Wheat is a very important source of carbohydrates, proteins, vitamins and minerals. It occupies 27 percent of the total cereal production worldwide. Among the biotic constraints, smut diseases of wheat are important because they affect yield, quality of the wheat grain and subproducts and are subject to domestic and international phytosanitary regulations. Although most of these diseases can be controlled with chemical treatments, in many wheat-producing areas farmers do not follow this practice due to economics and the effect that these chemicals may have on the environment. Breeding for resistance has been a successful research activity and certainly is the best control method in the long term. However, variation in the pathogen may sometimes pose a threat to wheat production. In most cases, the use of clean seed will help to avoid dissemination of the fungal propagules, a practice recommended.
Common bunt is a disease of Triticum species that is caused by two very closely related fungi, Tilletia tritici (syn. T. caries) and T. laevis (syn. T. foetida), which are distributed throughout the world on spring-planted and autumn-planted wheat. Common bunt has also been reported on numerous grasses, but most are considered hosts only in exceptional circumstances (Hardison et al., 1959; Duran and Fischer, 1961). The disease is called stinking smut and hill bunt in some areas. Other than differences in teliospore morphology, the two fungi that cause common bunt are essentially identical. Tilletia tritici teliospores have a reticulate exospore, whereas those of T. laevis are smooth. Teliospores typically are viable for only two years in soil under field conditions but can remain viable for many years on stored seed.
The disease is initiated when soil-borne, or in particular seed-borne, teliospores germinate and eventually produce hyphae that infect germinating seeds by penetrating the coleoptile before plants emerge. Optimum infection occurs when teliospore-laden seed is planted in soil at 5° to 10°C. Only slight infection occurs at 22°C (Purdy and Kendrick, 1963). The intercellular hyphae become established in the apical meristem and are maintained systemically within the plant. Symptoms of common bunt usually are not apparent until after heading when sporulation begins in the young ovary, but infected plants are often slightly stunted. After initial infection, hyphae are sparse in plants but proliferate in the spikes when ovaries begin to form. Sporulation occurs in endosperm tissue until usually the entire kernel is converted into a sorus consisting of a dark brown to black mass of teliospores covered by a modified periderm, which is thin and papery. The sorus is light to dark brown and is called a bunt ball (Plate 24). The spikes are somewhat normal in appearance at maturity except that the kernels are converted into sori. Compact-type spikes tend to become more lax when infected, and infected spikes of most genotypes become at least slightly lighter in colour at maturity (Plate 25). Disease spikes have a conspicuous odour similar to rotting fish. Sori often rupture during harvest and handling, which spreads teliospores on seed and soil, but intact sori can also be found among harvested grain.
When left unchecked, considerable yield losses can occur when the inoculum concentrations are high and the disease conducive conditions are ideal. In addition to yield losses, grain quality is also reduced due to the poor palatability of products made from highly contaminated grain, which causes an off colour and odour in the finished product.
Well-defined pathogenic races have been found among the bunt population, and the classic gene-for-gene relationship is present between the fungus and host (Hoffmann and Metzger, 1976; Goates, 1996). Although in some parts of the world breeding for resistance is an important part of common bunt management, most areas rely on seed treatments for control. Several systemic seed treatment chemicals, such as carboxin, difenoconazole, triadimenol and others, are highly effective for controlling the disease and have eliminated losses where they are commonly utilized (Hoffmann and Waldher, 1981; Gaudet et al., 1989; Williams, 1990). These chemicals adequately control disease that can result from both seed-borne and soil-borne teliospore inoculum. Even where seed treatments are commonly used, a residual amount of inoculum is often still present that can cause disease outbreaks when seed treatments are not used regularly. Hoffmann (1982) and Goates (1996) have presented comprehensive reviews of this disease. Additional information on common bunt is presented in section "Dwarf bunt".
Dwarf bunt, caused by the fungus T. controversa, occurs on autumn-planted wheat and also on numerous genera of winter annual grasses (Hardison et al., 1959; Schuhmann, 1960; Duran and Fischer, 1961; Hoffmann and Waldher, 1964; Ozkan, 1971). The disease has never been reported on spring-planted wheat. Teliospores of the fungus have a reticulate exospore and are similar in appearance to those of T. tritici, which causes common bunt. Tilletia controversa is of quarantine significance to several countries, so differentiation of these two pathogens can be important. Teliospores of T. controversa can be differentiated from those of T. tritici because the reticulations are typically 1.5 to 3.0 µm thick as compared to less than 1.5 µ in T. tritici, and T. controversa teliospores are covered with a conspicuous hyaline gelatinous sheath that is 1.5 to 5.5 µm thick (Duran and Fischer, 1961). In addition to these morphological differences, teliospores of T. tritici germinate on 2 percent water agar within three to five days at 18°C, whereas those of T. controversa will not germinate at this temperature. Teliospores of T. controversa germinate only after incubation for three to six weeks, optimally at 5°C with supplemental lighting under laboratory conditions.
Teliospores of T. controversa have been reported to survive in soil under field conditions for up to ten years (Tyler and Jensen, 1958). Infection occurs during the winter when, after several weeks of continuous cool, humid conditions, the teliospores at or near the soil surface germinate and eventually produce hyphae that infect seedlings. Continuous snow cover best produces these climatic conditions. Most infection occurs during late December to February (Purdy et al., 1963). Dwarf bunt is a soil-borne disease; however, a small amount of infection has been induced in experiments with extremely high levels of seed-borne inoculum (Grey et al., 1986; Goates and Peterson, 1997). The distribution and incidence of dwarf bunt is highly correlated with snow conditions. Significant yield losses occur only after a winter with an extended period of snow cover in areas where relatively high levels of teliospores are present in the soil. The disease has its greatest potential when persistent snow covers unfrozen ground. Dwarf bunt occurs sporadically in several areas of the world, and its geographic distribution and year to year incidence is limited by the special climatic conditions required for infection and establishment in particular areas. Losses in yield and quality caused by dwarf bunt are the same as those described in section "Common bunt".
Disease symptoms can be evident after early spring growth. Infected plants produce an abnormally high number of tillers, and in most genotypes, faint or distinct yellow spots and/or streaks appear in leaves. As plants grow, the culms that produce diseased spikes are shortened in height by about 50 percent (Plate 26). These symptoms are more pronounced when infection is severe. After heading, sori similar to those described for common bunt form instead of kernels. Sori of dwarf bunt are usually more rounded than those of common bunt and tend to flare the glumes, giving the spike a ragged appearance (Plate 27). Other than this, the infected spikes appear some-what normal. It is common for infection to occur in only a few spikes per plant and also in only a portion of the kernels of individual spikes, particularly in resistant genotypes or under marginal climatic conditions. Usually kernels are completely transformed into teliospores, but partially diseased kernels can occur, which appear similar to Karnal bunt disease caused by T. indica. This symptom can also occur in kernels infected with common bunt. Like common bunt, diseased spikes have a conspicuous fishy odour. Sori of dwarf bunt can swell and rupture during a period of wetting, which releases teliospores to the soil. In addition, sori are fragile and can rupture during harvest.
Numerous pathogenic races of the fungus have been identified that follow the classic gene-for-gene system in the host-pathogen relationship (Hoffmann and Metzger, 1976). The closely related common bunt pathogens are regulated in wheat by the same resistance genes. Thus, resistance to dwarf bunt can also confer resistance to common bunt. A very high level of resistance has been incorporated into several commercial cultivars in the United States that are commonly grown where the disease has the greatest potential (Goates, 1994). These resistant cultivars have eliminated yield and quality losses in areas of the United States that historically had the worst disease incidence. The primary source of this resistance has continued to be effective for about 25 years. In addition, new high-yielding cultivars are available in the United States, which have additional sources of resistance that are highly effective (Souza et al., 1995). In the United States, there is no known virulence to any of these sources of resistance; however virulence against these sources has been detected in some isolates from Eastern Europe. Goates (1998) has presented a comprehensive review of host resistance to dwarf bunt.
Most of the common seed treatment chemicals that control other smuts and bunts are ineffective at controlling dwarf bunt because infection occurs months after seeds germinate when the chemical has become too dilute. However, the registered seed treatment chemical difenoconazole is extremely effective at low application rates (Goates, 1992; Sitton et al., 1993). Informative reviews of dwarf bunt are included in Hoffmann (1982) and Goates (1996).
Karnal bunt or partial bunt, caused by T. indica (syn. Neovossia indica [Mitra] Mundkur) occurs endemically in India (Mitra, 1931), Pakistan (Munjal, 1975) and Mexico (Duran, 1972). It has also been detected in Nepal (Singh et al., 1989) and the United States (APHIS, 1996). Karnal bunt occurs naturally on bread wheat (T. aestivum) (Mitra, 1931), durum wheat (T. turgidum) and triticale (X Triticosecale) (Agarwal et al., 1977). Moderate temperatures, high relative humidity or free moisture, cloudiness and rainfall during anthesis favour disease development (Mundkur, 1943a; Bedi et al., 1949; Aujla et al., 1977). Not all spikes of a plant are affected (Mitra, 1935; Bedi et al., 1949), and usually only a few irregularly distributed kernels are bunted. Infection of individual kernels varies from small points to complete infection. Affected kernels are usually partially infected (Plate 28), and completely infected ones are rare. The embryo is largely undamaged except when infection is severe. In infected spikelets, the glumes may be flared to expose bunted kernels (Plate 29), which reek of an odour similar to rotten fish caused by trimethylamine (Mitra, 1935).
Despite the fact that an increase in disease severity results in proportional decrease in seed weight (Singh, 1980; Bedi et al., 1981), yield losses are generally light (Brennan et al., 1990). Although Karnal bunt affects flour quality (colour, odour and palatability), levels of 1 to 4 percent infected grains could be used for human consumption (Mehdi et al., 1973; Sekhon et al., 1980; Amaya, 1982; Medina, 1985; Hussain et al., 1988). If grains are washed and steeped, wheat lots with 7 to 10 percent infected grains are acceptable for consumption (Sekhon et al., 1981; Medina, 1985; Hussain et al., 1988).
Teliospores of the fungus are brown to dark brown, spherical, subspherical or oval and 22 to 42 µm x 25 to 40 µm in diameter (average is 35.5 µm, but some may be 55 µm). They occasionally have an apiculus (Roberson and Luttrell, 1987), papilla (Mitra, 1931) or a vestige of attached mycelium (Duran and Fischer, 1961). Though each teliospore generally produces one promycelium (Mitra, 1931), several promycelia may arise from a single teliospore and may be branched (Mitra, 1931; Krishna and Singh, 1981; Warham, 1988; Rivera-Sánchez and Fuentes-Dávila, 1997). Promycelia vary in length up to 1 500 µm and bear at the apex a whorl of 32 to 128 or more primary sporidia (Mitra, 1931; Holton, 1949). Variation in the enlargement of promycelial tips may occur. Primary sporidia are filiform, 64.4 to 78.8 µm long and 1.6 to 1.8 µm wide (Peterson et al., 1984). Primary sporidia germinate terminally or laterally to produce hyphae or sterigmata from which secondary falcate sporidia, 11.9 to 13 µm long and 2 to 2.03 µm wide (Peterson et al., 1984), are formed and forcibly discharged (Fuentes-Dávila, 1984). Falcate secondary sporidia produce hyphae or other sporidia by repetition. Hyphae that originate from primary or secondary sporidia produce large numbers of secondary, mononucleate falcate sporidia and somewhat fewer secondary filiform sporidia (Fuentes-Dávila, 1984). H-bodies are not formed by T. indica (Mitra, 1931).
During teliospore germination, meiosis occurs and the haploid nuclei migrate into the promycelium and primary sporidia, each of which receives one nucleus (Fuentes-Dávila and Duran, 1986). After one or two mitoses, most sporidia become septate, forming two to four monokaryotic cells. Most secondary sporidia are mononucleate. Mycelial cells that originate from either type of sporidia are also mononucleate. After anastomosis, the dikaryotic sporogenous mycelium bears intercalated Y-shaped septa formed at the base of the probasidial initials. Nuclei migrate to the teliospore initials, which enlarge to form the teliospores, and the nuclei presumably fuse to form a diploid nucleus (Fuentes-Dávila and Duran, 1986; Roberson and Luttrell, 1987).
Tilletia indica is heterothallic; heterothallism and pathogenicity are controlled by four alleles at one locus (Duran and Cromarty, 1977; Fuentes-Dávila, 1989). Solopathogenic lines have not been found. Although the site of dikaryotization in T. indica is not known, sporidial germ tubes penetrate stomata in the rachis (Dhaliwal et al., 1989), glumes, lemma and palea (Goates, 1988; Salazar-Huerta et al., 1990). Most freshly collected teliospores are dormant, as indicated by the failure of fresh teliospores to germinate (Mitra, 1931; Bansal et al., 1983; Smilanick et al., 1985a). The highest germination occurs with one-year old teliospores (Mathur and Ram, 1963; Kiryukhina and Shcherbakova, 1976). Teliospores germinate at 5° to 30°C (Mitra, 1935; Bansal et al., 1983; Krishna and Singh, 1982a; Zhang et al., 1984; Smilanick et al., 1985a; Dupler et al., 1987). Germination has been reported after 4 to 12 weeks at -30°C (Zhang et al., 1984). Optimum temperature for teliospore germination is between 15° and 25°C (Mitra, 1935; Mundkur, 1943b; Holton, 1949; Mathur and Ram, 1963; Duran and Cromarty, 1977; Zhang et al., 1984). Teliospores germinate between pH 4 and 11, the optimum being between pH 6 and 9.5 (Krishna and Singh, 1982a; Smilanick et al., 1985a). Teliospores also germinate after ingestion by livestock and grasshoppers, providing another means of dissemination (Smilanick et al., 1985b). Teliospores are viable in the laboratory for five to seven years (Mathur and Ram, 1963; Kiryukhina and Shcherbakova, 1976). Teliospores in unbroken sori and buried 8 or 15 cm in field soil or left on the soil surface can remain viable for 27 to 45 months (Krishna and Singh, 1982b). During harvest, sori may brake, and teliospores may contaminate healthy seed, soil, machinery or vehicles and may be blown by the wind for long distances. Viable teliospores were found up to 3 000 m over burning wheat fields (Bonde et al., 1987).
Since the 1940s, some cultivars of T. aestivum, T. turgidum, T. dicoccum and X Triticosecale have been reported to be resistant to Karnal bunt under field conditions in India (Bedi et al., 1949; Gautam et al., 1977; Meeta et al., 1980; Singh et al., 1986). Artificial inoculations have shown resistance among experimental lines and cultivars of Triticum, Triticosecale and grass species (Aujla et al., 1980; Warham et al., 1986; Royer and Rytter, 1988; Fuentes-Dávila et al., 1992; Fuentes-Dávila and Rodriguez-Ramos, 1993). Outstanding geographic groups for Karnal bunt resistance originate from China, India and Brazil (Fuentes-Dávila and Rajaram, 1994). In addition, some wheat lines developed by the International Maize and Wheat Improvement Center (CIMMYT) and some cultivars from other countries, such as Chris from the United States and Impeto from Italy, are resistant (Fuentes-Dávila and Rajaram, 1994). In 1992, resistant bread wheat cultivar Arivechi was released for commercial use by the Mexican national programme (Camacho-Casas et al., 1993); two more cultivars (Inifap and Tobarito) were released in 1997.
Studies on the mode of inheritance and allelic relationship among genes conferring Karnal bunt resistance in bread wheat have indicated two partially recessive and four partially dominant genes (Fuentes-Dávila et al., 1995). Other studies indicate polygenic and partially dominant genes; resistance genes are dispersed on chromosomes 1D, 2A, 3B, 3D, 5D and 7A (Gill et al., 1993). Several artificial inoculation methods have been used successfully to reproduce the disease (Bedi et al., 1949; Chona et al., 1961; Duran and Cromarty, 1977; Aujla et al., 1980; Goates, 1988). Disease scoring is primarily based on the percentage of infected kernels (Singh and Krishna, 1982; Aujla et al., 1982; Fuentes-Dávila and Rajaram, 1994). Lines are considered to be resistant when kernel infection percentage is below 5 percent in ten inoculated spikes after several tests (Fuentes-Dávila and Rajaram, 1994). Also used is a rating scale that considers the size of the lesion in the kernel, the number of kernels in each category and the total number of kernels (Aujla et al., 1989).
High rates of nitrogen applications, as well as heavy manuring, may increase disease incidence (Bedi et al., 1949; Aujla et al., 1981; Ortiz-Monasterio et al., 1993). In repeated experiments, Ortiz-Monasterio et al. (1993) found that disease incidence would increase with nitrogen applications during sowing compared to split applications. Karnal bunt incidence was also greater when wheat cultivars were sown in flats instead of beds, and some cultivars showed a direct correlation between plant density and disease incidence. Hot water and solar energy treatments have been applied to Karnal bunt infected seeds. However, they have had limited application. These treatments inhibit teliospore germination, but not as much as fungicide treatments (Mitra, 1937). Fungicide seed treatments have been investigated for Karnal bunt control since the 1930s (Mitra, 1935). Although many fungicides have been tested for effectiveness, results have not been completely satisfactory (Fuentes et al., 1982; Aujla et al., 1986; Figueroa-Lopez and Espinoza-Salazar, 1988; Warham and Prescott, 1989). A number of fungicides have been tested in foliar applications since the 1970s, and all have had positive results (Krishna and Singh, 1982b; Singh et al., 1985; Salazar-Huerta et al., 1986; Smilanick et al., 1987). For teliospores buried in soil, methyl bromide reduced teliospore germination almost 100 percent, when applied in wet soil and with plastic cover (Smilanick and Prescott, 1986; Fuentes-Dávila and Lawn, 1992).
Loose smut, caused by Ustilago tritici (Persoon) Rostrup, occurs wherever cultivated wheat (T. aestivum and T. turgidum) is grown (Anonymous, 1982). It is more common in regions with a cool, moist climate during flowering of the host. Since the pathogen is seed-borne, humans are the principal means of dissemination The disease is not devastating, but causes low to moderate losses. However, even in dry, warm climates economic losses occur. Ustilago tritici has been found on all Triticum spp. except T. timopheevii. Some races that are specialized on bread or durum wheats are pathogenic on some Aegilops spp., while most races on Aegilops spp. are not pathogenic on Triticum spp. (Nielsen, 1985). The fungus is also pathogenic on rye (Secale cereale L.) (Humphrey and Tapke, 1925) and triticale (X Triticosecale) (Nielsen, 1973). In nature, U. tritici is rare on wild grasses other than Aegilops spp. There are two reports of natural occurrence on Agropyron spp. in North America, and one report each on Elymus and Taeniatherum spp. in Morocco (Nielsen, 1978). Ustilago tritici is also pathogenic on Haynaldia, Hordeum and Secale spp.
Teliospores are light olivaceous-brown with one side lighter, globose to ovoid and 4 to 6 µm in diameter. Mature spores are raspberry-shaped, and the exospore is finely echinulate. Teliospores do not exhibit dormancy. During germination, the diploid nucleus divides meiotically, then mitotically, and a slender, slightly curved promycelium emerges on the lighter coloured side of the spore. It consists of four cells, each with a single haploid nucleus. These cells may divide before producing a short hypha within 18 hours at 20°C, which is the optimum temperature for germination, in either light or darkness.
Ustilago tritici is heterothallic and bipolar. Haploid monokaryotic hyphae, or a mycelium that has developed from it, can be either MAT-1 or MAT-2 mating types. Teliospores enter the floret, germinate and form dikaryotic hyphae that infect the ovary, usually at the brush end (Batts, 1955a; Shinohara, 1976). Once in the testa, hyphae grow intracellularly; but in the integument and nucellus, the fungus grows intercellularly, mainly on the dorsal side of the developing caryopsis. The mycelium enters the upper and side parts of the scutellum 10 to 15 days after penetration and grows through the hypocotyl into the plumular bud, or growing point of the embryo, where it will lie dormant in the mature seed. When the seed germinates, the mycelium is revitalized and carried in the crown node as the subcrown internode elongates. The fungus permeates crown tissues and enters the initials of the inflorescence (Batts and Jeater, 1958a).
The optimum temperature for teliospore germination and further growth is 20° to 25°C and 95 percent relative humidity (Danko and Michalikova, 1969). Excessive heat or dry air will lower germination and germ tube growth, delay penetration of the ovary and preclude the fungus from reaching the growing point. The environment can also cause florets to stay open for a shorter time, which will reduce spore entry (Tapke, 1931; Atkins et al., 1963).
The dikaryotic nuclei fuse to form a diploid nucleus as the teliospores mature. At emergence of the spike, the teliospores are readily carried by the wind to nearby florets, where they germinate and cause infection. Masses of teliospores are seen when the spike emerges from the boot with nearly all tissue of the spikelets affected (Plate 30). Only the rachis is intact, but it may be slightly shorter than the rachis of a healthy tiller. Rain or heavy dew can cause the spores to cake into a black, hardened mass as will a severe drought in the late stages of spore formation. Narrow linear sori form only rarely on the flag leaf, the leaf sheath, or the peduncle (Klushnikova, 1928; Batts and Jeater, 1958a). The number and dry weight of roots are reduced along with the number, height and dry weight of tillers.
After heading, plants with sporulation stop growing. The lower internodes are usually longer and the upper ones shorter than in healthy plants, but the peduncle of the spike with sporulation is much shorter. The leaf sheaths of some infected cultivars are greyish-purple; the leaves, particularly the flag leaf, are reduced in size, often yellowed and senesce early (Tingey and Tolman, 1934; Mather and Hansing, 1960; Gaunt and Manners, 1971; Gothwal, 1972a). Under some environmental conditions, sporulation may be confined to the lower part of the spike. Certain cultivars respond to infection with hypersensitive (Oort, 1944) or incompatible (Mantle, 1961a) reactions. Seedlings may die before emergence; others emerge but are stunted and have leaves that are brittle, often distorted, dark green and with necrotic tips. Seedlings developing from infected kernels are often weak and succumb to adverse environmental conditions, such as low soil temperature, drought, compacted soil, deep seeding and waterlogging (Mantle, 1961b).
Races of the fungus are determined by inoculating a series of differential cultivars. Several sets of differentials have been used in different countries (Tiemann, 1925; Piekenbrock, 1927; Grevel, 1930; Oort, 1947; Bever, 1953) based on reactions of local cultivars to local collections of the pathogen. The set most widely used is that of Oort (1947). The present set of spring wheat differentials (Nielsen, 1987; Nielsen and Dyck, 1988) contains 19 cultivars or lines, of which only five were originally proposed by Oort (1947). Resistance may be recognized by the absence of sporulation due to few penetrations of the ovary wall and little or no mycelium in the pericarp. The mycelium might become widely established in the pericarp, but there are few or no hyphae in the scutellum; hyphae may permeate the scutellum and may be found in the hypocotyl, but are absent in the growing point (Batts and Jeater, 1958a, 1958b; Mantle, 1961c, 1961d; Gaskin and Schafer, 1962). Krivchenko (1984) listed 52 genes for resistance to loose smut in 34 bread wheat cultivars or lines; some carried up to three genes. Most genes were dominant, 11 were recessive. The gene-for-gene relationship postulated by Flor (1947) exists in the U. tritici/Triticum pathogen-host system (Oort, 1963). It has been proposed that 11 genes for virulence correspond to 11 dominant genes for resistance (Tikhomirov, 1983). Some cultivars may have field resistance (Tyler, 1965; Nielsen, unpublished) due to smaller lodicules and a smaller angle of opening for the palea and lemma during flowering than in susceptible ones (Tavcar, 1934). Cultivars also differ in the length of time florets stay open, in the proportion of florets that do not open at all and in the extrusion of anthers (Ryzhei, 1960; Parii, 1973; Loria et al., 1982; Pandey and Gautam, 1988).
Early control means on wheat seed involved the use of warm water, alone or in combination (Tyner, 1953; Weibel, 1958) with ethanol (Gassner and Kichhoff, 1938), or mercurial seed treatment fungicides (Rodenhiser and Stakman, 1925; Bever, 1961), and anaerobic treatments (Zalesskij, 1935; Zemanek and Bartos, 1964). The 1,4-oxathiin derivatives are systemic, absorbed by plant tissue and translocated to the site of action on the mycelium of the pathogen (von Schmeling and Kulka, 1966; Hansing, 1967). The compounds, which dissolve in soil moisture and penetrate and spread throughout the hydrated embryo and the very young seedling, interfere with essential metabolic processes in the mycelium. Fungicides efficacious against loose smut include: carbathiin, carboxin, benomyl, difenoconazole, etaconazole, ethyltrianol, flutriafol, furmecyclox, myclobutanil, nuarimol and triadimenol. Proper and rigorous cleaning will remove many of the small kernels, and the crop will have less infection. Roguing infected plants as early as possible has been recommended, particularly in small isolated seed increase plots (Maddox, 1896; Freeman and Johnson, 1909). Seed certification schemes specify the incidence of loose smut infected plants at inspection of a field producing pedigreed seed. The tolerance level varies between 0.01 percent and 0.05 percent infection, with different levels for different classes of seed. Other tests have involved the inflorescence of whole or dissected kernels (Yablokova, 1939; Woestmann, 1942). Seed certification can be based on the embryo or crown test to determine the incidence of infection in a seed lot. The various embryo and crown tests use staining of whole embryos, (Skvortzov, 1937; Simmonds, 1946; Popp, 1958; Khanzada et al., 1980; Agarwal et al., 1981) or longitudinal sections, to detect the mycelium of the pathogen (Yablokova, 1939; Woestmann, 1942).
For artificial screening of wheat, a suspension of teliospores in tap water has, over the years, proven to be the most reliable and practical inoculum (Nielsen, 1987). For maximum infection, inoculate the host at early to midanthesis (growth stages 60 to 65) (Zadoks et al., 1974; Freeman and Johnson, 1909; Piekenbrock, 1927; Stringfield, 1929; Tapke, 1929; Oort, 1939; Batts, 1955b; Rod, 1958; Gothwal, 1972b). Most field inoculation methods have been developed to simulate natural conditions. Dry spores are introduced into the florets with forceps or a small brush, with a puff of air over a tiny piece of paper or on a ball of cotton containing spores, or by dusting spores over entire spikes (Maddox, 1896; Brefeld and Falck, 1905; Freeman and Johnson, 1909; Grevel, 1930; Mishra and Jain, 1968). To provide better access to the ovary, the tips of the florets are clipped. Other inoculation methods include: partial vacuum (Moore and Munnecke, 1954; Cherewick and Cunningham, 1956; Nielsen, 1983), go-go technique, air blast (Moore and Munnecke, 1954) and vacuum (Cherewick and Popp, 1950). Storing the spores at about 4°C will keep them viable for at least five years. Spores dehydrated and sealed under vacuum (Vander-walle, 1953) will remain viable much longer if stored in a refrigerator or freezer. For even longer preservation, the races can be kept as dormant mycelia in inoculated seed.
Flag smut, caused by Urocystis agropyri (Preuss) Schroter, has been reported from Australia, Chile, China, Egypt, India, Japan, Mexico, Pakistan, South Africa and the United States (Purdy, 1965; Anonymous, 1991). However, during the past twenty years, the only reports and research have been in Australia, China, India, Pakistan and Washington State in the United States. The most widespread and severe losses reported were in Australia earlier this century when popular cultivars were very susceptible and efficient chemical control was not available (Ballantyne, 1996). While a range of Triticum species and grasses have been listed as susceptible to U. agropyri, some of these reports involved a form of flag smut that does not infect wheat (Fischer and Holton, 1943; Purdy, 1965). It is unusual for a non-wheat host to be a potentially important source of infection (Rees and Platz, 1973).
Flag smut infects seedlings only during a limited period, until the first leaf breaks through the coleoptile (Griffiths, 1924). Soil type, moisture, temperature and sowing depth affect the incidence of the disease by influencing the seedling germination and emergence rates. Any factor that slows emergence may increase flag smut incidence. The influence of the time of sowing depends on the wheat-growing regime used. In some regions, the temperatures present in early sowings may be unfavourable for the disease, but in others may favour its development. Hence, the circumstances of each geographic area need to be considered. As a general rule, flag smut occurs more frequently in light, relatively dry soils in the 18° to 24°C temperature range (McAlpine, 1910; El-Helaly, 1948; Purdy, 1965, 1966; Greenhalgh and Brown, 1984).
Teliospores on the seed or in soil provide the inoculum. The apical cells of dikaryotic infection hyphae form appressoria with penetration pegs that enter directly through the epidermis. The pathogen infects both resistant and susceptible plants, but symptoms develop only in susceptible genotypes. The fungus grows intercellularly and intracellularly, ramifying through almost all plant parts. Sporulation occurs between the epidermal layers and the vascular tissues of the plant (Noble, 1924; Verwoerd, 1929; Nelson and Duran, 1984). Infected seedlings are twisted and bent (Plate 31). Older plants may have a large number of thin, stunted, wilted and yellowish-green leaves. Symptoms may develop any time after the third or fourth leaf, but are usually not seen until after flowering and are most obvious at the end of the season on late tillers. The leaves show white striations, which occasionally extend into the inflorescence (Plate 32). The striations change from white to shades of grey to black. Infected plants produce increased numbers of stunted, twisted and distorted tillers and may not develop seed heads (Angell, 1934a, 1934b; Miller and Millikan, 1934).
Spore balls produced on diseased leaves dislodge during harvest and fall to the ground. A dark brown to black dust may be seen behind harvesters in heavily infected wheat. The spores attach to seed, enter the soil and are blown by wind to adjacent fields. They may also be spread in animal manure, on the hooves of animals, in irrigation water and in straw used for packing (McAlpine, 1910; Putterill, 1920; Clayton, 1925; Miller and Millikan, 1934). The spore ball comprises up to six (usually three) hyaline or lightly tinted teliospores surrounded by flattened, sterile peripheral cells. The teliospores are globose to sub-globose, reddish to olivaceous and 8 to 8 µm in diameter (Mordue and Waller, 1981). They are resistant structures, surviving for four to seven years in soil and at least ten years in the laboratory, when stored at low humidity at 13° to 31°C (Noble, 1924; Sattar and Hafiz, 1952). They are still viable after passage through the digestive systems of horses and cattle (Clayton, 1925). The dormancy of recently formed teliospores may be broken by various chemical and physical treatments, but as a general rule, they germinate capriciously (McAlpine, 1910; Griffiths, 1924; Allan and Duran, 1979; Goel and Jhooty, 1987). Upon germination, they produce a promycelium that is 23 to 29 x 4.5 µm in size with two to five protuberances forming on the tip and developing into clusters of sporidia measuring about 25 x 4.5 µm (Noble, 1923, 1924; Griffiths, 1924; Verwoerd, 1929; El-Khadem et al., 1980; Nelson and Duran, 1984; Goel and Jhooty, 1986).
While the flag smut pathogen has shown less physiologic specialization than any other cereal smut, variation has been reported in collections from China, India, Pakistan and, to a lesser extent, from the United States. No pathogenic variation was detected in Australian isolates (Watson, 1958) despite surveying after many years of several epidemics providing heavy selection pressure. Studies on variation in the flag smut pathogen need cautious interpretation because of variation in the incidence of infection at different sites and in different seasons. Such research has been resource intensive because of the need to grow relatively large wheat populations to maturity and to have uniformity of inoculum and environmental conditions at germination and infection. A recent summary of pathogen variation surveys noted similarities in the responses of certain host testers and collections (certain of the testers were common to several studies), suggesting that the extent of variation may be more modest than previously claimed (Ballantyne, 1996). The reaction patterns suggested 12 groups in China (Yu et al., 1936, 1945), at least four in Pakistan (Hafiz, 1951) and about eight groups in collections from Australia, Chile, China, India, Japan and the United States (Johnson, 1959). Certain of the isolates from China, Pakistan and India were virulent on wheats resistant to Australian and North American isolates. This raises the possibility that the primary centre of origin of the flag smut pathogen was Asia. Australia was a possible secondary source early this century, when the very susceptible cultivars Federation and Baart were exported to and later grown in the Pacific Northwest of the United States, India, Chile and Peru (Ballantyne, 1996).
Selection for resistance has not been reported as a high priority in any breeding programme. While advanced breeding lines have been screened, especially in Australia, and the flag smut reaction may be given in the cultivar description (for an example in the United States, see Mackay, 1995), the escape rate in large-scale trials is significant. Many researchers have reported that resistance is widespread (summarized in Ballantyne, 1996). For example, in recent Indian (Goel and Gupta, 1990; Beniwal and Karwasra, 1996), Pakistani (Tariq et al., 1992) and Australian (Ballantyne, 1993) trials, many local cultivars and parents showed resistance. Semidwarf wheats and club wheats were more susceptible to flag smut (Allan, 1975; Allan and Pritchett, 1976) probably because of the delayed emergence typical of these traits. Most durum wheats screened have been resistant (Goel and Gupta, 1990; Ballantyne, 1993). Resistance is generally controlled by a number of genes and transgressive segregation is common (Shen et al., 1938; Helm and Allan, 1971; Goel, 1991a 1991b).
A range of modern systemic fungicides control flag smut. Certain chemicals are effective against the seed-borne phase only (for example, carboxin). However, others control both soil- and seed-borne inoculum (for example, triazoles, tebuconazole, triadimenol and carbozanilides-flutriafol). The main impetus for seed treatment of wheat has been for the control of bunt, a more widespread and destructive problem. The chemicals applied for control of bunt have generally been effective against flag smut. Exceptions are benomyl and pentachloro-nitrobenzene, which are less effective against flag smut than bunt (Cass Smith, 1954; Purdy, 1957, 1961, 1963, 1965; Line, 1972; Holton and Purdy, 1954; Kuiper, 1968; Metcalfe and Brown, 1969; Moore and Kuiper, 1974; Kuiper and Murray, 1978; Line and Scott, 1987; Loughman, 1989; Gammie, 1998).
Cultural practices, which can assist in control, include rotations with non-host crops for a longer period than for other diseases, stubble burning, shallower sowing and variations in planting time, which will be dependent on the wheat-growing regime (Brown, 1975; Ballantyne, 1996). Care in introducing seed is important as there is potential for flag smut to be brought into other geographic regions and to become destructive should very susceptible cultivars be grown on a large scale.
As new improved cultivars of unknown response to flag smut are introduced around the world, it is desirable that people in the wheat-growing industry realize that it is a potentially serious problem, are aware of its symptoms, look for the disease and, where appropriate and feasible, determine the response of the main cultivars to the local pathotype(s). Any production area with a significant area of a very susceptible cultivar is vulnerable, especially if flag smut has ever caused problems in the past. A range of inoculation methods has been used in trials to screen cultivar reaction and fungicide efficiency. For large-scale trials, inoculation of seed, mixing inoculum with soil before planting, spraying inoculum on the open row and planting in soil where a very susceptible cultivar was grown the previous season after inoculation have been used (Miller and Millikan, 1934; Line and Scott, 1987; Loughman, 1989; Ballantyne, 1993). McIntosh (1968) and Greenhalgh and Brown (1984) used precise methods for smaller scale tests.
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