Pyrenophora tritici-repentis (leaf spot of wheat)

Reduced tillage methods that leave exposed stubble have promoted the incidence of this disease in Germany (Wolf and Hoffmann, 1995; Garbe, 1994), Australia (Queensland) (Rees and Platz, 1978; Freebairn, 1986) (north-eastern Australia and Western Australia) (Murray and Brown, 1987), (Hermitage Research Station) (Marley and Littler, 1989) and the USA (Wiese, 1987; Schuh, 1990). In a detailed study (Zhang and Pfender, 1992) representative of many other experiments, the effect of some cultural practices were assessed relative to the development of over-wintering ascomata of P. tritici-repentis. One treatment - no-till was left with 35-40 cm stubble after combe harvesting and the straw was evenly dispersed in the rows. A second treatment - mowed - was mowed with a rotary mower set at 5 cm. The third treatment - disked - was like 'mowed' but cultivated once with a chisel plough and once with a disc. Measurements were made of the numbers of ascomata in threshed straw near the soil surface and above the soil surface; the 35-40 cm stubble left in 'no-till' was examined in the region close to the soil and the upper region. Ascomata were severely reduced in numbers when straw contacted soil in all treatments and the upper region of standing stubble had significantly more ascomata than the region near the soil surface (Zhang and Pfender, 1992). These results (Zhang and Pfender, 1992) related decreases in the primary infection ascomata to increased water content and presumed increased activity of biological antagonists (Zhang and Pfender, 1993). Summerell and Burgess (1989b) found that water levels influenced survival of P. tritici-repentis in straw at various temperatures and that there was a succession of fungi that replaced the tan spot organism. Summerell and Burgess (1989a) found that burial of infected stubble was more effective than incorporation by a rotary hoe in reducing recovery of fertile ascomata and that recovery was less on variety Kite, which decomposes rapidly, compared with the more durable variety Suneca. Summerell et al. (1988) found that stubble burning was the most effective method of control followed by incorporation of stubble in the soil. Pfender and Wootke (1987) considered the potential of nutrient competition as a control strategy.Bockus and Claasen (1992) found, in Kansas, USA, that mouldboard ploughing reduced tan spot in continuous wheat rotations as effectively as did a wheat-sorghum rotation with a 15-month break between wheat crops but chisel ploughing, V blade, and no-till produced no comparable reduction in disease. Sutton and Vyn (1990) found, in Ontario, Canada, that zero or minimum tillage increased tan spot of wheat. Jones et al. (1990) found in Morocco, that tan spot of durum wheat was influenced by added N; one susceptible variety exhibited less disease while the other exhibited more. Three-year rotation with non-grass crops and elimination of weedy grass hosts and volunteer wheat is recommended (Wiese, 1987). Stubble mulch and minimum tillage practices may increase disease (Wiese, 1987). Wide row spacing with adequate but not excessive fertilization is recommended (Wiese, 1987).Under conventional tillage in southern Indiana, USA, the severity of tan spot decreased and the rate of lesion development was decreased while yield increased with increased N rate (Luz and Bergstrom, 1986). However, Bockus and Davis (1993) found that application of nitrogen fertilizers did not produce consistent differences in disease severity or yield loss from tan spot but N fertilizers appear to reduce disease by delaying natural leaf senescence with no direct effect on tan spot.

A major emphasis for control of this disease has been through breeding resistant cultivars. Two major symptom types occur: tan, a restricted elliptical, tan, necrotic, lesion with a yellow margin and chl(orotic), an extended yellow streak (Lamari and Bernier, 1991). Some varieties of wheat exhibit 'tan', while others exhibit 'chl' and still others exhibit neither symptom. Some strains of the fungus are designated 'nec-chl+' and induce chlorosis. Other strains designated 'nec+chl-' produce tan necrotic lesions. F1, F2 and F3 generations derived from the three classes of wheat were studied. Resistance to tan necrosis was recessive. Resistance to chlorosis was dominant to incompletely dominant. The F2 and F3 ratios were consistent with the action of two independent genes, one controlling the development of tan necrosis and one controlling extensive chlorosis (Lamari and Bernier, 1991). The Mendelian nature of wheat reaction to P. tritici-repentis (Lamari and Bernier, 1991, 1989c) was confirmed in a comprehensive study involving all the reported virulent races of the pathogen (races 1, 2, 3 and 5). Ptr ToxA (formerly Ptr necrosis toxin) produced by isolates of races 1 and 2, and PtrToxB (formerly Ptr chlorosis toxin) produced by isolates of race 5, were used as surrogates for their producing races when seedlings were tested for reaction to two or three races simultaneously. Susceptibility was always found to be dominant (Sykes and Bernier, 1991; Stock et al., 1996).Three independently inherited loci were identified in hexaploid wheats: one locus controlled reaction to necrosis induced by races 1 and 2 and Ptr ToxA, one locus controlled reaction to race 5 and Ptr ToxB, and a third locus controlled reaction to race 3 (Gamba et al., 1998). In tetraploid wheats, four independently inherited loci were identified; one locus controlled reaction to races 1 and 2 and Ptr ToxA and is believed to be the same locus as in hexaploid wheats (Gamba and Lamari 1998). The remaining three loci appear to be specific to the tetraploid wheat lines used in the study.Faris et al. (1997) found that one region in wheat chromosome 1BL and one in chromosome 3BL were significantly associated with resistance to extensive chlorosis. Shabeer et al. (1991) found evidence of cytoplasmic or maternal determinants in resistance that play a relatively small role in determining resistance.The wheat gene conferring insensitivity to the toxin produced by the 'tan' isolates resides in the long arm of chromosome 5B and the symbol 'tsn1' was proposed for this gene (Faris et al., 1996; Stock et al., 1996). After evaluation of a number of genetic models (Carson, 1987), it was concluded that wheat resistance to P. tritici-repentis is stable and that the most aggressive pathogen isolates should be used in screening for resistance.

There appear to be two basic types of lesions formed on wheat leaves. The 'tan' lesion is elliptical with tan, necrotic centre and a yellow halo. The 'chl' is yellow and becomes more elongated than the 'tan' lesion.The necrosis ('tan') toxin is a protein with an isoelectric point near pH 10 and consists of 13% alpha-helix, 36% antiparallel beta-sheet, 25% turns and 25% other structures (Zhang et al., 1997). The toxin is a 14 kDa protein (Ballance et al., 1996). The host selective toxic protein designated ToxA is a 13.2 kDa heat-stable protein that induces visible necrosis in sensitive wheat cultivars at an av. min. concentration of 60nM (Tuori et al., 1995). Other less abundant necrosis inducing toxins were detected as well (Tuori et al., 1995). Ballance et al. (1989) found the toxin MW to be 13,900, determined the amino acid content and molar extinction, and found 10-13-10-14 mols of purified toxin will produce necrosis in susceptible cultivars. However, Tomas et al. (1990) found a necrosis toxin with MW 14,700 that caused symptoms on susceptible plants at 90 nM. The 'nec' toxin is heat labile at 120°C for 20 min. (Lamari and Bernier, 1989). The necrosis-inducing toxins characterized and named differently by the various groups represented in fact the same protein (100% homology in amino-acid sequence). Evidence was provided by the cloning of its encoding gene by two independent research groups (Ballance et al., 1996; Ciuffetti et al., 1997). To prevent a repetition of this situation, tan spot researchers agreed on a common and chronological naming of the existing and future host-specific toxins from P. tritici-repentis (Ciuffetti et al., 1998). Ptr necrosis toxin, ToxA and Ptr toxin are now referred to as Ptr ToxA. Ballance et al. (1996) showed by Southern analysis that the gene encoding Ptr ToxA was present in isolates of races 1 and 2, which is are the only races capable of inducing necrosis in Ptr ToxA-sensitive wheat genotypes. This gene is absent from all the other races. Ciuffeti et al. (1997) also found that the the gene encoding Ptr ToxA was absent in tox- isolates and showed, by transformation, that this gene was sufficient to confer virulence (ability to induce necrosis) to an avirulent isolate. The toxin causes enhanced electrolyte leakage in sensitive wheat lines (Kwon et al., 1996). The toxin is detectable in intercellular washing fluid of leaves infected with nec+ isolates (but not with nec-isolates) and on both susceptible and resistant cultivars (Lamari et al., 1995). When tested on susceptible wheat genotypes both the 'nec' and 'chl' host resistance increased at temperatures of 27 and 30°C compared with 25°C and below (Lamari and Bernier, 1994). The 'nec' toxin was ineffective on Glenlea plants kept at 30°C (Lamari and Bernier, 1994).A second host-specific toxin (Ptr ToxB, formerly Ptr chlorosis toxin) was identified in culture filtrate and spore germination fluid of isolates from race 5 (Orolaza et al., 1995). Ptr ToxB causes chlorosis in wheat genotypes, which develop chlorosis to race 5 isolates. This toxin was purified, characterized and found to be a protein with a MW of 6.61 kDa (Strelkov et al., 1999). The amino-acid sequence revealed that Ptr ToxB has no homology with Ptr ToxA. Work on the mode of action of Ptr ToxB revealed that this toxin was associated with chlorophyll degradation and had no effect on chlorophyll synthesis (Strelkov et al., 1998). The action of the toxin was found to be light-dependent; the chlorophyll degradation pattern was consistent with photooxidation. Both Ptr ToxA and Ptr ToxB are required for the establishment of compatible interactions with susceptible wheat genotypes, carrying the matching 'susceptibility' dominant gene. This attribute of host-specific toxins makes them very powerful tools for screening wheat germplasm and segregating populations for resistance to their respective producing races, as has been conclusively demonstrated by several studies (Lamari and Bernier, 1989c; Orolaza et al., 1995; Gamba and Lamari, 1998, Gamba et al., 1998). A low molecular weight toxin was reported by Hunger and Brown (1993) and shown to cause severe and moderate chlorosis in susceptible and resistant wheat genotypes, respectively. This toxin also caused mild chlorosis in barley but not in non-host plant species. In addition to the induction of chlorosis, the toxin reported by Hunger and Brown (1993) inhibited elongation of wheat seedling coleoptiles.Six triticones (gamma-lactams) were isolated from culture broth of P. tritici-repentis (Hallock et al., 1993). A method for examining the mode of action of triticones on fresh wheat protoplasts has been described by Berglund et al. (1988).

Biocontrol agents tested include Epicoccum nigrum, two basidiomycetes, Limonomyces roseipellis and Laetisaria arvalis, as well as an agonomycete Sterile II, which were effective on straw that had been kept wet for at least 12 h (Zhang and Pfender, 1993). Pfender et al. (1993a) found Limonomyces roseipellis to reduce inoculum by 60-80%, Laetisaria arvalis was less effective and the agonomycete Sterile II was ineffective. Pfender (1988) found the chytinolytic basidiomycete, Limonomyces roseipellis, suppressed P. tritici-repentis 50-99% in infected straw with greatest effect in straw moistened daily and kept warm under low humidity but Trichoderma koningii, an aggressive competitor, did not suppress sexual reproduction of P. tritici-repentis under the test conditions.Biocontrol organisms tested on leaves and found effective to reduce infection include: Alternaria alternata, Fusarium pallidoroseum, Acinetobacter calcoaceticus, Serratia liquefaciens, and white yeasts (Li and Sutton, 1995). Cochliobolus sativus conidia in mixed inocula reduced germination of P. tritici-repentis, slowed germ tube growth and appressorium development on wheat leaves. Use of modified C. sativus or its metabolites for biocontrol is suggested (Luz and Bergstrom, 1987).Pfender and Wootke (1987) suggested nutrient competition as a control measure to reduce ascospore inoculum of P. tritici-repentis.Biocontrol agents tested on wheat seed and found most efficacious are: Bacillus subtilis and two unidentified bacterial isolates; less effective were Rhodotorula sp. Sporobolomyces roseus and Pseudomonas fluorescens (Luz and Da-Luz, 1994). In vitro inhibition of P. tritici-repentis was observed with treatment by Pseudomonas fluorescens and some of its antibiotics (Levy et al., 1992).

In Brazil, propiconazole was effective in reducing wheat leaf diseases including tan spot and gave an average increase in yield of 44% (Picinini et al., 1996). Products of Pseudomonas fluorescens Pf-5 inhibited mycelial growth of P. tritici-repentis in agar culture and suppressed ascocarp formation; purified pyrrolnitrin was similarly inhibitory (Pfender et al., 1993b). BAS 480 F in trials in Denmark, France, Germany and UK, controlled tan spot (and other leaf diseases) and increased yield (Saur et al., 1990). Propiconazole reduced levels of tan spot (and other diseases) and increased yields where infection levels were high. In lower infection levels, the beneficial effect was mainly in larger grain size (Entz et al., 1990). Glyphosate applied to straw infested with P. tritici-repentis inhibited ascocarp development under certain conditions but it was not determined if the effect is due to the active ingredient or to non-herbicidal components of the product (Sharma et al., 1989). Propiconazole applied at growth stage 41-47, which proved to be the optimum stage for application to spring wheat at Outlook Saskatchewan, Canada, gave improved yields by about 10% for Fielder and 3% for Katepwa in the presence of several foliage diseases including tan spot (Duczek and Jones-Flory, 1994).

A disease forecast method tested on tan spot of wheat correctly predicted 87% of the infection periods based on 5 processing elements (Wolf et al., 1997). Area Under Disease Progress Curve (AUDPC) studies in Kansas for two years estimated that a 90% reduction in AUDPC occurred at 3.6-5.4m from the source and, consequently, that fields where tan spot does not occur will not be greatly affected by neighbouring, diseased fields (Sone et al., 1994). Sensors that measure moisture retention in diseased straw were used to predict ascospore maturation (Fernandes et al., 1991). Adee and Pfender (1989) studied the effect of different levels of primary infection from different numbers of ascomata applied to wheat plots in the fall. Disease Progress Curves were constructed based on measurements made every 5-8 days. Infection levels depended on primary inoculum levels. Consequently, control measures that reduce primary inoculum [ascospores] can decrease epidemic development and crop damage, despite multiple infection cycles by wind disseminated secondary inoculum [conidia] (Adee and Pfender, 1989). Schuh (1990) made spatial pattern analyses using Morista's index of dispersion, and found a shift from clumped to random distribution over time, indicating the importance of residue-borne inoculum under conservation tillage systems.The effect of water potential of infected leaves on production of ascomata was as follows: maximum at -0.5MPa, significantly reduced at -1.6 MPa, very few and small at -2.4 MPa and none at -3.8MPa (Pfender et al., 1988).

In Brazil, where P. tritici-repentis was listed fourth among the major wheat diseases, fungicide treatments of wheat over a 12 year period increased mean yield to 3743 kg/ha, an increase of 1152 kg/ha, equated to an average net return of US$161/ha from use of propiconazole. The loss from all four diseases was 44% (Picinini et al., 1996). By means of mobile potted wheat plants placed among infected plants in the field and returned to controlled conditions after 24 h, it was found that the minimum wetness duration for infection in tan spot was 6-7 h (Francl, 1995). Field experiments in Bavaria established two thresholds for fungicide treatment of tan spot: the first when conidia can be found on 5% of leaves of a given leaf stage and the secon, when symptoms are observed on more than 5% of the upper leaves (Wolf and Hoffmann, 1994b). Conidium liberation from stubble was nearly 100% at windspeeds of 3.3 m/s. Speeds as low as 0.7 m/s at RH 35% gave greater than 60% spore liberation. Changing RH gave greater liberation than constant RH due, perhaps to drying and consequent flicking movements. Daytime summer conditions in western Canada will almost always ensure 100% liberation of conidia produced the night before (Platt and Morrall, 1980b). Production of tan spot conidia was maximum at 100% RH but some sporulation occurred at 83-85% RH (Platt and Morrall, 1980a). Spore trapping from April to November 1970 and 1971 over a native prairie (Agropyron dasystachyum and A. smithii) at Matador, Saskatchewan, Canada, revealed ascospores of P. tritici-repentis early in the season followed by much larger numbers of conidia later in the season. Conidia exhibited a diurnal periodicity, highest at ca 12.00 h. Simple meteorological explanations could not be found for the wide fluctuations (0-707) in the daily total catches of conidia in midsummer (Morrall and Howard, 1975). In an earlier study (Howard and Morrall, 1975), Disease progress curves were established for tan spot on native grasses at Matador. Disease was reduced following irrigation and after burning in the preceding summer. Lesion size classes were established; most lesions were always greater than 0.31 mm. Overall disease intensities were always low, despite sometimes apparently favourable environmental conditions. In Queensland, Australia, a formula based on disease severity on the top two leaves (Rees et al., 1981) seriously underestimated actual grain loss from yellow spot (estimate 13.2%, actual 29%) (Rees and Platz, 1978).Carbohydrate and nitrogen determinations were made in relation to growth stage at which infection started. Translocation to the endosperm was restricted by leaf necrosis and more protein remained in the infected leaves. The overall protein content of the grains was largely unaffected but the total protein was lower because of reduced yield (Kremer and Hoffmann, 1993). Yield losses were highest from infection at the boot and flowering stages (Shabeer and Bockus, 1988).

Tan spot was first recorded in Australia by Valder and Shaw (1952). Rees and Platz (1978) reported grain yield losses of 29% in field trials conducted in 1976 at four sites in Queensland. The authors pointed out that an equation relating yield reduction to disease severity on the top 2 leaves predicted only 13.2%. The equation obtained by linear regression, relating disease severity and yield loss, was developed by Rees et al. (1981) as: L = 0.26X, where L is the percentage grain loss and X the average level of severity (%) on the top 2 leaves. This equation was believed to be appropriate for most seasons, but may underestimate disease loss in exceptionally favourable seasons. Comparison of estimates derived from single tillers and plots showed that yield losses of 49% can be observed under conditions that favour disease development in Australia (Rees et al., 1982). In experiments conducted to compare epidemics of tan spot at different stages of crop development (Rees and Platz, 1983; Rees, 1987a), grain yield of cv. Banks was found to be reduced by 13% by early disease (up to jointing stage), 35% by late disease (starting at jointing) and 48% by disease occurring throughout the season. The increased incidence of tan spot in Australia was generally attributed to stubble retention (Rees and Platz, 1980). However, a greenhouse and field study involving 80 wheat cultivars grown in Australia revealed that modern cultivars (released after 1960) were more susceptible, as a group, than those released before 1960, suggesting that the introduction of susceptible cultivars may have contributed to the upsurge of tan spot in Australia (Rees, 1987b; Rees et al., 1988). In field trials conducted at Toowoomba (Queensland, Australia) to evaluate the effectiveness of incomplete resistance (Rees and Platz, 1989), losses in the susceptible cultivar Banks reached 65% in grain yield and 45.7% in thousand kernel weight, compared with the fungicide-treated control. In New South Wales, Australia, Weelings et al. (1985) compared five recommended cultivars for losses to tan spot in field plot trials and reported losses of 13% and 21% for leaf rust-resistant cvs Banks and Durati, respectively. Cultivar Cook suffered 36% loss from a combination of tan spot and leaf rust. In cultivar Banks, losses appeared to be associated with reduced kernel weight. Lemerle et al. (1996) surveyed 83 fields in 1993 in southern New South Wales and found that 21% of the fields were infested with P. tritici-repentis. However, the severity was generally less than 5% of leaf area. Seed contamination by P. tritici-repentis in New South Wales was high in wheat grains collected from silos of the Grain Handling Authority of NSW from 1978 to 1981 (Klein, 1987). In Victoria, Australia, systematic surveys of tan spot incidence conducted by the Crop Information Service of the Victorian Department of Agriculture and Rural Affairs in 1986 (Clark and Gagen, 1988) revealed that tan spot was favoured by wheat/wheat rotations. The incidence and severity (10%) of tan spot were very low to have caused significant losses in 1986 in Victoria. A combination of five diseases of wheat (in order of importance: take-all, septoria glume blotch, cereal cyst nematode, black point and yellow spot) produced an estimated loss of $400 million (Brennan and Murray, 1988). More recently, Loughman et al. (1998) reported yield losses of 23-50% in cultivars affected by P. tritici-repentis and S. nodorum in fungicide trials conducted in 1995 at East Chapman, Western Australia. According to the authors, fungicide treatments in Western Australia are only economically justified with minimum returns of 150 kg/ha.

Tan spot was first reported in commercial wheat fields in Western Canada in 1974 (Tekauz, 1976). P. tritici-repentis was isolated from 23 of 43 fields surveyed, primarily from Manitoba and Saskatchewan. Subsequent assessment of damage due to leaf diseases using fungicides indicated that, under Manitoba conditions, losses to P. tritici-repentis were up to 14.8% in common wheat (Tekauz, 1982) and 27% in winter wheat (Tekauz et al., 1983). In the latter study, losses were due to the combined effect of tan spot and Septoria glume blotch. In a study on the effect of agronomic practices on leaf spot diseases of wheat conducted in a zero-tillage area in Manitoba, Sisson (1996) estimated losses caused by M. graminicola and P. tritici-repentis to be around 40% for total yield and 20% reduction in kernel weight. In this study, large plot sizes were used and the fungicide triticonazole applied several times during the season to provide a disease-free control. Large scale surveys of leaf spot diseases conducted between 1989 and 1993 in southern Manitoba (Gilbert et al., 1998) consistently showed an incidence of tan spot between 50 and 80%. P. tritici-repentis was the predominant pathogen in 2 years out of the 5-year duration of the study.In Saskatchewan, a study on native grasses dominated by Agropyron dasystachyum, conducted by Morrall and Howard (1975), indicated that P. tritici-repentis was the most prevalent pathogen. Fungicide trials to control the disease indicated yield losses of 52.1% of dry weight of live grass and 26.7% loss when live and dead grass were used for yield loss measurements (Howard and Morrall, 1974). Duczek and Jones (1994) reported a 10% (soft white) and 3% (hard red spring wheat) yield increase by foliar application of fungicides in plots where the main pathogens were S. nodorum (most prevalent) followed by S. tritici, S. avenae f.sp. triticea [Leptosphaeria avenaria] and P. tritici-repentis. In studies of durum wheat fields conducted in Saskatchewan (Canada), Fernandez et al. (1994) reported incidences of red smudge of 1.7 to 2.3% in 1992 and 0.2% in 1990-1991. Although the pink discoloration caused by P. tritici-repentis in wheat is not known to be associated with poisonous compounds, the tolerance of red smudge in the Canadian marketing system is quite low (Canadian Grain Commission, 1991, in Fernandez et al., 1998). Red smudge alone or in combination with black point results in lower grades of wheat. For example, a 0.25% incidence of red smudge alone or a 10% combined incidence of red smudge and black point lowers the grade of durum wheat from No. 1 to No. 2, resulting in an average loss of CAN $12 per tonne (Fernandez et al., 1998).

The first occurrence of tan spot in North Dakota was recorded by Hosford (1971a), when the disease became epidemic throughout the state. Isolations made from infected tissue allowed Hosford (1971a) to establish for the first time the true destructive potential of this pathogen and to correctly associate the outbreak of the disease with stubble retention, on which P. tritici-repentis overwinters. Subsequently, field experiments were conducted to assess yield losses to tan spot using infested straw as inoculum and multiple fungicide applications to provide a disease-free control (Hosford, 1971b). Yield losses of four cultivars ranged from 8% (cv. Wells) to 28% (cv. Waldron) and were attributed to a combination of P. tritici-repentis and Leptosphaeria avenaria f.sp. triticea. Hosford and Bush (1974) conducted experiments in five sites across North Dakota to assess crop losses caused by a combination of P. tritici-repentis and L. avenaria f.sp. triticea. The authors reported an average loss of 12.9% in grain yield and 1.0% reduction in test weight in damp weather and no losses under dry conditions. Jons (1982) surveyed 673 fields in 1978-1980. P. tritici-repentis was found in 86% of the fields, significantly higher than leaf rust (25%), loose smut (19%) and scab (14%). A survey of leaf-spotting fungi associated with wheat in Minnesota conducted in 1980 revealed the presence of P. tritici-repentis at a low frequency (Vargo et al., 1982), suggesting that tan spot was not a major problem of wheat in Minnesota. McMullen and Nelson (1992) conducted a five-year survey to assess the presence, distribution, incidence and severity of the wheat leaf and head diseases in North Dakota. Tan spot had the highest disease index (incidence x severity) of one bacterial and six fungal pathogens encountered in each of the 4 years of the study. In Montana, Sharp et al. (1976) recorded losses of up to 19.7% in 1000-kernel weight in the evaluation of 30 cultivars in artificially inoculated small plots. In the Mississippi delta of Arkansas, Hirrell et al. (1990) reported the occurrence of tan spot for the first time. An 81 ha soft red wheat field (cv. Florida 302) with a history of reduced tillage and summer fallow since 1986 was infested by P. tritici-repentis. The authors recorded an incidence >90% and disease severity of 1-10% at the soft dough stage. Cultivar Florida 302 yielded 65% less than its typical yield. However, it is not clear from the note if all the yield loss could be attributed to tan spot alone.Watkins et al. (1978) documented a tan spot epidemic that occurred throughout Nebraska in 1977. A combination of favourable weather conditions, susceptible cultivars and crop residues from wheat monoculture were believed to have contributed to the outbreak of 1977. By 1977, tan spot had become the most prominent leaf spotting disease of wheat in Nebraska (Watkins et al., 1982). In Oklahoma, Evans et al. (1999) compared greenhouse and field testing methods to identify resistance to tan spot. They observed a yield loss of 15% in untreated field plots. Kernel weight was reduced on average by 7 and 13% at two field locations. Shuh (1990) assessed the severity and spatial pattern of P. tritici-repentis in 4 commercial fields in north central Oklahoma. Spatial pattern analysis revealed a shift from clumped to random pattern of infection, indicating the importance of residue-borne inoculum under conservation tillage. Under conventional tillage, random spatial patterns were observed indicating that airborne inoculum was the source of infection. In Kansas, Raymond and Bockus (1985) obtained yield losses of 27.4% in a study aimed at developing field and greenhouse protocols for testing cultivar resistance to tan spot. The field epidemic was initiated by ascospores generated by infected oat kernels broadcast onto the plots in the autumn. Shabeer and Bockus (1988) investigated the effects of tan spot on yield and yield components relative to wheat growth stage. Yield losses of 34.1% were obtained with disease throughout the growing season. The authors showed that substantial yield losses (17%) could result from early epidemics (up to pseudostem erect), suggesting that early chemical control of tan spot in winter wheat may prevent early season disease. Furthermore, this study indicated that losses were the result of reduced number of grains/head and reduced kernel weight.Surveys of foliar diseases in New York State were conducted in 1984-1985 by Luz and Bergstrom (1986). Ten foliar diseases were found on the two spring wheat cultivars surveyed; P. tritici-repentis was one of the three most prevalent foliar pathogens in 1984. A survey of leaf and spike diseases of winter wheat was conducted in 1986 (32 fields) and 1987 (29 fields) by Schilder and Bergstrom (1989). Leptosphaeria nodorum blotch was the most prevalent disease, followed by Septoria tritici blotch, tan spot and Septoria avenae blotch; the latter two occurred sporadically. Luz and Bergstrom (1986) evaluated triadimenol seed treatments for early season control of tan spot, powdery mildew, spot blotch and Leptosphaeria nodorum blotch in spring wheat. In the field, triadimenol provided control of powdery mildew and tan spot in cv. Sinton and of tan spot in cv. Max, resulting in yield increases of 20% and 15%, respectively, at two different locations.

Tan spot of wheat occurs in several countries of Central and South America, including Mexico, Argentina, Bolivia, Brazil, Chile, Paraguay and Uruguay (Kohli et al., 1992). The disease became economically threatening in the mid-1980s and resulted in severe epidemics in 1990 in Paraguay and in Argentina in 1991, with estimated yield losses in farmers' fields between 27 and 70% (Kohli et al., 1992). Mehta and Gaudencio (in Kohli et al., 1992) consider that yield losses in the State of Parana (Brazil) are around 36%. Data collected in the period 1991-1994 from a regional disease nursery (LACOS), involving CIMMYT and local institutions in the Southern Cone Region of South America, indicated tan spot levels of 80-100% on susceptible material. In 1993, an average infection index of 54% was recorded on approximately 300 advanced lines (Kohli and Diaz de Ackemann, 1998).In Paraguay, P. tritici-repentis was consistently detected in wheat field surveys from 1972 to 1995 (Viedma and Kohli, 1998). In 1992 and 1993, which were favourable for disease development, fungicide applications provided 36-61% yield increases in field plot experiments. However, only 6% yield increase was recorded in the dry year of 1994. In Uruguay, losses to leaf blights caused by S. tritici and P. tritici-repentis ranged from 4% in 1990 to 44% in 1977 (Diaz de Ackermann and Kohli, 1998). On-farm replicated fungicide trials conducted in Oaxaca State in Mexico showed that disease levels could be reduced by up to 80% by application of cypronazole or triticonazole (Osorio et al., 1998). Up to 75% yield increases were obtained with two sprays of tebuconazole. A mean yield increase of 53% was obtained when all the fungicide treatments were averaged. Cortazar (1979) reported that 120 out of 206 lines, obtained from CIMMYT and sown in 1979 at La Platina Research Station, Chile, showed evidence of infection by P. tritici-repentis and suffered an average 6.6% yield loss. It is not clear if the yield loss was attributable to tan spot alone or to a combination of tan spot and powdery mildew. Herrera (1981) reported that M. graminicola and P. tritici-repentis were the most common pathogens in the coastal region of Chile in 1977-1978. Goulart et al. (1995) reported that 1.5% of 2238 seed lots analyzed were infected by P. tritici-repentis. The study included 26 cultivars from 11 counties in Brazil. In a study conducted in 1994 and 1996 to estimate the effect of tan spot on the yield of six cultivars in Pergamino (Argentina), yield losses ranged from 1.7% (most resistant/tolerant cv.) to 16.6% (most susceptible cv.) (Annone, 1998). Tebuconazole (125 g ai/ha) was used to provide a disease-free control. Losses of 6-13.5% were recorded in the province of Cordoba (Argentina) in response to infection by P. tritici-repentis and Septoria tritici blotch (Galich and Galich, 1994, in Annone, 1998).

P. tritici-repentis was reported in Europe well before the 1970s, which witnessed the status of this fungus change into an economically important pathogen of wheat worldwide. A list of publications tracing the identification of this fungus in various parts of the world from 1902 to 1981 can be found in Hosford (1982). Schmitz and Grossmann (1987) reported a severe outbreak of P. tritici-repentis in Germany in two experimental fields under different crop rotation programmes and found a distinct relationship between disease severity and spray programmes only in isolated cases. Wheat under monoculture had more infection than wheat grown in rotation with other crops. Obst (1988) evaluated, in the field, 10 winter wheat varieties widely grown in Bavaria (Germany) for resistance to tan spot and identified three resistance categories in which disease development increased from 0 to 90% in 55, 48 or 43 days, respectively. In earlier trials, Obst (1988) found that yield losses were ca 23-53%. In a crop rotation experiment at Frankendorf (Germany), Odorfer et al. (1994) reported that the most important pathogens of wheat were P. tritici-repentis and Septoria tritici. Yield differences in the rotation study could not be explained by pathological causes, as no yield response was observed following fungicide application. Wolf (1991, referenced by Verreet, 1995) conducted extensive epidemiological studies in Germany. He identified P. tritici-repentis on wheat in several regions of Germany, including Bavaria, Baden-Württemberg, North-Rhine Westphalia, Lower Saxony and Rhineland-Palatinate. Field studies aimed at developing a control strategy for tan spot showed that losses in the susceptible cv. Kanzler could reach 16 dt/ha (ca. 30%), if unprotected by fungicides.In Hungary, a countrywide survey to determine the frequency and severity of B. sorokinia and D. tritici-repentis was conducted in 1989 and 1990 (Bakyoni et al., 1998). Tan spot was recorded in 70% of the total area surveyed in 1989 and 51% in 1990. The occurrence of P. tritici-repentis in England and Wales was reported in several wheat fields by Cook and Yarham (1989). In Poland, Jaczewska (1998) reported losses of 12.8% and the estimated profitability of fungicide application to be 1.5 dt/ha. This study included Septoria spp., P. tritici-repentis, Erysiphe graminis and Pseudocercosporella herpotrichoides. Wakulinsky et al. (1998) reported seed infection of 44% and 56%, respectively, from viable and non-viable seeds collected from a variety trial in Ursynow (Warsaw) in 1995, 1996 and 1997. The most serious aspect of seed infection was considered to be the seed to seedling transmission observed in 39% of cases. Zamorski et al. (1997) conducted varietal observation trials throughout Poland in 1992-96 on triticales and their progenitor species (wheat and rye) and found that P. tritici-repentis and Phaeosphaeria nodorum developed intensively at the end of the season, while Rynchosporium secalis was present early in the season.In France, losses to node canker caused by "septoriosis" reduced yields by 1.5-2 t/ha (Henaff et al., 1998). In the same report the authors stated that 'node canker' was often caused by P. tritici-repentis. It is not clear if the losses caused by P. tritici-repentis were of the same magnitude as those caused by S. tritici in France.

P. tritici-repentis was the most prevalent pathogen in varietal evaluations of triticales at ENA, Meknes (Morocco), causing an average disease severity of 47% in 1989-1990 (El Harrak et al., 1998). According to Nsarellah and Mergoum (1998), yield losses caused by tan spot range between 12 and 18% in Morocco. However, data or references to studies from which these values were obtained are not available. The pathogen has been reported in a survey of durum wheat fields in eastern Algeria (Lamari et al., 1995). The extent of economic losses due to this pathogen is not known. Similarly, P. tritici-repentis was reported in field surveys of cereal diseases conducted in 1989-1991 in Tunisia (Cherif et al., 1994) but data on economic losses to the pathogen are not available. P. tritici-repentis was recorded in Tunisian wheat samples infected in 1968-1970 (Hosford, 1972).

P. tritici-repentis has been reported in many Asian countries, including Japan, India, China, Thailand, Georgia, Afganistan, Iran and Nepal (list in chronological order in Hosford, 1982). However, little is known about the economic importance of tan spot in most of these countries, some of which have only limited acreage of wheat.Maraite et al. (1998) processed 360 leaf samples with symptoms of leaf blight collected from Bangladesh, China, India, Nepal, Vietnam, Morocco, South Africa, Mexico, Bolivia and Argentina. Bipolaris sorokinia and Drechslera tritici-repentis (P. tritici-repentis) were detected in 81% and 29% of the samples, respectively. B. sorokinia prevailed in the warmer countries, whereas P. tritici-repentis predominated in the cooler regions. In the Gangetic plains, both pathogens were associated with 'indistinguishable blight symptoms', and were sometimes detected on the same leaf. Karki (1982) estimated the yearly yield losses to tan spot in Nepal to be 5-10%, representing 30-60 million Nepalese Roupies (NR) at the market rate of NR 1.5 per kg of wheat. The occurrence of tan spot and other leaf blight diseases in South and Southeast Asia was summarized by Saari (1998), who reported a 19.6% average yield loss for the region, including India, Nepal and Bangladesh. According to Saari (1998), P. tritici-repentis is considered to be of moderate level (3 on a scale of 0 to 5) in South Asia and absent or not reported in Southeast Asia. References to country-specific reports on yield losses due to cereal leaf blights (spot blotch, tan spot and Alternaria blight) can be found in Saari (1998) and are summarized as India (15.5%), Nepal (19.5%) and Bangladesh (23.2%). These values were derived from data generated by variety and fungicide trials. Tan spot is considered to be one of the main wheat diseases in central Asia, where it has been annually found in winter wheat fields in parts of Uzbekistan, Tadjikistan and southern and northern Kazakhstan (Postnikova and Khazanov, 1998). Disease intensities of 25 to 50% were recorded. Under cereal monoculture, an incidence of 100% and disease intensity of 70-80% were recorded in Uzbekistan and Tadjikistan. In Kazakhstan, 60-80% of all fields surveyed were infested by P. tritici-repentis with within-field incidence of 100% (Postnikova and Khazanov, 1998). However, details of the specific surveys and yield loss assessment studies were not included in the publication.