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a USDA-ARS, Northern Crop Science Lab., Fargo, ND 58105
b Dep. of Entomology, North Dakota State Univ., Fargo, ND 58105. Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture
* Corresponding author (timothy.friesen{at}ars.usda.gov).
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ABSTRACT |
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 TOPNOTES ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Abbreviations: BG, BR34 x Grandin • HRSW, hard red spring wheat • HST, host-selective toxin • QTL, quantitative trait loci • SHW, synthetic hexaploid wheat • SNB, Stagonospora nodorum blotch
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INTRODUCTION |
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TOPNOTESABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Synthetic hexaploid wheat (SHW) lines, derived from the hybrids between tetraploid wheat (T. turgidum L.) and A. tauschii, has been used for the direct introgression of desirable genes for various traits from A. tauschii to bread wheat. These traits include resistance to leaf rust (caused by Puccinia triticina Eriks.), Septoria tritici blotch (caused by Septoria tritici Rob. ex Desm.), Karnal bunt (caused by Tilletia indica Mitra), wheat curl mite (Eriophyes tulipae Keifer), Hessian fly (Ratcliffe et al., 2000), and greenbug [Schizaphis graminium (Rondani)] (Cox, 1998; Lazar et al., 1996; Porter et al., 1989). The SHW lines derived from the crosses of durum and A. tauschii lines have proven to be beneficial in breeding programs due to their broadening of the base of resistance sources to many diseases and due to the ease of introgression of new traits from SHW lines into acceptable wheat varieties.
In the 1980s, USDA-ARS geneticist L.R. Joppa developed a number of spontaneous SHW lines from partially fertile hybrids between ‘Langdon’ durum and different A. tauschii accessions. A SHW line developed from the cross Langdon x A. tauschii PI268210 with resistance to biotype E greenbug was named ‘Largo’ (CI 17895) and released as greenbug-resistant germplasm (Joppa and Williams, 1982). The greenbug resistance gene (Gb3) in Largo has been introduced into commercially grown hard red winter wheat in Texas (Lazar et al., 1996; Porter et al., 1989). Recently, Oliver et al. (2005) evaluated 25 Langdon–A. tauschii SHW lines for resistance to Fusarium head blight and identified two resistant lines. However, the majority of Langdon–A. tauschii SHW lines have not been evaluated for reactions to other diseases and pests.
Puccinia graminis Pers.:Pers. f. sp. tritici Eriks. and E. Henn., the causal agent of stem rust of wheat, occurs wherever wheat is grown and has the potential to be one of its most devastating diseases. Although stem rust on wheat has recently been controlled in North America by genetic resistance, several historical outbreaks of this disease have been reported including the current epidemic reported in Africa (Pretorius et al., 2000; Wanyera et al., 2006). For symptom development of stem rust, uredinial pustules of P. graminis f. sp. tritici generally occur on stems, leaf sheaths, and spikes as well as leaves (Weise, 1987). Yield losses of 50% can be common if a susceptible variety is planted. This host–pathogen system follows a model gene-for-gene interaction (Flor, 1956) where avirulence genes are present in the pathogen and major resistance genes, most often inherited in a qualitative manner, are present in the host. More than 40 resistance genes have been designated for stem rust, with only 20 of these genes originating from hexaploid bread wheat (Leonard and Szabo, 2005), indicating that alternate sources of resistance have been critical to controlling this disease. It is also universally recognized that for each stem rust resistance gene there is a corresponding avirulence gene in the pathogen that the host recognizes, which leads to the onset of the resistance response in the host. The pathogen population is in constant flux and has the ability to overcome resistance by virulence shifts on a population scale. Because of this potential for virulence shifts, it is important that novel resistance genes or other forms of resistance be identified and characterized for this disease.
Tan spot, caused by Pyrenophora tritici-repentis (Died.) Drechs. [anamorph: Drechslera tritici-repentis (Died.) Shoem.] is a major foliar disease of wheat in North America and other major wheat-growing areas throughout the world. Typical symptoms include a tan-colored, diamond-shaped necrotic lesion with a small, dark brown infection site. Lesions are often surrounded by chlorotic halos (Weise, 1987). Both qualitative and quantitative resistance have been reported for tan spot (DeWolf et al., 1998). Tan spot has also been identified as a toxin system containing multiple host-selective toxins (HSTs) corresponding to single dominant host toxin sensitivity genes (Lamari et al., 2003). A race identification system has been used for P. tritici-repentis based on the production of three HSTs Ptr ToxA, Ptr ToxB, and Ptr ToxC. Both Ptr ToxA and Ptr ToxB have been purified and identified as proteins (Strelkov et al., 1999; Tomás et al., 1990) whereas less work has been done on Ptr ToxC. Single dominant host sensitivity genes corresponding to each toxin have been identified. Ptr ToxA sensitivity, identified as Tsn1, was located on wheat chromosome 5B (Faris et al., 1996) and Ptr ToxA sensitivity has been shown to be highly significant in disease development (Friesen et al., 2003; Lamari and Bernier, 1991). Ptr ToxB and Ptr ToxC are both chlorosis-producing toxins. Genes conferring sensitivity to Ptr ToxB and Ptr ToxC have been localized to chromosome 2B (Friesen and Faris, 2004) and 1A (Effertz et al., 2002), respectively, and both toxin sensitivities have been shown to be highly significant in disease development (Effertz et al., 2001; Friesen and Faris, 2004). Several nontoxin sensitivity loci have also been shown to be significantly associated with disease showing that resistance other than toxin insensitivity is also important in the wheat tan spot system.
Stagonospora nodorum blotch is caused by the fungus Phaeosphaeria nodorum (E. Mull.) Hedjar [anamorph: Stagonospora nodorum (Berk.) E. Castell. and E.G. Germano]. It is a major foliar and glume disease of wheat and has the potential to cause yield losses of up to 50% (King et al., 1983; Wicki et al., 1999). Utilization of host resistance is the most effective and preferred method to control disease. The inheritance of resistance to SNB has also been reported as qualitative, but more often as quantitative in nature (Xu et al., 2004a). Typical SNB foliar disease symptoms include lens-shaped necrotic and chlorotic lesions on susceptible genotypes very similar to that of tan spot, while only small restricted lesions develop on resistant genotypes. Recently the SNB system has also been shown to be a HST system similar to the tan spot system with multiple HSTs produced by the pathogen that interact directly or indirectly with products of single dominant host sensitivity genes that have been shown to be highly important in disease development (Friesen et al., 2006, 2007; Liu et al., 2006, 2004a, 2004b). It also has been shown that a functional ToxA gene highly similar to that of P. tritici-repentis is present in P. nodorum and the ToxA protein is highly important in the P. nodorum–wheat interaction (Friesen et al., 2006; Liu et al., 2006). The ToxA gene was also implicated in a recent horizontal gene transfer event from P. nodorum to P. tritici-repentis (Friesen et al., 2006). SnToxA, SnTox1, and SnTox2 have all been shown to have a significant involvement in disease development caused by P. nodorum isolates producing each toxin (Friesen et al., 2006, 2007; Liu et al., 2004b). Several other toxins have also been implicated in disease caused by P. nodorum (Friesen et al., unpublished data).
Hessian fly is an important pest of wheat in many regions where wheat is grown (Berzonsky et al., 2003). The pest could cause severe yield losses in susceptible wheat cultivars (Smiley et al., 2004). Hessian fly can be effectively controlled by utilization of resistance genes (Berzonsky et al., 2003). Thus far, 32 resistance genes (H1 through H32) have been identified in wheat and related species (McIntosh et al., 2006). Some resistance genes such as H13 have been successfully deployed in commercial wheat cultivars in the United States (Ratcliffe et al., 2000). Since virulent Hessian fly genotypes continuously emerge to overcome resistance sources (Berzonsky et al., 2003), novel sources of resistance are needed.
The objective of this study was to assess seedling resistance to stem rust, tan spot, Stagonospora nodorum leaf blotch, and Hessian fly in SHW lines as well as the evaluation of the A. tauschii and durum lines used in their development.
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MATERIALS AND METHODS |
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TOPNOTESABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Tan Spot
For tan spot evaluations, plants were grown and inoculated as described in Friesen and Faris (2004) using the P. tritici-repentis race 1 isolate Pti 2 (Friesen et al., 2003). Briefly, plants were placed in racks of 98 conetainers (Stuewe and Sons, Inc., Corvallis, OR) consisting of 20 lines, and a border of ‘Grandin’ wheat was used to eliminate any edge effect. Cultures were grown and conidia were harvested as described by Lamari and Bernier (1989). Spore inoculum was diluted to 3000 spores mL–1, and two drops of Tween 20 (polyoxyethylene sorbitan monolaurate) were added per 100 mL of inoculum. Plants were sprayed until runoff, and were then placed into a humidity chamber with 100% relative humidity at 21°C for 24 h in a 12-h photoperiod. After the humidity period, plants were held at 21°C in a 12-h photoperiod for the remainder of the experiment. Plants were evaluated 7 d post-inoculation using the 1 to 5 scale developed by Lamari and Bernier (1989). Lines with equal percentage of two reaction types were given an intermediate score (e.g., equal percent of reaction type 2 and 3 equals 2.5). Three replicates of nine plants per replicate were completed for each line.
Stagonospora nodorum Blotch
Seedling evaluations for SNB were done at the two- to three-leaf stage using the toxin-producing P. nodorum isolate Sn2000 (Friesen et al., 2006, Liu et al., 2004a, 2004b; Xu et al., 2004b). Isolate Sn2000 was grown and inoculated as described by Xu et al. (2004b) and inoculation and post-inoculation treatment was done as described for P. tritici-repentis except that disease reactions were evaluated 10 d post-inoculation using the 1 to 5 reaction type scale developed by Xu et al. (2004b). As with tan spot, lines with equal percentages of two reaction types were given an intermediate score. Three replicates of nine plants per replicate were completed for each line.
ToxA
A bioassay was used to characterize the response of wheat lines to Ptr ToxA based on the development of necrosis. Ptr ToxA was produced as described by Zhang et al. (1997). Approximately 25 µL of ToxA at a concentration of 10 ng µL–1 was infiltrated into a fully expanded secondary leaf using a 1-mL syringe with the needle removed. The boundaries of the infiltration site were marked before water-soaking disappeared. After infiltration, all plants were moved to a growth chamber at 21°C with a 12-h photoperiod. Leaves were evaluated 3 d after infiltration and scored as sensitive or insensitive based on the development or absence of necrosis. Two replicates were completed for each experiment.
Hessian Fly
Hessian fly resistance evaluation was performed using the procedure described by Wang et al. (2006) and Xu et al. (2006). Briefly, five plants of each genotype were individually grown in the super-cell cones placed in RL98 trays (Stuewe and Sons, Inc.) in a greenhouse. At the two-leaf stage, the plants were infested with 15 to 20 eggs oviposited on each plant from mated female adult Hessian flies (Great Plains biotype). Three days after eggs were deposited, infested plants were placed in a high humidity chamber (25°C, 60% relative humidity) for 24 h to ensure good survival rates during the migration of larvae from leaf blade to the base of the plant. The plants were then moved to the greenhouse at 25°C in a 16-h photoperiod. The plant and insect reactions were evaluated 15 d after infestation. Plants with normal growth having dead larvae at the crown were scored as resistant. Plants with stunted leaf growth having large larvae at the crown were scored as susceptible (Xu et al., 2006). Genotypes exhibiting resistant reactions were evaluated a second time using the same procedure.
Statistical Analysis
Statistical analysis was performed using the Statistical Analysis System version 9.1 (SAS Institute, 2004). ANOVA were conducted on average reactions of the SHW lines, durum Langdon, A. tauschii accessions, and checks to P. tritici-repentis and P. nodorum, respectively. The least significant difference (LSD) was used to test the difference of average reactions to P. tritici-repentis and P. nodorum between each of the SHW lines and its parental materials (i.e., durum Langdon and A. tauschii accession).
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RESULTS |
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TOPNOTESABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Langdon durum is moderately susceptible to P. tritici-repentis (tan spot) with an average reaction type 3.2 and therefore increased resistance in any SHW line most likely is a result of genes derived from the A. tauschii parental lines or is a result of an interaction of genes conferred by the A. tauschii lines with genes in Langdon. Twenty-one SHW lines showed significantly (P = 0.05) lower average disease reactions than those found in Langdon with all 21 lines having disease reaction types ranging from 1.2 to 2.2 with 1 being resistant and 2 being moderately resistant (Table 1). In contrast, three SHW lines (SW10, SW19, and SW21) had significantly (P = 0.05) higher average disease reactions (4.2) than those in Langdon. Of the 46 SHW lines developed, 28 of the corresponding A. tauschii parental lines were available for testing and a comparison could be made between the A. tauschii parent and the corresponding SHW line (Table 2). Of these 28 sets of lines, two SHW lines (SW2 and SW21) developed from crosses with resistant (reaction type <2) A. tauschii lines (e.g., CIae 5 and RL5263) did not result in significantly (P = 0.05) lower reaction types in the SHW lines compared to Langdon (Table 2). As expected, Langdon and all SHW lines were sensitive to ToxA.
Langdon and the susceptible check ND495 are highly susceptible to P. nodorum (Table 1). Of the 46 SHW lines, 30 showed significantly (P = 0.05) lower reaction types than that of Langdon (Table 1). However, 14 of the 28 A. tauschii lines (Table 2) showed a significantly (P = 0.05) lower disease reaction type than that found in the corresponding SHW lines. Only six of the SHW lines tested showed average disease reaction types of 2 or less with several others showing moderate levels of resistance in the 2 to 3 range.
Hessian fly resistance evaluation revealed that four SHW lines (SW8, SW23, SW34, and SW39) were resistant to the GP biotype of Hessian fly while Langdon and 38 other SHW lines were susceptible (Table 1). The remaining four lines including SW3, SW4, SW7, and SW12 showed segregation of resistant and susceptible plants (Table 1). Of 28 evaluated A. tauschii lines, 22 showed the same reactions as their respective SHW lines, that is, two (CIae 25 and RL5271) were resistant and 20 were susceptible (Table 2). The other six A. tauschii including CIae 9, CIae 11, CIae 19, CIae 22, RL5286, and PI268210 had the same normal plant growth as the resistant accessions. However no larvae, dead or alive, were observed at the crown (Table 2).
Five of the SHW lines tested (SW3, SW21, SW52, SW53, and SW57-1) showed good levels of resistance to both SNB and tan spot as well as resistance to all races tested for stem rust. Synthetic hexaploid wheat line SW23 was also a very good line showing resistance to both tan spot (average reaction type = 1.5), SNB (average reaction type = 2.17), stem rust as well as Hessian fly. It is also interesting to note that the A. tauschii accession (RL5271) used to generate this SHW line was highly resistant to all Pgt races tested for stem rust.
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DISCUSSION |
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TOPNOTESABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Langdon durum is a good source of stem rust resistance to multiple Pgt races. It is difficult therefore to evaluate whether the resistance from each A. tauschii accession is functional after the transfer into the corresponding SHW line. It is probable that novel sources of resistance on the D genome are present in these SHW lines. These genes could be useful for broadening the base of stem rust resistance used by bread wheat breeders for resistance gene pyramiding. It should also be noted that the resistance reaction to various races in the A. tauschii lines provides good parent materials for the development of mapping populations for the identification and genetic characterization of these sources of resistance to stem rust found on the D genome. Several of these lines have been crossed with highly susceptible hexaploid wheat lines and the populations are presently being characterized for disease resistance traits.
Several similarities exist between P. tritici-repentis and P. nodorum. Both are necrotrophic fungi that attack the leaves of plants. Both are known producers of HSTs, and both pathogens produce proteinaceous HSTs, which are rare among known HSTs (Wolpert et al., 2002). All known HSTs produced by these two pathogens are known to interact with single dominant host genes conferring susceptibility (Friesen et al., 2007; Gamba et al., 1998; Liu et al., 2006, 2004a). Of the known HSTs produced by these two pathogens, ToxA is the most well characterized and interestingly is produced by both pathogens (SnToxA and Ptr ToxA) due to a recent horizontal gene transfer event from P. nodorum to P. tritici-repentis (Friesen et al., 2006). HSTs produced by each of these fungi have been shown to be highly important in disease giving these pathogens a greater ability to colonize additional host tissue leading to sporulation and additional secondary disease cycles.
The durum cultivar Langdon is known to possess Tsn1 (Faris et al., 2000), the host gene conferring sensitivity to ToxA, found on chromosome 5B (Faris et al., 1996). Conversely, the A. tauschii (DD) lines would not contain Tsn1 since they do not possess the B genome found in durum (AABB) and hexaploid wheat (AABBDD). Previous work has shown that race nonspecific genes may be effective against the tan spot and SNB fungi even in the presence of Tsn1 (ToxA sensitivity). Faris and Friesen (2005) showed that quantitative trait loci (QTL) associated with tan spot resistance were effective against races 1 (ToxA+, ToxB–, ToxC+), 2 (ToxA+, ToxB–, ToxC–), 3 (ToxA–, ToxB–, ToxC+), and 5 (ToxA–, ToxB+, ToxC–) in the BR34 x Grandin (BG) hexaploid wheat population indicating a non–toxin-associated resistance. Interestingly, the host gene for ToxA sensitivity (Tsn1) is known to segregate in the BG population, but Tsn1 was not significantly associated with tan spot disease development using races producing Ptr ToxA. This same population was also used to evaluate resistance to P. nodorum and it was shown that Tsn1 (ToxA insensitivity) was highly correlated with susceptibility to P. nodorum isolate Sn2000, the same isolate used in the present study, with the Tsn1 locus accounting for 62% of the phenotypic variation (Liu et al., 2006). Although no significance for tan spot resistance was identified for Tsn1, as previously stated, Faris and Friesen (2005) identified non–race-specific QTL on chromosomes 1B and 5A for resistance to tan spot, and Liu et al. (2006) and Friesen et al. (2007) identified QTL at similar locations on 1B and on 1B and 5A, respectively, for SNB. This would indicate that additional non–toxin-associated resistance can be effective against these two toxin-producing necrotrophic fungi. This non–toxin-associated resistance would explain the resistance acquired from the addition of the D genome by the A. tauschii parent in the SHW lines. This would make sense given the fact that all toxin sensitivity in both systems has been shown to be dominant (Friesen et al., 2007; Gamba et al., 1998; Liu et al., 2006, 2004a), likely due to a primary gene product being produced by the host which interacts with the HST being produced by each pathogen. If this is the case, addition of the D genome in the SHW lines (and hence addition of new genes for toxin sensitivity) could increase susceptibility rather than resistance. However, for SNB we did not observe this and therefore conclude that the increase in resistance is not due to passive resistance (toxin insensitivity). Rather, it is likely caused by the presence of a plant architectural resistance mechanism that circumvents toxin sensitivity, possibly due to the reduction in penetration or proliferation immediately after penetration, yielding the toxin less effective.
Langdon, which harbors the ToxA sensitivity gene (Tsn1) is a poor source of resistance to tan spot (average disease reaction score of 3.2) and SNB (average disease reaction score of 5.0). Therefore, a significant increase in resistance over that of the durum parental line Langdon indicates there is a resistance mechanism conferred by the A. tauschii parent. Twenty-one SHW lines had significantly increased levels of resistance to tan spot relative to Langdon and three SHW lines had a significantly higher disease reaction than that of Langdon, indicating the potential for the presence of additional toxin sensitivity loci present on the D genome resulting in increased susceptibility in the corresponding SHW line. In two SHW lines developed from crosses with resistant A. tauschii accessions there was no significant increase in levels of resistance over the Langdon parent. This may be due to the recessive nature of resistance (i.e., dominant toxin sensitivity) in the tan spot system.
For SNB, Langdon is extremely susceptible, consequently, the addition of the A. tauschii genome had a striking impact on the increase of resistance levels in the SHW lines. Only 16 of the 46 SHW lines tested showed no significant increase in resistance compared to Langdon. Therefore, A. tauschii appears to be a good source of resistance to SNB. Because the HST ToxA has been shown to be produced in both the tan spot and SNB system (Friesen et al., 2006; Tomás and Bockus, 1987), it is possible that even higher levels of resistance could be attained to both diseases if ToxA sensitivity (Tsn1) could be eliminated from these SHW lines. It is also interesting to note that although ToxA sensitivity is present in all SHW lines tested; high levels of resistance are still present in some lines, indicating that this resistance may circumvent the susceptibility incurred by ToxA sensitivity.
In this study, we identified four SHW lines (SW8, SW23, SW34, and SW39) resistant to Hessian fly. Based on this study, three lines SW8 (PI 639730), SW34 (PI 639731), and SW39 (PI 639732) have been recently released as germplasm resistant to Hessian fly (Xu et al., 2006). Since Langdon is susceptible, the resistance in the four SHW lines should be contributed by the resistance genes from A. tauschii, which has been considered a good resistance source for Hessian fly. Currently, six (i.e., H13, H22, H23, H24, H26, and H32) out of the 32 resistance genes have been identified from A. tauschii (Cox and Hatchett, 1994; Gill et al., 1986, 1991a, 1991b; Martin et al., 1982; Raupp et al., 1993; Sardesai et al., 2005). Wang et al. (2006) conducted allelism tests for resistance genes in SW8 and SW34 with the known genes derived from A. tauschii and suggested that SW8 and SW34 might carry H26 and H13 loci, respectively. The allelism tests for resistance genes in SW23 and SW39 are currently in progress.
Due to the multiple sources of resistance identified, this study has opened up several possible areas of future research. These include the genetic characterization of resistance found in both the SHW lines as well as the corresponding A. tauschii lines and the introgression of resistance into acceptable germplasm. These areas of research will increase our knowledge about this material and therefore increase their usefulness for the future introgression of these beneficial traits.
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ACKNOWLEDGMENTS |
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NOTES |
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TOPNOTESABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Received for publication August 20, 2007.
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TOPNOTESABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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