to 1.8 µm, respectively. Sporidia foreign plant pathogens. Because of its Symptoms of Disease germinate to produce mycelia, which in regulatory significance, T. indica was a turn produce large numbers of secondary primary target. and Life Cycle of Pathogen The Frederick unit conducts research on The disease is difficult to detect under foreign pathogens in a plant disease con- fields conditions, and generally only care- tainment facility (Bldg. 374) leased from ful examination will reveal evidence of Fig. 3. Typical wheat head with Karnal bunt infection. Under natural field condi- tions, symptoms are not readily appar- Fig. 2. Arizona Department of Agriculture laboratory in 1997 testing wheat seed sam- ent. Surveying for Karnal bunt infection ples for the presence of Tilletia indica teliospores. In 1996, more than 4,700 wheat requires harvesting the seed and thresh- fields were preharvest and postharvest tested. ing the grain to expose the kernels. Plant Disease / December 1997 1371 sporidia with mean lengths for different nels. Dhaliwal and Singh (14) presented to higher leaves. In this manner, the fungus isolates of 11.9 to 13.0 µm, and a mean evidence that T. indica may travel in steps travels up the plant to reach developing width of 2.0 µm (31). At the time of flow- from the soil surface to susceptible heads. heads. Here, the sporidia on the glumes ering of the wheat plants, primary and According to them, sporidia from the soil germinate and penetrate the stomates if the secondary sporidia are presumably surface germinate on lower plant leaves, plant is in the 2- to 3-week susceptible splashed and blown onto the surface of colonize the leaf surface, and produce fur- period at or near anthesis.