Wheat (Triticum aestivum L.) is the most important crop after rice in China. The acreage devoted to wheat production has outnumbered 20 million acres in 2005. However, wheat production is constantly challenged by scab disease or Fusarium head blight (FHB), mainly caused by Fusarium graminearum Schw. In a period of 54 years from 1950 to 2003, nine severe epidemics and 17 medium epidemics occurred in the mid-lower reaches of the Yangtze valley. The warm and humid climate during the flowering stage of wheat growth favors the outbreak of this disease (Bai and Shaner 1994; Parry et al. 1995; Galich 1997; Dill Macky 1997; McMullen et al. 1997). Due to the global weather changes and a significant increase in the amount of inoculums resulted from increased practices of maize-wheat or rice-wheat crop rotations and minimum tillage, scab epidemics have become more and more frequent. Scab disease causes sterility, poor seed filling, low test-weight and tombstone seeds, thus resulting in great yield loss in epidemic years. Besides reduced yield, the consumption of scabbed seeds is a direct threat to the health of human beings and livestocks because the scabby grains are contaminated with toxic mycotoxins (mainly deoxynivalenol (DON) and zearalenone) (Chen et al. 2000).

It has been long recognized that deployment of scab-resistant varieties is the most economical, environmental friendly, and efficient method in controlling the disease. Progress has been made in identifying resistant germplasms and breeding resistant varieties. Since Arthur reported in 1891 the genetic variation of scab resistance in wheat, a large number of germplasms have been evaluated (Liu and Wang 1991; Snijders 1990; Saur 1991). However, resistant cultivars or landraces are few in terms of the number of accessions surveyed. Moreover, many of these resistant germplasms originated from the lower Yangtze River region of China, few of which but 'Sumai No. 3' have been successfully used in scab resistance breeding program. Their genetic diversity in resistance has yet to be characterized. Schroeder and Christensen (1963) classified wheat scab resistance into two types, type I against initial penetration, type II against fungal spread within spikes. Other types of resistance were proposed later, such as type III for toxin decomposition (Miller et al. 1985), type IV reducing kernel infection and type V for tolerance (Mesterhazy 1995). In almost all the germplasms characterized genetically, the resistance is controlled by both major and minor genes whose effects are greatly influenced by environments (Snijders 1990; Ban and Suenaga 2000). Because of the complexity in inheritance and resistance mechanisms, our understanding of the resistance is still very limited and the progress in scab resistance breeding has been slow and far from meeting our needs.

Wheat geneticists and breeders have well taken advantage of molecular markers and genetic maps in studying the scab resistance. Quantitative trait loci (QTL) for scab resistance, mostly type II, have been reported in Sumai No. 3 and its derivatives as well as a few other resistant varieties (Bai et al. 1999; Waldron et al. 1999; Anderson et al. 2001; Buerstmayr et al. 2002,2003; del Blanco et al. 2003; Gervais et al. 2003; Shen et al. 2003a). Most of these studies concluded that the major genes controlling scab resistance were on chromosomes 5A, 3B and 6B of the wheat genome.

   Among the Chinese germplasms for scab resistance, 'Wangshuibai' is a landrace originated from Jiangsu. To elucidate its genetic basis for scab resistance, we conducted QTL mapping for type I and type II resistance using a recombinant inbred line (RIL) population created by single seed descent from 'Nanda2419' x Wangshuibai and a 3,410 cM molecular marker map. The major QTLs for type I resistance in Wangshuibai were mapped to the interval of Xgwm149∼Xcfd22-2 on 4B and the interval of Xmag1281∼Xmag1036-2 on 5AS, and those for type II resistance were mapped to the interval of XSTS49-1∼Xbarc102-1 on 3BS and the interval of Xgwm644∼Xwmc341 on 6BS. Within each type, the QTLs functioned additively. Epistasis analysis showed that co- adapted gene complex and complementary epistasis QTLs also conferred the scab resistance. For type I resistance, significant QTL x E interactions were detected.

Population and resistance evaluation

The mapping population used was created by single seed descent from Nanda2419 x Wangshuibai. Nanda2419, a spike selection of the Italian variety 'Mentana', is susceptible to scab (Fig. 1). One hundred fifty four of the F6: 7 recombinant inbred lines (RIL) were examined for scab resistance.

To evaluate type I resistance, field experiments in a randomized complete block design were conducted in Nanjung in a natural scab disease nursery with two replicates in 2003 and four in 2004. In the 2004 trial, artificial spray at the flowering stage of the mixed conidial suspension of four local virulent strains of F. graminearum was employed to supplement the conidia. Twenty days after anthesis the percentage of infected spikes (PIS) of each line was investigated to represent type I resistance. The trials in different years were regarded as environments.

Type II resistance was evaluated in 2002 in a field at Nanjing Agricultural University with two replicates in a randomized complete block design and in 2003 with one replicate. Approximately 15 to 20 spikes per line were inoculated at anthesis by single floret inoculation with the mixed conidial suspension of about 1,000 conidiospores. A misting system was used to maintain the moisture for disease development. Fifteen to twenty days after the inoculation, data were collected for the number of diseased spikelets (NDS) and the length of diseased rachis (LDR). Since NDS and LDR were highly correlated with each other and gave similar results in QTL mapping (Lin et al. 2004), the later was mainly discussed for its better consistency across the environments.

For both types of resistance, the variation among the RIL was significant (P< 0.0001 for PIS and P=0.0009 for LDR), and there were transgressive segregants for both traits. The broad sense heritability estimated for PIS varied from 63.1% to 81.5% and was 31.4% for LDR. The line means of PIS displayed a near-normal distribution with a slight skew toward the resistance parent. The LDR data showed a double peak like distribution in both years.

Linkage map

To map scab resistance QTLs, 513 polymorphic marker loci were detected with RAPD, EST-STS and EST-SSR markers developed in our laboratory, and SSR markers including the gwm series (Roder et al. 1998), barc series (published by P. Cregan's lab) and wine series (Gao et al. 2003). The marker map was constructed using Mapmaker Macintosh V2.0 (Lander et al. 1987) and included 42 linkage groups, spanning 3,410 cM of the total genome size (Table 1), involving all chromosomes but 6A. The average marker interval of the molecular map was 5.9 cM. The mapped total genetic distance for the A, B and D genomes was 1,172 cM, 1,377 cM and 861 cM, respectively. Among the seven homoeologous groups, group 6 was covered least, with only 160 cM mapped. No linkage map was constructed for chromosome 6A and the linkage map for chromosome 6D had only 38.6 cM. The linkage group - chromosome associations were established according to published marker maps and Chinese Spring nulli-tetrasomic line analysis.

QTL detection and epistasis detection

Simple interval mapping (SIM) and simplified composite interval mapping (sCIM) were carried out to map QTLs and QTL x E (environment) interactions for scab resistance using the multiple-environment model of MQTL version 1.0 (Tinker and Mather 1995a, 1995b) that was programmed to use data from multiple environments. A framework with 350 markers extracted from the linkage map constructed was scanned using 1-cM walking speed. sCIM was performed using 30 randomly chosen background markers. In the multiple environment model, the presence of QTLs was inferred based on SIM, and the QTL positions were refined according to the sCIM test statistics (Tinker and Mather 1995b). When two linked peaks were over 30 cM away from each other, they were considered as two different QTLs. Detection of QTL x E interactions was based on SIM multiple-environment model. Statistical significance thresholds to declare the presences of QTLs and QTL x E interactions were determined by 1,000 random permutations with 5% genome-wide type I error. The proportion of variance explained by the main effect of a single QTL to the total variance was estimated using the equation R² =1-1/exp (TS/n) (Tinker 1996), where n is the total number of lines excluding those with missing data, the TS is the peak value of a distribution generated by SIM. For single environment QTL detection, the test statistic used as the threshold to declare the presence of a QTL was 9.1, which is equivalent to LOD=2.O in MAPMAKER/QTL (Tinker 1996).

Two-locus epistatic interactions were surveyed using the epistasis model of MQTL. We first held one of the marker locus (the anchor locus 'A') constant, and then scan the genome for a second locus 'B' that interacted with the 'A' locus using a walking speed of 1 cM. When the test statistic for interaction model (A+B+A*B) vs. additive model (A+B) was equal to or larger than 9.1, the specific locus pair were considered as the putative epistasis QTLs (eQTL). To better establish the intervals of the two locus interactions, a second round of genome scan was then performed using 1 cM walking speed after holding the 'B' locus of a pair of putative eQTLs constant. The final significant threshold was set with 10% genome-wide type I error. Linked eQTLs were defined as independent when the interval peaks were separated by more than 30 cM. The variance explained by the epistasis interaction (R²) was calculated using the formula described as above.

QTLs for type 1 resistance

Main QTLs : Table 2 listed the single environment QTLs identified for PIS. Four putative QTLs in Wangshuibai for type I resistance were detected using the 2003 and 2004 data. Two of them were constantly identified in the similar chromosomal regions of chromosomes 4B and 5AS in both years. Using the multiple-environment model, Qfhs.nau-4B was mapped to the interval of Xgwm149∼Xcfd22-2 (Fig. 2a). The peak was right at Xgwm149. Qfhs.nau -5A was mapped to the interval of Xmag1281∼Xmag1O36-2, 2.8 cM from Xmag1O36-2 (Fig. 2b). The 2D QTL₂₀₀₃ and the 3A QTL₂₀₀₄ appeared only once (Table 2), but the former was also revealed when the threshold was set with 10 % genome wide error. In. addition, QTL x E was identified at 10 cM from Xgwm437 in the interval of Xgwm437-Xwmc488 on chromosome 7D.

Epistasis interactions : Interactions of 137 locus pairs were significant with a test statistic equal to or larger than 9.1 in the first round scan for digenic interactions. These loci involved 49 genetically independent chromosomal regions. After the second round of genome scanning by holding the 'B' locus of each of these locus pairs constant, two pairs of interactions were found to be significant with 10% genome-wide type I error (Table 3). The Xcfd42∼Xwmc390-2 pair was significant with 5% genome-wide type I error. The phenotypic variation explained by them varied from 14.0% to 15.8%.

QTLs for type II resistance

Main QTLs : SIM analysis showed that two chromosomal regions in Wangshuibai have contributed significantly to the lower score of LDR (Table 4). One QTL on chromosome 6BS was detected using both years' data with the almost same peak position. On chromosome 3BS, two linked peaks, which were significant higher than the threshold and separated by 27.4 cM, were revealed using the 2002 data. The 2003 data resulted in the similar test statistic distribution (data not shown), but only one peak was above the threshold and fell in the interval of Xmag1166∼XSTS49-1 that was tightly linked to one of the peaks detected using the 2002 data. These results were similar to the previous reports by Lin et al. (2004), who examined type II scab resistance using the NDS and LDR data based on a 2,210 cM SSR map of the Wangshuibai x Nanda2419 RIL population.

In the multiple-environment model, Qfhs.nau-6B was mapped to the interval of Xgwm644∼Xwmc341 (Fig. 3b), 1 cM from Xgwm644. The test statistic curve from 3B scanning displayed double peaks beyond the threshold (Fig. 3a). However, because the two peaks were only about 15 cM from each other, we could not tell if they represent two linked QTLs without colloboration. The higher peak was 2 cM from XSTS49-1 in the region of XSTS49-1∼Xbarc1O2-1 (Fig. 3a). A test statistic peak appeared in the region corresponding to Qfhs.nau-3B1 in Lin et al. (2004), but it did not reach the threshold set with 5% genome-wide type I error. Further experiment is needed to confirm this QTL. Qfhs.nau-3B2 identified by Lin et al. (2004) was much closer to the peak flanked by Xgwm389∼Xgwm533-3 than to the one flanked by XSTS49-1∼Xbarc102-1. The latter is therefore tentatively designated as Qfhs.nau-3B3. Qfhs.nau-3B2 appeared to have larger effect than Qfhs.nau-3B3 in SIM, but the sCIM favored Qfhs.nau-3B3 (Fig . 3a). In addition, a test statistic peak in the region of Xwmc154∼Xgwm429 on chromosome 2B almost reached the threshold (data not shown). No significant QTL x E interaction was found.

Epistasis interactions : Epistasis of 104 locus pairs involving 44 different chromosomal regions gave test statistics equal to or larger than 9.1 in the preliminary round of scanning for two-locus interactions. Three locus pairs produced test statistics beyond the threshold with 10% genome-wide type I error in the second round of scanning (Table 5). The phenotypic variation explained by them varied from 14.1% to 15.3%. As shown in the table, the six eQTLs distributed in different chromosomes, three of which were mapped to the D genome. No major QTL for scab resistance has been detected in the D genome so far. Eleven more interactions were likely associated with these eQTL according to the first round scan.

Polymorphism in chromosomal regions associated with the main QTLs

Survey of the main QTL-associated regions in Wangshuibai, Nanda2419, Sumai No. 3, 'Funo' and 'Taiwan Xiaomai' (the two crossing parents of Sumai No. 3) with markers close to the QTL peaks showed that the bands in Wangshuibai that were associated with these QTLs were polymorphic to Sumai No. 3 except the one detected by wmcO96 (Fig. 4). These results implied that haplotype diversity exists in most of the QTL-associated regions between Wangshuibai and Sumai No. 3.

Discussion and perspectives

Main QTLs for scab resistance : Using a marker map with nearly full coverage of the genome and a composite interval mapping approach, we concluded that in Wangshuibai chromosomal regions in 4B and 5AS have major effects on type I scab resistance and those in 3BS and 6BS have major effects on type II scab resistance. These main QTLs seemed to act additively and independently. Based on our results, Wangshuibai has stronger ability to resist fungal penetration than spreading.

Major QTLs for type I resistance have been reported in chromosomes 3A of 'Frontana' (Steiner et al. 2004) and 5AS in the doubled haploid population derived from 'CM-82036' x 'Remus' (Buerstmayr et al. 2003). The 5AS QTLs in both populations were mapped to similar chromosome regions. CM-82036 is a Sumai No. 3 derivative In an RIL population developed from Sumai No. 3 x Funo, we did not find the association of Xmag1281∼ Xmag1O36-2 interval with type I resistance (F. Lin et al. unpublished data).

Type II resistance QTLs have been indicated on all wheat chromosomes but 1A, 4Dand the 7th homoeologous group employing different lines (Waidron et al. 1999; Ittu et al. 2000; Anderson et al. 2001; Buerstmayr et al. 2002; Gervais et al. 2003; Shen et al. 2003a; Paillard et al. 2004; Steiner et al. 2004). On some chromosomes, two or more regions have been related to scab resistance. However, for most of the lines examined so far, only one or two major QTLs for type II resistance were detected. Major QTLs in the similar regions on the 3BS and 6BS were most commonly identified in different, related or un-related, lines.

QTLs on 1B, 2A and 3A were also often detected in various germplasms with less effects and consistency across the environments. Loci correspondence of these QTLs between different lines needs to be verified. Some minor QTLs in Wangshuibai reported by Lin et al . (2004) did not reach the significance threshold in sCIM analysis even though the test statistic peaks were observed in these chromosomal regions.

The 3BS map corresponded well to its counterparts in Sumai No. 3 (Anderson et al . 2001) and CM-82036 (Buerstmayr et al . 2002). Since the QTL-scan test statistic corresponding to 3BS displayed a two-peak distribution, we double-checked the marker data to ensure a correct marker map. Actually, the marker order presented in Fig. 3a was 5-LOD better than the next one. The LOD distribution from 3B scanning for type II resistance QTL in 'N7840' x 'Clark' population was quite similar to ours (Guo et al . 2003). Qfhs.nau-3B3, associated with XSTS49-1∼Xbarc102-1, seemed more likely to be in the position of the 3BS QTL found in Sumai No. 3 (Anderson et al . 2001) or its derivatives such as CM-82036 (Buerstnmayr et al . 2002) and 'Ning894037' (Shen et al . 2003b). Qfhs.nau 6B in Wangshuibai also showed coincidence in position with the corresponding QTL in Sumai No. 3 and Ning894037 (Waldron et al . 1999; Shen et al . 2003b).

In spite that both Wangshuibai and Sumai No. 3 were germplasms originated or developed in Jiangsu of China, no relationship in pedigrees between them is known. Based on the polymorphic patterns (Fig. 4), Taiwan Xiaomai is the donor of the 3BS and 6BS QTLs in Sumai No. 3. Our results and others (Bai et al . 2003; McCartney et al . 2004) have demonstrated the haplotype diversity in the 3B and 6B QTLs-associated regions, but comparative fine-mapping and even QTL cloning is required to tell if these QTLs in the same or similar positions are allelic to each other. Likely, they have common progenitors. The relevant genome structures have undergone changes during evolution, but the functions for scab resistance were kept because of the selection pressure in the scab epidemic areas, for instance, the lower Yangtze River of China. The conservation of QTL positions among the different sources of scab resistance germplasms implies a narrow genetic basis for scab resistance in common wheat.

Epistasis on scab resistance: Epistasis contributed significantly to the scab resistance in the Wangshuibai x Nanda2419 population. All the eQTLs detected were significant at P<0.0001. In one kind of the digenic interactions, the parental genotypes had better resistance, for instance, the eQTLs for type I resistance and the 1D-3A and 4A-7D pair for type II resistance (Tables 3 and 5). The breakage of the parental combinations or repulse phases of the loci involved conferred susceptibility. Evolutionarily, this phenomenon is called co-adaptation and the loci involved are considered as co-adaptation gene complex. In another kind of the digenic interactions, the recombinant combinations favored the resistance, for example the 7B-2D pair for type II resistance. No individual effects were detected for all of the relevant loci. A similar phenomenon has been reported in the population derived from a wide cross of common beans for a few quantitative traits (Johnson and Gepts 2002). In populations derived from inter-subspecies crosses of rice, Li et al . (1997) found that the effects of recombinant genotypes were mostly negative in conditioning the grain yield components. Obviously, epistasis plays substantial roles in the formation of complex traits. Validation of the eQTLs for scab resistance is essential to understand the genetic basis and use them in breeding programs. Existence of the co-adapted gene complexes in determining scab resistance suggests multiple pathways in the expression of resistance. In addition, our results indicate that co-adaptation phenomenon exists not only at the inter-species or inter-subspecies level, but also within cultivars. Higher order of epistatic interactions could also exist and should be examined using larger populations.

Breeding for scab resistance: Scab resistance is a trait that is heavily affected by humidity and temperature at the flowering stage. Special facilities for disease development are often required for resistance screening. Marker assisted selection is the option of choice in improving the evaluation accuracy, saving labor and resources, and speeding up the breeding progress. Wangshuibai is an indigenous germplasm with poor agronomical traits. The SSR markers tightly linked to its resistance QTLs will facilitate their transfer to elite cultivars. Special attention should be paid to the use of type I resistance of Wangshuibai, which functions as the first barrier in combating the disease.

Based on various QTL mapping studies, it is known that scab resistance in wheat is controlled by QTLs with independent effects, eQTLs including co-adapted gene complexes and complementary QTLs, and QTL x E. Both resistant and susceptible lines could contribute to the resistance. The lack of diversity in major QTLs for scab resistance requires more extensive screening for resistance resources using molecular markers. That loci conferring resistance exist in susceptible lines appears to be a common phenomenon (Gervais et al. 2003; Lin et al. 2004; Paillard et al. 2004; Steiner et al. 2004). Selection of transgressive segregants thus is possible and should allow accumulation of resistance genes, which has become more feasible with the help of molecular markers.

Breeding and mapping schemes for maximizing the chances of QTL discovery have to be designed to take advantage of the various genetic components for scab resistance, especially for the epistasis loci. S. D. Tanksley proposed the advanced backcross QTL (AB QTL) mapping strategy for the simultanecuous discovery and transfer of valuable QTLs from un-adapted germplasm into elite breeding lines (Tanksley and Nelson 1996). This method should be applicable to scab resistance improvement. Use of prudential resistance evaluation and the availability of large amounts of SSR markers will facilitate its success.

In summary, we have already had a good start in understanding the genetic basis of scab resistance: However, greater challenge is still in the face of us. Enhancing the diversity of scab resistance gene resources, breeding cultivars with higher level of resistance, and elucidating the resistance pathways of the hosts are the priority. Genomics tools such as rice genome sequence information, Triticeae ESTs, differential display of expressed genes using microarray or other strategies, mutant analysis and virtually unlimited molecular markers have provided us with unprecedented opportunities to achieve our goals.

Acknowledgements

This project was partially supported by '973' program (G1998010200), NFSC program (30270807, 30430440), NSFC-outstanding youth fund and '863' program (2002AA224 161, 2003AA207100). We thank all the staffs and graduate students in our laboratories who have contributed to this work. Special thanks to Professor Dajun Liu for his constant support of the research work conducted in the first author's laboratory.

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