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a Dep. of Plant and Soil Science, Oklahoma State University, Stillwater, OK 74078
b Dep. of Crop Sciences, University of Illinois, Urbana, IL 61801
* Corresponding author (bai{at}mail.pss.okstate.edu)
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Abbreviations: QTL, quantitative trait locus • AFLP, amplified fragment length polymorphism • SSR, simple sequence repeat • PCA, principal coordinate analysis
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Germplasm characterization is one of the major aspects of genetic resource management (Clark et al., 1997). Assessment of genetic relationships among diverse accessions allows breeders to select diverse resistance genes from different sources and to accumulate those resistance genes in one cultivar to enhance levels of head blight resistance. Meanwhile, understanding the genetic relationships between various accessions may eliminate unwanted duplications in the germplasm collection and increase the efficiency of breeding efforts to improve wheat head blight resistance, and may also lead to diversification of head blight resistance genes in breeding programs.
Wheat resistance to head blight is a quantitative trait and is controlled by several genes (Bai and Shaner, 1994). Expression of different genes results in similar phenotypes. Therefore, resistance contributed by different genes cannot be separated on the basis of disease evaluation. Molecular markers tightly linked to resistance genes provide a powerful alternative tool for tracing genes conferring head blight resistance. In addition, molecular markers offer an easily quantifiable measure to study the genetic relationships among cultivars.
Restriction fragment length polymorphisms (RFLPs) have been used to study genetic diversity in a range of species due to their reliability and reproducibility (Castagna et al., 1997; Federici et al., 1998; Lu et al., 1996; Paull et al., 1998); however, a low level of polymorphism hampers their application in wheat (Chao et al., 1989; Paull et al., 1998). Polymerase chain reaction (PCR)-based markers can overcome this disadvantage. A relatively high level of polymorphism makes SSRs and AFLPs more attractive marker systems for studying genetic diversity of plant germplasm (Bai et al., 1999b; Bertin et al., 2001).
Several AFLP and SSR markers associated with the major QTL on chromosome 3BS have been identified from cultivars Ning 7840 and Sumai 3 (Anderson et al., 2001; Bai et al., 1999a; Zhou et al., 2002). Since the major QTL explained a large portion of the genetic variation for head blight resistance, these closely linked markers are useful tools for study of genetic relationships between the QTL from Ning 7840 and QTL from other cultivars. In this study, AFLP and SSR markers were analyzed in 65 wheat cultivars and breeding lines collected from eight countries, and head blight resistance of these cultivars was evaluated under favorable head blight infection conditions in the greenhouse. Our objectives were to investigate the possible origin of the major QTL on chromosome 3BS by means of AFLP and SSR markers, and to study the genetic relationships among resistant cultivars from different countries to provide useful information for the effective use of an array of genetic resources to improve head blight resistance in wheat.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The greenhouse disease evaluation was conducted in a completely randomized block design with three replications (pots). Each replication had three inoculated plants. Visual head blight ratings were analyzed on a single plant basis. Symptomatic spikelets and the total number of spikelets on each inoculated spike were counted at 21 d after inoculation. Disease severity was calculated as the proportion of symptomatic spikelets per inoculated spike at 21 d after inoculation.
In the field test, the same set of cultivars were planted; only winter type of cultivars could be evaluated for head blight because spring wheat were killed by the cold weather in the winter. These spring wheat cultivars were mainly from China and their resistance levels were repeatedly evaluated (Bai et al., 1989; Bai and Shaner, 1996). Disease evaluation was conducted as described by Bai et al. (2001). In brief, wheat cultivars were planted in 0.9-m-long rows in the fall of 1997 and arranged in a completely randomized block design with two replications. When the wheat reached the boot stage in the spring of 1998, scabbed wheat kernels were scattered on the soil surface in the plot areas at a density of 60 kg/ha. From flower to early dough stages, plots were misted daily for two 30-min periods starting at 0900 and 1500 h, respectively. Percentage of scabbed spikelets was recorded at late dough stage by selecting 10 spikes per row.
Molecular Marker Analysis
DNA was isolated from bulked leaves of two seedlings by means of the CTAB (hexadecyltrimethylammonium bromide) procedure (Saghai-Maroof et al., 1984). A total of 16 pairs of AFLP (Table 2) and three pairs of SSR primers (Gwm 389, Gwm 533 and Gwm 261; Roder et al., 1998), synthesized by integrated DNA Technology, Inc. (Coralville, IA) were analyzed in this study. AFLP analysis was performed as described by Bai et al. (1999a). Briefly, genomic DNA (about 300 ng) was double digested with EcoRI and MseI restriction enzymes. AFLP adapters for both restriction enzymes were then ligated to restriction fragments. The ligated DNA was preamplified with a primer combination based on the sequences of the adapters without any selective nucleotide at the 3'-end. All PCR reactions were performed in a MJ PTC-100 thermocycler. Preamplification was performed for 30 cycles of 30 s at 94°C, 1 min at 65°C, and 1 min at 72°C. For selective amplification, selection of 16 AFLP primer combinations were based on a previous survey of polymorphism levels between the cultivars Ning 7840 and Clark and those markers linked to the major QTL in Ning 7840 (Bai et al., 1999a). Before selective amplification, all selective EcoRI primers were labeled with [
-33P]ATP for AFLP detection. The following touchdown thermal profile was used in all amplifications: one cycle of 30 s at 94°C, 30 s at 65°C, 1 min at 72°C; 12 cycles in which the initial annealing temperature of 65°C was lowered by 0.7°C each cycle; and 23 cycles in which the annealing temperature was held constant at 56°C. AFLP-PCR products were separated on a 5% (w/v) denatured polyacrylamide gel followed by exposure to Kodak BioMax MR film for 2 to 3 d depending on intensity of signals.
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Data Analysis
Polymorphic AFLP fragments were visually inspected from radiograms. Presence and absence of a band with the same molecular size was assumed to be two alleles at a locus and variation in band presence was recorded as a polymorphism. SSRs were visualized on a computer screen using RFLPscan software from LI-COR. The method used for SSR scoring was the same as for AFLPs. Bands clearly absent in at least one cultivar were scored (1 for present and 0 for absent) and entered in a computer file as a binary matrix. To ensure accurate scoring, all markers were scored at least twice. Loci with ambiguous bands in some lines were either recorded as missing data or excluded from the analysis. Similarities for pairwise accessions were calculated by the SIMQUAL module. The unweighted pair-group method with arithmetical average (UPGMA) was used for cluster analysis with NTSYSpc software, version 2.0 (Rohlf, 1998), and resulting clusters were presented as dendrograms. A principal coordinate analysis to construct a two-dimensional array of eigenvectors was performed by the DCENTER module of the NTSYSpc program.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Genetic Relationship among Wheat Cultivars
Sixty-five cultivars were analyzed with 324 AFLP and 19 SSR alleles. Considering the geographic distribution of the cultivars tested, two major clusters were observed when cluster analysis was performed: an Asian cluster and a European–American cluster (Fig. 1). Principal coordinate analysis with the same data supports the conclusion from the cluster analysis (Fig. 2). All 65 cultivars can be separated at various similarity levels. Among them, ‘OH 552’ and ‘OH 569’ were the closest with 99% similarity. ‘Encruzilhada’ from Brazil was the only cultivar independent from either of the two major clusters and branched at 61% similarity in cluster analysis (Fig. 1), but it was plotted next to the European–American cluster in PCA (Fig. 2 and 3).
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The Asian cluster consisted of diverse cultivars with pedigrees from several sources and can be further separated into five subclusters: Ning 7840, landrace, Funo, Sumai 3, and Fengkang 15 related sub-clusters (Fig. 1). In the principal coordinate plot, first and second coordinates effectively differentiated all the five subclusters from each others (Fig. 2). Eight cultivars clustered in the hierarchy subcluster of Ning 7840. Most of them either shared similar parents with Ning 7840 or had Ning 7840 or its sister lines in their pedigrees. The landrace subcluster included all landraces from China and Japan, and a high level of genetic similarity was observed among these landraces. Although Funo and Fengkang 15 clusters were grouped in the Asian cluster, they located between the Asian cluster and European–American clusters in PCA because of the fact that they were cultivars from the USA, Italy, or Argentina (Fig. 2 and 3). In the Funo subcluster, ‘Yangmai 1’ and ‘Wannian 2’ were selected from Funo and its close relative ‘Mentana’, respectively, while Funo and Wannian 2 were parents of ‘Fumai 3’ and ‘Xiangmai 1’, respectively (Table 1). Three closely related lines from Argentina with Fengkang 15 in the pedigree were close to the Ning 7840 subcluster because of their common ancestor ‘Bezostaja1’ in the pedigrees of their parents (Fig. 1 and 2). Therefore, pedigree information coincides with results from the cluster analysis and PCA. The Sumai 3 group was closer to the landraces, rather than to the Funo group, which was unexpected since Funo was a parent of Sumai 3. In addition, Sumai 3 was one of the parents of Ning 7840, but Ning 7840 was further from Sumai 3 than the distance from the landraces to Sumai 3. This may be due to the Russian cultivar Avrora (PI 410426), which was not related to the Chinese cultivars, in the pedigree of Ning 7840.
The American–European cluster included cultivars from several western countries and consisted of three subclusters (Fig. 1 and 3). The first subcluster included two well-known U.S. "head blight resistant" cultivars, Freedom and Ernie. Although an obvious genetic relationship cannot be established between them on the basis of their pedigrees (Table 1), the two cultivars seem on the basis of their DNA fingerprinting data to be close (Fig. 1 and 3). The second subcluster included breeding lines from Illinois and some other U.S. breeding programs and some commercial cultivars (Fig. 1 and 3). Many of these U.S. materials have some head blight resistance, high yield potential, or good adaptation to U.S. environments where wheat is grown. Susceptible controls from four Midwest states were also included in this subcluster. The third cluster consisted of cultivars from Argentina, Austria, France, and Brazil.
On the basis of cluster analysis, PCA and pedigree information, only IL 9634-24851 in the American–European cluster showed obvious association with Ning 7840 (Table 1). Chinese sources of head blight resistance were not found in the pedigrees of any other cultivars in this cluster. The result indicated that the resistance from the cultivars in American–European cluster might be controlled by QTL other than those from Chinese sources.
To compare the DNA profiles of the same cultivars from different sources, three cultivars (Ning 7840, Sumai 3, and Wangshuibai) in the Asian cluster were analyzed with all markers (324 AFLPs and 19 SSRs). Slight variation in banding patterns between the two sources was detected. In a total of 343 DNA fragments scored, percentages of variable bands were 0.8% between sources of Sumai 3, 1.5% between sources of Ning 7840, and 5.2% between sources of Wangshuibai when missing bands were excluded. Larger variation between sources of Wangshuibai than between Ning 7840 or Sumai 3 sources might be due to the fact that Wangshibai is a landrace and is most likely more heterogeneous than cultivars Sumai 3 and Ning 7840, which are products of breeding programs.
Results in this study demonstrated a good agreement among PCA and cluster analysis of the marker data, geographic distribution, and pedigree information of the cultivars studied. Cultivars from eastern and western countries formed two distinct clusters at 65% similarity (Fig. 1). The similarity among cultivars from the two regions was lower than among cultivars from within a region. The U.S. cultivars distributed in two of the three subclusters in the European–American cluster, indicating that relatively diverse head blight resistant germplasm from western countries has been used in U.S. head blight resistance breeding programs. However, in general, genetic diversity among Chinese resistant cultivars was much greater than that among U.S. cultivars (Fig. 1 and 2).
Marker Analysis of the Major QTL on 3BS
To determine the relationship between the marker alleles linked to the 3BS QTL from Ning 7840 and from other sources, six AFLP and two SSR markers linked to the major QTL were used to characterize all cultivars (Table 3). To determine the possible origin of the major QTL, the two parents of Sumai 3, Taiwan Wheat and Funo, were also included. Sumai 3, Ning 7840, and Taiwan Wheat exhibited the same banding pattern, but Funo showed alternative alleles for all the marker loci analyzed. The results suggest that Ning 7840 may carry the same major QTL as that in Sumai 3, and the QTL most likely originated from the Chinese landrace Taiwan Wheat, not from the Italian parent Funo. Identical banding patterns for the marker loci on 3BS were detected for two different sources of the same cultivars, indicating that marker alleles linked to the major QTL remained unchanged, although overall genetic variation was observed between different sources of the same cultivars. The marker alleles tightly linked to the major QTL appeared in almost all the Sumai 3 and Ning 7840 related resistant cultivars. In addition, two Japanese landraces and PC-2 also showed the same banding pattern as Ning 7840 for all the marker loci on 3BS. Sumai 49 and ‘F 5125’ had Sumai 3 in their pedigree and carried five and six marker alleles tightly linked to the Sumai 3 major QTL, respectively; thus, they were likely to carry the 3BS major QTL. Although there was no pedigree information available for Wuhan 3 and ‘FSW’, these cultivars had seven Ning 7840 marker alleles on the 3BS, suggesting that the two cultivars may also carry the 3BS QTL. The other cultivars carried less than half of marker alleles on 3BS and on the basis of their pedigree and fingerprinting data were unlikely to carry the 3BS QTL (Table 1 and Fig. 1).
Therefore, combining major QTL from Ning 7840 and other non-Sumai 3 resistant sources can facilitate pyramiding of head blight resistance QTL in wheat.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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All wheat cultivars in this study were clearly placed into two major clusters that match with their geographic classification and growth habit. The Asian cluster mainly includes spring or the facultative type of cultivars with Chinese or Japanese pedigrees; while the America–Europe cluster consists of winter type cultivars from western countries such as the USA, Argentina, Austria, France, and Brazil. Therefore, cultivars in the two clusters are from two distinct gene pools.
In the Asian cluster, closely related cultivars were clustered together to form distinct subclusters. For example, all cultivars closely related to Ning 7840 together formed a hierarchy group on the basis of their degrees of relatedness. Pedigree connections could also be established between subclusters. Funo was a parent of Sumai 3 and Sumai 3 was a parent of Ning 7840; thus, Sumai 3 connected Funo and Ning 7840 subclusters in the Asian cluster. However, Sumai 3 clustering closer to the landrace group than to Funo was unexpected. A possible explanation could be that the Chinese landrace Taiwan Wheat was another parent of Sumai 3. Taiwan Wheat was not included in the original experiment because seed was not available at that time. Our expectation is that Taiwan Wheat should be in the landrace group because it was collected from the same area as the other Chinese resistant landraces used in this study. Ning 7840 is farther from Sumai 3 than the distance between the landraces and Sumai 3 as seen in the dendrogram (Fig. 1) and PCA (Fig. 2). This may be due to the Russian cultivar Avrora (‘Neuzucht’/‘Bezostaja 4’//‘Bezostaja 1’) in the pedigree of Ning 7840. Fengkang 15 related Brazilian lines formed a separated subcluster and showed close relationship to Ning 7840 subcluster. This may result from the Romanian cultivar Lovrin 10 (‘Abondanze’/‘Triumph’//‘Bezostaja 1’) in the pedigree of Fengkang 15, and Lovrin 10 shares a common parent Bezostaja 1 with Avrora. In the PCA, the second principal coordinate clearly separated the Ning 7840 and Fengkang 15 related subclusters from other subclusters (Fig. 2), therefore the genetic makeup of Avrora and Lovrin 10 is probably distinct from that in other Asian and western cultivars used in this study.
In the European–American cluster, pedigrees of some U.S. cultivars were complicated because of multiple crosses involved and uninformative accession numbers used in some pedigrees. However, a good agreement between cluster analysis and pedigree data still can be visualized on the basis of the information available. For example, in the Freedom group, Freedom was one parent of ‘IL 95-2909’, and they clustered together. ‘OH 552’ and ‘OH 569’ were two sister-lines with an Indiana line in their pedigrees; therefore, they were close to the Indiana line P91193D1-10-2. In another U.S. subclusters, ‘PA 8769-158’, ‘Kaskaskia’, and ‘IL 93-2283’ and ‘Roane’ were clustered together because they had either ‘Caldwell’ or a Caldwell's relative (‘Coker 68-15’) in their pedigrees. Cultivars from these countries other than the USA formed a distinct subcluster. In this cluster, ‘Extrem’ was an old Austrian cultivar, and all cultivars with Extrem in their pedigrees clustered together. The French cultivar Poncheau was clustered closer to the Austrian cultivars than did two landraces and ‘38 M.A.’ from Argentina. This may be explained by the geographic distribution of these cultivars.
Among the 66 cultivars studied, two Chinese cultivars Wuhan 3 and PC-2 were introduced to the USA through CIMMYT's wheat-breeding program, and pedigree information is unknown. On the basis of their DNA profiles from this study, they were close to Sumai 3 and carried the same markers on 3BS; therefore, they were most likely relatives of Sumai 3.
Several landraces from different countries were included in this study because of their head blight resistance. Landraces are old varieties selected by farmers from natural variation that occurred in production fields; therefore, pedigree information is not documented. DNA fingerprints may be the best way to determine their genetic relatedness. In this study, all the head blight resistant landraces from China and Japan clustered in one group without including any improved cultivars; therefore, the genetic relationship among those landraces is closer than that between the landraces and improved cultivars. This may be because these landraces were grown geographically close to each other and developed under similar climatic conditions, or originated from a common ancestor. Chinese landraces were mainly collected from three east coast provinces of China—Jiangsu (Wangshuibai, ‘Caizihuang’, ‘NTDHP’), Zhejiang (‘WZHHS’), and Fujiang (‘FSW’) —and were selected and grown in similar environments under favorable conditions for wheat head blight epidemics. The results also indicated that the genetic diversity among these Asian head blight resistant landraces is very narrow and may be derived from a limited source.
Origins of Head Blight Resistance QTL
On the basis of breeding experience, it was generally believed that major resistance QTL in the cultivar Sumai 3 was derived from Funo (Wang et al., 1989) or from transgressive segregation of resistance genes from both parents (Liu and Wang, 1990). The results from this study provide molecular evidence that Taiwan Wheat was most likely the donor of the major 3BS QTL by demonstrating that Sumai 3, Ning 7840 and Taiwan Wheat exhibited the same banding pattern in the 3BS QTL region, while Funo had an alternative pattern for these marker loci. This major QTL explained a large portion of the phenotypic variation for head blight resistance (Anderson et al., 2001; Bai et al., 1999a; Zhou et al., 2002) and can be putatively detected in all resistant cultivars with a Sumai 3 pedigree through closely linked markers on 3BS in this study. Although some genetic variation was detected between different sources of the same cultivars, marker loci on 3BS remained the same. The result confirms that the QTL from Sumai 3 (Taiwan Wheat) is a major QTL for head blight resistance in Sumai 3 related cultivars; however, this major QTL did not explain all the genetic variation for head blight resistance. Thus, some other modifying QTL might also be involved in Sumai 3 resistance. Interaction between the major QTL and QTL from Funo might play a significant role in enhancing the head blight resistance level and result in transgressive segregation (Liu and Wang, 1990). Because of large environmental variation and interactions between genotypes and environments, these minor QTL usually showed small coefficients of determination (R2) individually and R2 values varied from experiment to experiment (Bai et al., unpublished data; Anderson et al., 2001). Investigation of functions of these QTL may provide more insight to further understanding of the genetic mechanisms of head blight resistance in Sumai 3.
Japanese and Chinese landraces have generally been considered as different head blight resistance sources; however, this study showed some evidence that resistance QTL in these landraces might derive from similar sources. All marker alleles linked to the major QTL in Ning 7840 appeared in Japanese landraces Shinchunaga and Shirasaya No1, suggesting that the two Japanese landraces might contain the same major QTL as that in Sumai 3. In addition, the Chinese landrace Wangshuibai and the Japanese landrace Sanshukomugi were very close in the dendrogram and carried four Ning 7840 marker alleles for the 3BS QTL, suggesting that they may not carry the same 3BS QTL as that in Ning 7840. The results also indicated that head blight resistant landraces from Japan and China might derive from similar sources. In addition to resistant cultivars from China and Japan, several other cultivars with head blight resistance were identified from the USA and other countries. These cultivars did not have Chinese pedigrees and showed different banding patterns from that of marker alleles tightly linked to the 3BS QTL in Ning 7840, and therefore, resistance in those cultivars may be controlled by QTL different from that in Ning 7840 and integration of head blight resistance genes from Asia may diversify the European-American gene pool for improvement of wheat head blight resistance.
In the last decade, Sumai 3 and Ning 7840 have been introduced to European and American countries and used extensively as head blight resistant parents in wheat breeding programs worldwide. In this study, only one Illinois line had Ning 7840 in its pedigree. This may be due to the fact that crosses with Chinese resistant cultivars as resistant parents were still in early generations when the materials were collected for this study.
Since the major QTL on 3BS explains a large portion of genetic variation for head blight resistance (Bai et al., 1999a; Zhou et al., 2002), identification of the QTL in cultivars is important when selecting parents. The results suggested that most resistant cultivars with Sumai 3, Ning 7840, or their relatives as one of parents possibly contained the major 3BS QTL. The 3BS QTL was detected in 14 cultivars with average head blight severity of 17%. Most of these cultivars shared all the 3BS marker alleles with Ning 7840. The markers covered a distance about 25 cM (Bai et al., 1999a). It appears that the QTL and a segment of the chromosome surrounding the QTL presents in these cultivars. In this study we assumed that if a cultivar has pedigrees of Sumai 3 or its relatives, and carries most of the flanking molecular markers for the 3BS QTL, the QTL for head blight resistance is also present. On the basis of molecular marker data, a large DNA fragment carrying the major 3BS QTL and associated markers have been inherited together in a number of cultivars and, therefore, marker-assisted selection with closely linked flanking markers may be efficient.
Enhancing Genetic Diversity by Integrating Different Sources of Resistance
On the basis of this study, genetic diversity among head blight resistant landraces from Japan and China was narrow. Genetic exchange between Asian and western gene pools was limited until the 1950s when Funo and its relatives (Mentana and ‘Ardito’) were introduced into China from Italy. These cultivars were very well adapted to wheat growing conditions in the Yangtze River Valley of China, and performed better than the prevalent landraces in yield and other important traits; therefore, these introductions were used on a large scale to replace landraces during the 1950s and 1960s. They were moderately susceptible to head blight infection, however (Liu and Wang, 1990). To improve the resistance level, they were used extensively as breeding materials in breeding programs during that time. As a result, many well-known cultivars, such as Yangmai 1, Nanda 2419, and Sumai 3, were either selected variants from Italian cultivars or selected progenies from the crosses with one of the Italian cultivars as a parent. In the 1970s, Sumai 3 was released and identified as a cultivar with a high level of head blight resistance, and has become a predominant parent for improving head blight resistance. During the 1980s, most Chinese head blight resistant lines with improved agronomic traits derived from Sumai 3 or its relatives. The combination of Funo and Taiwan Wheat not only significantly improved the head blight resistance level and agronomic traits of wheat resistant cultivars, but also broadened the genetic diversity of wheat head blight resistant germplasm in China. This is a successful example of integration of diverse genetic sources to broaden genetic diversity, enhance head blight resistance, and improve agronomic traits of wheat cultivars. In addition, all cultivars with Avrora in their pedigrees formed a district group in the Asian cluster in this study, indicating the introduction of the cultivar Avrora from Russia also significantly increased the genetic diversity of Chinese wheat.
A wide range of wheat cultivars and breeding lines with various degrees of resistance were evaluated for head blight resistance in this study. These resistant cultivars also had a relatively low level of DON (Bai et al., 2001). Among them, on the basis of their pedigree and marker information, 14 cultivars may have the 3BS QTL, whereas the other cultivars may not contain the QTL. Thus, some head blight resistant landraces from China, Japan, Austria, and improved cultivars from the USA and other countries have various levels of head blight resistance, and may carry other QTL than the 3BS QTL in Sumai 3. Combination of resistance QTL from different sources should enhance genetic diversity and incorporate different types of resistance in head blight resistant cultivars. Molecular mapping of the genes from different sources may facilitate further classification of these genes and improve breeding efficiency.
Cultivars with head blight resistance from Austria, Argentina, France, and Brazil appear to be closely related to each other. Cultivars from the USA are more closely related to European and Argentina cultivars. Within the USA, the diversity of resistant cultivars is limited. Ernie and Freedom seem to be closely related. The distinction between eastern and western germplasm was obvious; therefore, gene flow between the two major regions may help to broaden the genetic diversity of resistant cultivars in the USA.
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