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Published online 8 September 2006
Published in Crop Sci 46:2047-2053 (2006)
© 2006 Crop Science Society of America
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PLANT GENETIC RESOURCES

Identification of New Sources of Resistance to Tan Spot, Stagonospora Nodorum Blotch, and Septoria Tritici Blotch of Wheat

P. K. Singha, M. Mergouma,*, S. Alib, T. B. Adhikarib, E. M. Eliasa and G. R. Hughesc

a Dep. of Plant Sciences, North Dakota State Univ., Fargo, ND 58105, USA
b Dep. of Plant Pathology, North Dakota State Univ., Fargo, ND 58105, USA
c Dep. of Plant Sciences, Univ. of Saskatchewan, Saskatoon, SK, S7N 5A8 Canada

* Corresponding author (mohamed.mergoum{at}ndsu.edu)


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Leaf spot of wheat (Triticum aestivum L.) in North America consists of a group of diseases involving tan spot [Pyrenophora tritici-repentis (Died.) Drechs.], Stagonospora nodorum blotch [Phaeosphaeria nodorum (E.Müller) Hedjarroude], and Septoria tritici blotch [Mycosphaerella graminicola (Fückl) J. Schröt. in Cohn]. A complex of these diseases occurs in nature hence managing leaf spots is difficult. Use of resistant cultivars is the most effective and economical means of controlling leaf spot; however, none of the widely grown wheat cultivars in North America show high levels of resistance to these diseases. Hence, this study aimed to identify new sources of resistance to leaf spotting diseases. To achieve this objective, 975 accessions of wheat and its relatives were evaluated for P. tritici-repentis, race 1, resistance under controlled environments. Of these 975 accessions, 40 selected accessions were further screened against six virulent races (1, 2, 3, 5, 10, and 11) of P.tritici-repentis and to foliar pathogens P. nodorum and M. graminicola. New sources of resistance effective against the three leaf spotting disease were identified in accessions of T.monococcum L., T. turgidum L., T. dicoccum Schrank ex Schübler, T. dicoccoides (Körn. ex Asch and Graebner) Schweinf., T. timopheevii (Zhuk.) Zhuk., T. spelta L., and T. aestivum L. including synthetic wheat. Resistance was observed in all three ploidy levels of the wheat genome and presently efforts are being made to transfer the leaf spot resistance into adapted wheat and durum cultivars.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
INTENSIFIED wheat production, changes in cultural practices including shifts from conventional tillage and stubble burning to reduced tillage practices, shorter crop rotations, and growing of cultivars resistant to the rusts but susceptible to leaf spots has resulted in development of leaf spots of wheat to epidemic proportions worldwide (De Wolf et al., 1998). Leaf spot of wheat in North America consists of a group of diseases involving tan spot caused by Pyrenophora tritici-repentis [anamorph: Drechslera tritici-repentis (Died.) Shoem.], Stagonospora nodorum blotch caused by Phaeosphaeria nodorum [anamorph: Stagonospora nodorum (Berk.) Castellani & Germano], and Septoria tritici blotch caused by Mycosphaerella graminicola (anamorph: Septoria tritici Rob. ex Desm.) (Fernandez et al., 1999; Gilbert and Woods, 2001). Leaf spots on average cause yield losses of 10 to 15%; however, under conditions favorable for disease development, it can be higher than 50% (King et al., 1983; Riede et al., 1996). Leaf spots also cause significant loss in grain quality by grain shriveling, red smudge, and black point (Fernandez et al., 1998; McKendry et al., 1995).

A complex of these diseases occurs in nature, hence managing leaf spots is difficult. A number of management practices are useful in controlling leaf spots. These include the use of nonhost crops in the crop rotations and destruction and avoidance of infested straw, stubble, and volunteer plants by either burning or burying (De Wolf et al., 1998). However, stubble burning and tillage increases the risk of soil erosion and can contribute to pollution of the environment. The application of fungicides is also effective in controlling leaf spot, but when grain prices are low, their use is not cost effective. Therefore, the use of resistant cultivars is the most effective and economical means of controlling leaf spots (De Wolf et al., 1998). To our knowledge, most of the widely grown wheat cultivars in North America are susceptible to leaf spotting diseases.

Presently, isolates of the P. tritici-repentis are classified into 11 races on the basis of their ability to induce tan necrosis and/or extensive chlorosis symptoms on a set of differential wheat cultivars (Ali and Francl, 2002; Ali et al., 2002; Lamari et al., 2003; Manning et al., 2002). Races 1 to 5 and 9 of P. tritici-repentis are reported to occur in North America (Ali and Francl, 2003; Manning et al., 2002); races 6, 7, and 8 have been identified in North Africa and the Middle East region (Lamari et al., 2003); and races 10 and 11 are found in South America (Ali and Francl, 2002; Ali et al., 2002). There have been conflicting reports regarding the existence of specific virulence in the wheat–M. graminicola pathosystem. Some researchers believe that no true differences in virulence of isolates exist (van Ginkel and Rajaram, 1993) while others (Kema et al., 1996; McCartney et al., 2002) reported that isolate-specific resistance of wheat to Septoria tritici blotch follows a gene-for-gene relationship. However, the total number of races of M. graminicola is unknown. Similarly, no physiological races of P. nodorum have been convincingly reported, but variation in aggressiveness in the fungal population has been observed (Krupinsky, 1997; Scharen et al., 1985). Some level of gene-for-gene interaction has been demonstrated in studies with selected host genotypes inoculated under controlled environments with selected isolates (Arseniuk and Czembor, 1999). Arseniuk and Czembor (1999) further concluded that a single aggressive isolate might be more reliable than a mixture of isolates in screening for Stagonospora nodorum blotch resistance.

Both qualitative and quantitative resistance has been reported for tan spot (Friesen and Faris, 2004; Gamba et al., 1998), Stagonospora nodorum blotch (Feng et al., 2004; Wicki et al., 1999), and Septoria tritici blotch (McCartney et al., 2002; Zhang et al., 2001). Although resistance genes effective against each race or pathogen causing leaf spotting diseases have been identified (Feng et al., 2004; Gamba and Lamari, 1998; McCartney et al., 2002), the total number of genes currently available for resistance breeding is small. For example, only one gene for resistance (tsn1) to necrosis caused by P. tritici-repentis races 1 and 2, the most prevalent races in North America, is available in both durum and common wheat (Anderson et al., 1999; Singh and Hughes, 2005). The narrow genetic basis of resistance necessitates the need to identify novel resistance genes. This research aims to identify novel sources of resistance effective against multiple races of P. tritici-repentis and the foliar pathogens P. nodorum and M. graminicola.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 REFERENCES
 
Wheat Germplasm and Seedling Production
A total of 441 accessions from a diverse range of wheat genotypes were tested in the greenhouse at the seedling stage for resistance to different races or pathogens causing tan spot, Stagonospora nodorum blotch, and Septoria tritici blotch of wheat. Seed of the 441 "wheat relatives" accessions belonging to seven tetraploid species; T. turgidum, T. dicoccoides, T. dicoccum, T. polonicum L., T. turancium, T. carthlicum Nevski in Kom., and T. timopheevii, diploid wheat species, T. monococcum, and one hexaploid species T. spelta, used in this study was obtained from the USDA worldwide wheat collection and other breeding programs (Table 1). The classification of wheat species was done following Dorofeev et al. (1979). In addition, 534 "common and durum wheat" accessions consisting of synthetic hexaploid and tetraploid wheat, introductions, durum, and common wheat genotypes that were collected from a variety of sources were also included in this study (Table 1).


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  		Table 1. Distribution of wheat relative species, durum, and common wheat collection for resistance to tan spot caused by Pyrenophora tritici-repentis, race 1.

 
To optimize uniform emergence, seeds of the wheat accessions and appropriate checks to be screened were pregerminated and seeds at a similar stage of germination were planted in 10 by 10 cm pots containing soil-less mix (Redi-Earth, W.R. Grace and Co. of Canada Ltd., Ajax, ON). Nine seedlings were maintained in each pot until used for disease screening. The seedlings were watered and fertilized as needed to maintain healthy growth.

Disease Screening Procedures
Tan Spot
In the first screening test, all 975 accessions were tested with P. tritici-repentis, race 1, isolate Ptr 200 (Singh and Hughes, 2005). Subsequently, a subset of 40 selected accessions were tested in replicated tests with isolates Ptr 200 (race 1), D-1998-WT VII-2 (race 2), D-2000-ST VI-2 (race 3), Ptr DW-13 (race 5), Ptr BR1 (race 10), and Ptr ARD1 (race 11). Before screening, each P. tritici-repentis isolate was characterized for its race designation following the procedures reported by Lamari and Bernier (1989b).

The inoculum was produced using a modification of the method of Lamari and Bernier (1989a). The inoculum of P. tritici-repentis races 1, 2, 3, 5, 10, and 11 were obtained by placing 0.5-cm-diameter dried mycelial plugs of each race, previously stored at –20°C, on 10-cm petri plates containing V8-potato dextrose agar (PDA) (150 mL V8-juice, 10 g PDA, 10 g agar, 3 g CaCO3, and 850 mL distilled water). These cultures were incubated in the dark at 20 to 22°C for 6 d. The plates were then flooded with sterile distilled water and the mycelium was flattened with the base of a sterile test tube. Excess water was decanted from the dishes and the plates were incubated under continuous light at 22 to 24°C for 2 d followed by 1 d in the dark in an incubator at 16°C to induce conidiophore and conidia production, respectively. The plates were flooded with sterile distilled water and the conidia were dislodged with a camel-hair brush. Spore concentration was measured with a haemocytometer and adjusted to 3.0 x 103 conidia mL–1 before inoculation.

Using a hand sprayer, plants at the two-leaf stage were sprayed until runoff with the conidial suspension of the appropriate race. Following inoculation, the seedlings were incubated for 24 h maintaining continuous leaf wetness in a mist chamber located in a growth room at 22/17°C (day/night) with a 16-h photoperiod and then returned to benches in the same growth room. Appropriate checks were included in each test to verify the validity of the inoculation and the race used. Eight days after inoculation, the seedlings were rated for disease reaction based on the 1 to 5 lesion-type rating scale developed by Lamari and Bernier (1989a), with 1 being highly resistant; 2, resistant; 3, moderately susceptible; 4, susceptible; and 5, highly susceptible.

Stagonospora Nodorum Blotch
Phaeosphaeria nodorum isolate Kelvington-SK (Feng et al., 2004) was used to induce Stagonospora nodorum blotch. Inoculum was produced using a modified method of Ma and Hughes (1995). Cultures were grown at room temperature on V8-agar medium (150 mL V8-juice, 15 g agar, 1.5 g CaCO3, and 850 mL distilled water) in 10-cm petri dishes under continuous illumination provided by 25-W cool-white fluorescent tubes. Fresh cultures of P. nodorum were prepared by rubbing a 0.5-cm-diameter plug of stock cultures with upside down surface of fresh V8-agar medium. After 7 d, pink pycnidia were obvious on the surface of fresh V8-agar media and a spore suspension was prepared by flooding each Petri dish with sterile distilled water and gently brushing the medium surface with a camel-hair brush to liberate the spores. The resulting suspension was filtered through two layers of cheesecloth. The spore concentration was adjusted to 3.75 x 106 spores mL–1 before inoculation.

Three-leaf stage seedlings of the 40 selected wheat accessions were inoculated with P. nodorum by spraying the spore suspension until runoff using a hand sprayer. The inoculated seedlings were placed in a mist chamber for 48 h to enhance the infection process. Subsequently, they were moved to a growth chamber bench, under similar light and temperature regime as reported for tan spot, until the seedlings were scored for disease reaction. Seven days after inoculation, plants were rated for Stagonospora nodorum blotch using a 1 to 5 disease scale developed by Feng et al. (2004) wherein 1 is highly resistant; 2, resistant; 3, moderately susceptible; 4, susceptible; and 5, highly susceptible.

Septoria Tritici Blotch
Inoculum was produced using a modified method of McCartney et al. (2002). Fresh V8-potato dextrose agar (150 mL V8-juice, 10 g PDA, 10 g agar, 3 g CaCO3, and 850 mL distilled water) plates were streaked with pycnidiospore suspension of M. graminicola isolate Ma04–9-4. The plates were placed under continuous light at room temperature for 7 d to produce pycnidiospores. Approximately, 30 mL of sterile distilled water was added to each plate and pycnidiospores were collected using a flamed looped wire. The spore suspension was adjusted to 1.0 x 107 spores mL–1 using a haemocytometer.

Seedlings of the 40 accessions were inoculated with a spore suspension at the three-leaf stage using a CO2–pressurized hand sprayer until runoff. After inoculation, the plants were kept in the mist chamber under continuous leaf wetness for 48 h. Subsequently, the plants were moved to a growth chamber bench with the same light and temperature regime as for tan spot screening. Fourteen days after inoculation, plants were rated for Septoria tritici blotch using a modification in the 0 to 5 lesion-type disease scale developed by McCartney et al. (2002) wherein 0 is immune; 1, highly resistant; 2, resistant; 3, moderately susceptible; 4, susceptible; and 5, highly susceptible.

Statistical Analysis
A randomized block design with three replicates, each with nine plants, was used for each of the race or pathogen disease tests. The statistical analysis included an analysis of variance for each race or pathogen causing leaf spot using the Statistical Analysis System version 8.2 (SAS Institute, 1999). The existence of significant differences (P < 0.05) in disease reaction among genotypes was detected with PROC GLM using LSD option.


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
REFERENCES
 
A total of 975 accessions, including 441 accessions belonging to the wheat relative species and 534 durum and common wheat accessions, were evaluated for seedling reaction to P. tritici-repentis, race 1, the most prevalent race in North America. This race has the combination of the virulence of race 2 and race 3 (Lamari and Bernier, 1989b; Lamari et al., 1998); hence, it was chosen for the initial screening. Disease reactions of the 975 accession to P. tritici-repentis, race 1, are available on request from the corresponding author. Based on the results of the initial screening, a set of 40 accessions was selected for evaluation to P. tritici-repentis races 1, 2, 3, 5, 10, and 11. These 40 accessions were also tested for resistance to leaf spotting pathogens, P. nodorum and M. graminicola.

Wheat Relative Species
Among the 441 wheat relative accessions tested, 39 (9%) were highly resistant (rating 1) to tan spot (Table 1). Most of the accessions were resistant to both necrosis and chlorosis component of tan spot, and these belonged to either T. timopheevii or T. monococcum. A few resistant accessions were also identified in four other species, T. dicoccoides, T. dicoccum, T. turgidum, and T. spelta. Overall, approximately 30% of the accessions were resistant (rating 1 or 2). Among the wild relatives tested, T. monococcum and T. timopheevii had the highest number of highly resistant accessions, whereas no accessions were found highly resistant (rating 1) to tan spot in other species such as T. polonicum, T. carthlicum, and T. turanicum Jakubz.. This indicates that not all wheat relatives are likely to be useful sources of resistance. Since T. monococcum and T. timopheevii lack the B genome (Zhang and Jin, 1998), the resistance observed could be attributed to the absence of the susceptibility gene mapped on chromosome 5BL (Anderson et al., 1999).

Results from this study also indicate that the majority of accessions possessing the B genome were susceptible to tan spot. However, further allelic studies should be conducted to verify the genetics of susceptibility observed in the relatives of wheat. The occurrence of few accessions of T. monococcum and T. timopheevii with moderately susceptible reactions could be attributed to factors other than the 5BL susceptibility gene (Friesen et al., 2003) and/or the chlorosis induced by race 1 isolates. Similar to previous reports (Lamari and Bernier, 1989a; Zhang and Jin, 1998), this study reveals that resistance to tan spot is present in the primary and secondary gene pool of wheat. The resistance observed in some accessions of T. turgidum (AABB) and T. spelta (AABBDD) could be directly exploited in transferring resistance to tan spot into durum and common wheat, respectively. Based on the resistant reaction to P. tritici-repentis, race 1, nine accessions from six species were selected and examined in detail among the 40 genotypes evaluated to multiple races or pathogens causing leaf spots (Table 2).


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  		Table 2. Pedigree, genome, and disease reaction of 40 genotypes to P. nodorum and M. gramminicola isolates.

 
Durum and Common Wheat Collection
A total of 546 durum and common wheat accessions including hexaploid and tetraploid synthetics were evaluated for tan spot resistance of which 60 (11%) were highly resistant (rating 1) (Table 1). Common wheat and synthetic tetraploid wheat accounted for only few highly resistant genotypes (n = 13). A high proportion of the resistant accessions in this collection was due to the synthetic hexaploid wheat accessions (n= 47). Since the wild relative Aegilops tauschii Coss. is a common parent in all the hexaploid synthetic wheats, this suggests that this species, believed the contributor of the D genome in common wheat, may also be a valuable source of resistance to tan spot. Similar suggestions have been made by other researchers (Xu et al., 2004; Zhang and Jin, 1998). No durum genotype was observed to be highly resistant (rating 1) although 10 accessions were rated as resistant (rating 2). Overall, approximately 28% of accessions of the "durum and wheat collection" were resistant or highly resistant (rating 1 or 2) (Table 1). A total of 31 accessions from this collection including resistant genotypes, appropriate cultivars, and checks to our studies were selected and included in an elaborate study with multiple races or pathogens of P. tritici-repentis, P. nodorum, and M. graminicola.

Elaborated Study of Selected Genotypes
A detailed study with individual races and pathogens causing leaf spotting diseases was undertaken using 40 accessions selected based on their reaction to P. tritici-repentis, race 1, pedigree information, genome composition, genetic diversity, agronomic characteristic, and/or to be used as disease checks. The pedigree, genome composition, and reaction to leaf spotting pathogens P.nodorum and M. graminicola are given in Table 2. High level of resistance was observed for Stagonospora nodorum blotch and Septoria tritici blotch in each of the three ploidy levels of wheat. Most genotypes showing high level of resistance to P. tritici-repentis, race 1, exhibited resistance to Septoria tritici blotch and Stagonospora nodorum blotch, although a few genotypes gave different disease reaction. There were 20 accessions (Table 2, S.N. no. 1–6, 8–11, and 31–40) that were resistant to both Stagonospora nodorum blotch and Septoria tritici blotch while five accessions (Table 2, S.N. no. 7, 17, 22, 26, and 28) were resistant to one and susceptible to the other foliar disease. These findings indicate that different genes may control resistance to Septoria tritici blotch and Stagonospora nodorum blotch.

The newly identified genotypes had high level of resistance to P. tritici-repentis races 1, 2, 3, 5, 10, and 11 (Table 3). There were 17 accessions (Table 3, S.N. no. 4–11 and 32–33) that were consistently resistant to all races of P. tritici-repentis tested. Three accessions (Syn. Hex. Elite no. 1, Syn. Hex. Elite no. 9, and Syn. Hex. Elite no. 25) showed moderate chlorosis when challenged with P.tritici-repentis, race 5, although they show high level resistance to all other P. tritici-repentis races and leaf spotting pathogens P. nodorum and M. graminicola. Only the U.S. spring wheat cultivar Erik possessed resistance to tan necrosis induced by races 1, 2, 10, and 11, however a higher proportion of commercial cultivars including Erik, Crocus, Alsen, and Glenlea exhibit resistance to the extensive chlorosis symptom induced by races 1, 3, 5, and 10 (Table 3).


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  		Table 3. Disease reaction of 40 genotypes screened against Pyrenophora tritici-repentis races 1, 2, 3, 5, 10, and 11.

 
This study identified new resistant sources that are effective against the three leaf spotting pathogens, P. tritici-repentis, M. graminicola, and P. nodorum. None of the cultivars or breeding lines (Table 2, 3, S.N. no. 12 to 30) tested in this study showed resistance to all races and pathogens, although resistance to one or more races or pathogens was observed. These cultivars and lines can be beneficial in wheat breeding programs as a combination of these cultivars and breeding lines may result in development of adapted resistant cultivars. For tan spot, more than 90% of susceptible genotypes showed necrotic symptom. Similar results were observed by Lamari and Bernier (1989a). Hence, additional efforts should be made to breed for resistance to the necrosis component of tan spot. Similar to the findings of Lamari and Bernier (1989a), the majority of genotypes showed resistance to extensive chlorosis. Equal proportion of accessions had susceptibility to chlorosis induced by races 3 or 5. Hence, wheat breeding programs when screening for tan spot resistance should include all the virulent races of P. tritici-repentis.

Cultivated durum genotypes showed poor resistance to leaf spot; however, the potential to transfer resistance from related species such at T. timopheevii, T. turgidum, T. dicoccum, and T. dicoccoides exits. Similar findings were observed in previous studies (Lamari and Bernier, 1989a; Zhang and Jin, 1998). Most cultivated common wheat genotypes show susceptibility to leaf spot. However, among hexaploid wheat tested, a high level of resistance in CIMMYT synthetic wheat lines, some introductions, and breeding lines was observed. The synthetic wheat lines besides showing resistance to leaf spots are also good sources for stripe rust (Puccinia striiformis Westend.), Karnal bunt (Tilletia indica Mitra), and Fusarium head blight (Fusarium graminearum Schwabe) resistance (Mujeeb-Kazi and Delgado, 2001). Unfortunately, these synthetic wheats have several undesirable traits including poor quality, late maturity, nonthreshing, abnormal height, and lodging. Therefore, several backcrosses are required to develop germplasm with acceptable agronomic performance and disease resistance (Riede et al., 1996).

In conclusion, this study showed that resistance to multiple leaf spotting pathogens in wheat is present in a wide range of genetically diverse genotypes, including certain wild relatives of wheat. The newly identified resistance sources with multiple disease resistance may directly, or after backcrossing, be used in breeding resistant wheat germplasm and/or cultivars. These resistance sources can also serve as excellent parental germplasm for developing mapping populations for multiple diseases. These resistant accessions may possess different resistance genes and could be utilized in broadening the genetic basis of resistance to leaf spots to prevent any potential disease epidemics. The presence of novel genes in the newly identified resistance sources cannot be resolved with any certainty until the proper allelism tests are conducted. Studies are underway to determine the inheritance, allelic relationship, and chromosomal location of the different resistance genes to the different diseases of the leaf spotting complex. This information will facilitate the efficient transfer of diverse and broad-based resistance to leaf spots into adapted cultivars.


   ACKNOWLEDGMENTS
 
Financial support from Saskatchewan Agriculture Development Fund, Saskatchewan, Canada and State Board of Agricultural Research and Education, North Dakota, USA is gratefully acknowledged. The authors wish to express their appreciation to Jie Feng, Seema Singh, and Ryan Babonich for their assistance throughout this study.

Received for publication March 15, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 




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