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Published online 24 January 2006
Published in Crop Sci 46:234-242 (2006)
© 2006 Crop Science Society of America
677 S. Segoe Rd., Madison, WI 53711 USA
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CROP BREEDING, GENETICS & CYTOLOGY

Intersubgenomic Heterosis in Rapeseed Production with a Partial New-Typed Brassica napus Containing Subgenome Ar from B. rapa and Cc from Brassica carinata

Maoteng Li, Xin Chen and Jinling Meng*

National Key Lab. of Crop Improvement, Huazhong Agricultural Univ., Wuhan 430070, China

* Corresponding author (jmeng{at}mail.hzau.edu.cn)


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
A breeding strategy for utilizing intersubgenomic heterosis in rapeseed (Brassica spp.) was proposed by partially replacing the An and Cn subgenomes of B. napus L. (AnAnCnCn) with the Ar subgenome of B. rapa L. (ArAr) and Cc of B. carinata A. Braun (BcBcCcCc), respectively. To replace the subgenomes of natural B. napus (AnAnCnCn), pentaploid hybrids were first produced by mating the synthetic hexaploid (ArArBcBcCcCc) with natural B. napus. Progenies of pentaploid hybrids were considered as the partial new-typed B. napus (ArArCcCc) since they contained 38 chromosomes and half of their genome was introgressed from Ar/Cc subgenome based on cytological and molecular assay. Most individuals of the partial new-typed B. napus showed normal meiotic behavior, high portion of germinated-pollen and good seed set. Intersubgenomic hybrids were produced by crossing cultivars of natural B. napus with the partial new-typed B. napus plants selected from F3, F4, and F5 generations. Seed yield potential of intersubgenomic hybrids was tested for three successive years and most hybrids showed strong over-control or midparent heterosis. Seed yield of hybrids was positively correlated with the genomic proportion of Ar, Cc and Ar + Cc in the new-typed B. napus. It is suggested that increasing the subgenomic portion of Ar/Cc in the new-typed B. napus might further strengthen the intersubgenomic heterosis for seed yield.

Abbreviations: AFLP, amplified fragment length polymorphism • HPH, high parent heterosis • PCR, polymerase chain reaction • PMCs, pollen mother cells • SSR, single sequence repeat


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
HETEROSIS produced by interspecific or distant cross has been reported in many organisms (Allard, 1960; Harvey and Dario, 1994; Li and Wu, 1996; Brewbaker and Sun, 1999; John et al., 2003) and thus distant crosses are frequently used in plant breeding. For example, hybrids yielded more than their parent lines with a mean relative superiority of 54% in grain sorghum (Sorghum bicolor L.) (Haussmann et al., 2000). Grain yield and its components both showed strong heterosis in hybrids between common wheat (Triticum aestivum L.) and spelt (Triticum spelta L.) (Schmid and Winzeler, 1990; Winzeler et al., 1994). In rice (Oryza sativa L.), intersubspecific hybrids between indica and japonica types show great yield potential because of significant genetic differentiation (Yuan, 1987). Li et al. (1998) revealed that heterosis for grain yield in rice is highest when the frequency of japonica alleles in the male parent is between 50 and 60% in two testcross populations. Sun et al. (2002) proposed that the favorable heterozygous interactions of genes are the reason for the production of heterosis in rice.

In rapeseed, strong biomass heterosis in interspecific hybrids between B. napus (AACC, 2n = 38) and B. rapa (AA, 2n = 20) is frequently observed (Sun, 1943; Zhao and Becker, 1998; Qian et al., 2003). Liu et al. (2002) observed in hybrids between B. napus and B. rapa that the average midparent heterosis for biomass production was around 30% with the highest value of 175.4%. Hybrids between B. napus and B. carinata (BBCC, 2n = 34), B. napus and B. juncea (AABB, 2n = 36) also exhibit strong biomass heterosis (Meng et al., 1998; Liu, 2000; Liu et al., 2001). However, this kind of heterosis cannot be used in seed production because of unbalanced chromosome pairing during meiosis (Grirke et al., 1999). Brassica napus, B. carinata, and B. juncea are amphidiploid species, which originated from the natural doubling of the hybrids between two of three diploids, B. rapa (AA, 2n = 20), B. oleracea (CC, 2n = 18), and B. nigra (BB, 2n = 16) (U, 1935; and Tsunoda, 1980). Divergent evolution and artificial selection have caused differentiation within the same genome among different species. To distinguish such differentiation, the concept of subgenome was introduced to the genus Brassica. Ar, Bb and Co were designated as the genome constitution in three diploid species, B. rapa (ArAr), B. nigra (BbBb, here b refers for the first letter of the term "black mustard") and B. oleracea (CoCo), and the letters AnCn, AjBj, and BcCc were used for three amphidiploid species, B. napus (AnAnCnCn), B. juncea (AjAjBjBj), and B. carinata (BcBcCcCc), respectively (Li et al., 2004). Thereafter, most interspecific hybrids in Brassica spp. could be considered as intersubgenomic hybrids, such as ArAnCn (B. rapa xB. napus) and ArBcCc (B. rapa x B. carinata). Brassica napus (rapeseed) (AnAnCnCn) is a widely grown oilseed crop in the world. If a new-typed B. napus, ArArCcCc, can be created by interspecific hybridization and selection, a hybrid of ArAnCcCn, where normal chromosome pairing might be expected, could be developed for seed production by crossing the new-typed B. napus (ArArCcCc) to natural B. napus (AnAnCnCn). Consequently, strong interspecific heterosis would be realized in the form of intersubgenomic heterosis in B. napus since there are significant correlations between biomass production and seed yield in rapeseed and other crops (Cabelguenne et al., 1999; and Liu, 2000).

Two aspects are addressed in this paper: (i) a way to create the partial new-typed B. napus (ArArCcCc) by combining the Ar subgenome of B. rapa and Cc subgenome of B. carinata; and (ii) heterosis potential for seed production with intersubgenomic hybrids between partial new-typed B. napus lines and natural B. napus.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Plants Materials and Field Experiment
Nine pentaploid combinations (ArAnBcCnCc) between synthetic hexaploid plants (ArArBcBcCcCc) and cultivars of natural B. napus (AnAnCnCn) were self-pollinated to produce new-typed B. napus (Li et al., 2004; Table 1). Seed yield potential of intersubgenomic hybrids was tested with the plants of partial new-typed B. napus selected in F3, F4, and F5 generations and cross-pollinated with natural B. napus as a tester in the three successive years. All F1s were planted in the field in a randomized block design in Wuhan, China. In the first year one-row plots were used with 12 plants in each row and two replications. Rows were 1.9 m long with a spacing of 25.6 cm between rows. Eight plants in the center of each plot were harvested to measure the seed yield. The experiment in the second year was planted in two rows per plot with two replications. Zhongyou 821 (an elite cultivar of B. napus with high erucic acid and high glucosinolates in seed, which is widely used as a standard cultivar in regional tests of rapeseed cultivars in recent years in China) was used as a control in the first and the second year. In the third year (2003), hybrid plants and their parents were grown in three-row plots with three replications. Twenty-four plants in the center of each plot were harvested to determine seed yield and high-parent heterosis (HPH). Soil type in Wuhan is the yellow-brown soil.


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  		Table 1. Plant materials used for developing new-typed B. napus.

 
Erucic acid and glucosinolate content in seeds was analyzed using near-infrared reflectance spectroscopy (Velasco and Möllers, 2000).

Cytological Methods
Root tips and young styles were used to determine chromosome number of the new-typed B. napus lines. Chromosome counting and meiosis behavior analysis followed the method of Li et al. (2004). The pollen-germination ability was measured following Roberts et al. (1983) with minor modifications.

Molecular Marker Analysis
Total genomic DNA was isolated from young leaves as described by Horn and Rafalski (1992) and digested with two restriction enzymes, EcoRI and MseI, for AFLP analysis. The adaptor ligation and two successive PCR reactions followed the method described by Vos et al. (1995). Four pairs of primers with three selective nucleotides at the 3' end were used: E+AGT/M+CTC, E+AAG/M+CTC, E+AGC/M+CAA, and E+AGC/M+CAT, which were selected from 16 AFLP primer pairs. Silver staining followed by the manual of sequencing kit of Q4310 (Promega Corporation, Madison, WI).

Five primer pairs, Ra3-H09, Ra2-H12, Ra3-C04, Ra2-H07,

and Na10-E09, which were selected from 22 primers downloaded from the Brassica database (UK CROPNET, www. ukcrop.net/perl/ace/search/BrassicaDB; verified 26 Aug. 2005), were used for developing SSR markers. The PCR procedure followed the method of Saal et al. (2001).

Each DNA band of AFLP and SSR on the polyacrylamide gel was treated as a separate character and scored as either present (1) or absent (0). Parental specific bands of B. rapa and B. carinata were scored from total bands appearing in new-typed B. napus. Specific bands from B. nigra (‘Juntus’) were used to monitor the bands of Bc genome from B. carinata. The index of subgenomic components, ISG (Xy), was used to estimate the ratio of introgression of foreign subgenome, which was visualized by the molecular markers, within corresponding genome A or C in the new-typed B. napus. Where Xy = Ar, Cc, or Ar + Cc.

Formula

Formula

Formula
Where nAr or nCc is the number of subgenomic specific bands that appeared in new-typed B. napus and their parents of B. rapa (Ar genome) and B. carinata (Cc genome), respectively. N is the total bands that appeared in new-typed B. napus. Analysis of variance (ANOVA) of different combinations was done with Statistical Analysis System (SAS Institute, 1994). Correlation coefficients among seed yield, seed yield components and the genomic components in new-typed B. napus were calculated through the CORREL analysis with Microsoft Excel.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Production of Partial New-Typed B. napus and Its Fertility
Thousands of seeds were obtained from selfing the 196 pentaploid hybrid plants (ArAnBcCcCn, 2n = 46) that were derived from crosses between the synthesized hexaploid of ArArBcBcCcCc (2n = 54) and double-low cultivars (low erucic acid and low glucosinolates) of B. napus (AnAnCnCn, 2n = 38) (Li et al., 2004) (Table 1). Seven hundred fifty-three seeds with zero erucic acid and low or medium glucosinolate content were screened out from 25 000 seeds. Chromosome number varied a lot with a range of 30 to 55 and a mode of 38 in those double-low plants (Fig. 1 ). It would indicate the Bc chromosomes were lost partially or completely during meiosis of pentaploid plants.


Figure 1
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  		Fig. 1. The variation of chromosome numbers in plants derived from pentaploid hybrids (AnArBcCnCc).

 
Ninety 38-chromosomed plants, which were coincident with the chromosome number of natural B. napus, were subjected to fertility analysis and heterosis potential estimation. Nineteen bivalents were observed in pollen mother cells (PMCs) in most cases suggesting that Ar/An and Cc/Cn chromosomes paired well in the new-typed B. napus although the paired chromosomes, or paired segments, may come from different species (Fig. 2a ). However, unpaired chromosomes were also observed in PMCs with low frequency (Fig. 2b), which reflected that a few chromosomes from Bc genome may be transmitted to the progenies or a few Ar/An or Cc/Cn recombinate chromosomes do not pair well in some combinations.


Figure 2
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  		Fig. 2. Fertility characteristics of new-typed B. napus. (a) A PMC with 19 bivalents from one of 38-chromosomed plant family, 1SH. (b) A PMC with univalents in one partial new-typed B. napus of 1SH family (arrow shows the univalent). (c) Developing siliques from another 38-chromosomed family, GXX, showing normal seed setting.

 
Pollen grains of 38-chromosomed plants germinated well in general in the medium. The germination ratio varied with individuals, from 65.3 to 90.8% with an average of 79.4% (Table 2). The pollen fertility of 38-chromosomed plants was proven in vivo where numerous germinated pollen grains with pollen tubes entering stigma tissue could be observed from the plants with higher pollen germination ratios. Seed set of 38-chromosomed plants was near normal in most cases but still varied a lot with individual plants (Fig. 2c, Table 2).


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  		Table 2. Characteristics of fertility of new-typed B. napus.

 
After chromosome selection, the genomic composition of 38-chromosomed plants was estimated with 274 AFLP markers and 43 SSR markers. Ar and Cc subgenomic specific markers were detected from all of the chromosome-selected plants (Fig. 3 ). The index of ISG (Ar + Cc) in the genome varied a lot with different individuals, from 11.85 to 83.25%, and was about 50% on average (Table 3). The 38-chromosomed plants with partially ArCc replacement were termed as partial new-typed B. napus (Ar/nAr/nCc/nCc/n) to distinguish from natural B. napus. The Bc genome specific bands appeared in every new-typed B. napus plant at very low frequencies, which indicated that the chromosomes of Bc genome were basically excluded from the partial new-typed B. napus after selfing the ArAnBcCcCn pentaploids. It also suggested that some chromosome fragments of Bc genome might have been introgressed into the partial new-typed B. napus via homeologous chromosome recombination, and the probability of Bc chromosome substitution plants, if any, should be very few.


Figure 3
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  		Fig. 3. Identification of new-typed B. napus with AFLP markers. Lanes from left to right: B. nigra var. Juntus (BbBb), B. oleracea var. Sucheng 1 (C°Co), B. rapa var. Shiqian Baiyoucai (S) (ArAr), B. carinata var. 10167 (BcBcCcCc); and B. napus var. Hua Shuang 3 (H) (AnAnCnCn) and individual plants of partial new-typed B. napus (Ar/An/Cn/Cc) came from a F3 family derived from 1SH, an interspecific cross, (B. carinata var. 10167 x B. rapa var. Shiqian Baiyoucai) x B. napus var. Hua Shuang 3. The subgenomic specific bands were shown with blank arrow (Ar), coattail arrow (Bc), and quinquangular arrow (Cc), respectively. AFLP markers were amplified with the primer pair E+AGT/M+CTC.

 

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  		Table 3. The replacement of subgenomes in new-typed B. napus estimated with molecular markers.

 
Seed Yield Potential of Partially Intersubgenomic Hybrids
The partial new-typed B. napus (Ar/nAr/nCc/nCc/n) was cross-pollinated with natural B. napus (AnAnCnCn) in the three successive years to test the seed yield potential of partially intersubgenomic hybrids Ar/nAnCc/nCn. One hundred eighty-three double-low (low erucic acid and low glucosinolates) plants from nine families of new-typed B. napus in the F3 generation were selected to randomly hybridize with five cultivars of natural B. napus. Three hundred seventy-three partially intersubgenomic hybrids were produced in 2000. Most of the intersubgenomic hybrids grew vigorously from seedling stage to flowering stage (Fig. 4a , b). Fertility of intersubgenomic hybrids was highly correlated with the parents of new-typed B. napus (r = 0.77). Seed yield of intersubgenomic hybrids was better than the control and showed obvious over-standard heterosis on average (Table 4) but varied greatly according to parental combinations, ranging from 3.36 to 20.43 g plant–1. Almost two-thirds of the hybrid combinations exceeded the control cultivar in seed yield (Fig. 5 ).


Figure 4
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  		Fig. 4. Intersubgenomic hybrids growing at different stages. (a) Seedlings. Left two, a intersubgenomic hybrid Xiangyou 15 x GXX-5; right two, natural B. napus, elite cultivar Zhongyou 821 as standard control. (b) The intersubgenomic hybrid of Xiangyou 15 x GXX-5 at flowering stage (blank arrow and coattail arrow represent Zhongyou 821 and intersubgenomic hybrid, respectively).

 

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  		Table 4. Seed yield and heterosis of partially intersubgenomic hybrids between natural B. napus and new-typed B. napus lines selected from F3 and F4 generation, respectively.

 

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  		Table 6. Correlation coefficients between the content of Ar/Cc subgenome (ISG) in plants of new-typed B. napus and the seed yield of intersubgenomic hybrids.

 

Figure 5
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  		Fig. 5. Frequency distribution of partially intersubgenomic hybrids on seed yield. Curve I and II represent the seed yield of hybrids that were made with partial new-typed B. napus in F3 and F4 generations separately and sown in 2000 and 2001, respectively. The asterisk on the curve shows the seed yield of Zhongyou 821.

 
Forty-one plants from five families of new-typed B. napus lines were selected in the F4 generation for crossing with three sterile lines of natural B. napus. Sixty-three F1s were obtained and grown for seed yield testing in 2001. Although variation of the seed yield of intersubgenomic hybrids was still large, from 5.78 to 18.64 g plant–1, the variation coefficient was reduced, from 3.18% down to 2.58%, compared with the previous growing season. The families showed the same general level of heterosis as the F3 generation in seed yield and almost all of intersubgenomic combinations exceeded the control cultivar (Table 4; Fig. 5).

Three lines of partial new-typed B. napus, 1TH-1–3, GXX-1–3, and GXX-2–3, with desirable characteristics were further selected from the F5 generation. Compared with their AnCn receptor parents of natural B. napus, ‘Hua Shuang 3’ and ‘Xiang You 15’ (Table 1), the three new lines had much higher yield than their receptor parents, more than 21.8% on average (Table 5). Because the yield improvements for the new lines were the results of Ar and Cc introduced from B. rapa and B. carinata respectively, a kind of "fixed heterosis" might be achieved from Ar/nAr/nCc/nCc/n genomic interactions. The three new lines were then crossed to five tester cultivars of natural B. napus (including the two receptors) to further test the potential of intersubgenomic hybrids on seed production. Half of combinations showed high parent heterosis (HPH) of 11.98% on average. Two combinations had HPH values of ≥40% (Table 5). Significant differences were found among testers for general combining ability for seed yield (P ≤ 0.01). The highest HPH value was achieved when the three new lines were crossed to the European tester ‘Grouse’. The seed yield of five hybrids (Ar/nAnCc/nCn) was higher on average than that of their new-typed B. napus parents (Ar/nAr/nCc/nCc/n), which revealed the crossed intersubgenomic heterosis in addition to the fixed heterosis.


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  		Table 5. Seed yield and high-parent heterosis (HPH) of partially intersubgenomic hybrids between natural B. napus and new-typed B. napus lines selected from F5 generation.

 
The Correlation between Hybrid Seed Yield and the Content of Ar/Cc in the Partial New-Typed B. napus
Data collected from 120 intersubgenomic combinations involving three family–tester groups, that is, 1SH x Hua Shuang 3, 1Sv6 x 6203, and GXX x Xiang You 15 (Table 4), were chosen to analyze the relationship between the seed yield of the hybrids and the content of Ar/Cc in new-typed B. napus parents. Since the tester was also used as a parent to develop the new-typed B. napus in each family–tester group (Table 1), the genetic background of the tester was different from the hybrids only without any newly introduced subgenomes, Ar and Cc. Thereafter, the yield differences between hybrids in the same family–tester group represented the effect of content of Ar and Cc subgenome in different plants of new-typed B. napus. Correlation analysis showed that the subgenomic portion of Ar or Cc in each plant of new-typed B. napus, indicated with ISG (Xy), was positively correlated with the seed yield in hybrids. When both Ar and Cc composition, indicated with ISG (Ar + Cc), were considered, correlation coefficient values were increased significantly with an average r value of 0.56 in three investigated families (Table 6, Fig. 6 ). This indicates that the introduction of Ar and Cc components into new-typed B. napus substantially increased heterosis in the subgenomic hybrids. On the contrary, the ISG Bc showed a negative correlation with the seed yield of intersubgenomic hybrids although Bc specific DNA bands appeared in new-typed B. napus with a low frequency.


Figure 6
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  		Fig. 6. The scatter plot of intersubgenomic hybrids derived from crosses between natural B. napus cultivar Huanshuang 3 and plants of 1SH, partial new-typed B. napus.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
As a cultivated oilseed crop, B. napus has progressively increased its role as an economic edible crop in several countries although it is only 400 yr old as a known species (Gómez and Prakash, 1999). By contrast, B. rapa was cultivated in Europe around 2500 to 2000 BCE and spread to Asia after 1000 BCE. It is widely distributed with some desirable characteristics as an oilseed crop, such as self-incompatibility, good adaptation to dry conditions, and maturity that is earlier than other Brassica crops (Mackay, 1977; Choudhary et al., 2000; Liu, 2000). Interspecific hybridization between B. napus and B. rapa has had great success and led to a large number of cultivars released in the past century (Liu, 2000). This indicates that the chromosomes of the Ar and An subgenome would be very compatible in the recombined B. napus.

On the other hand, B. carinata (BcBcCcCc) has been grown for centuries in Ethiopia with several desirable traits, such as drought tolerance and disease resistance (Singh and Singh, 1987; Malik, 1990; Gómez and Prakash, 1999). More recently, yellow-seeded genes have been successfully transferred from old species, B. rapa and B. carinata, into B. napus. The fertility of those new yellow-seeded lines of B. napus was restored to normal (Qi et al., 1996; Meng et al., 1998; Rahman, 2001), indicating that the Cn/Cc and Ar/An subgenomes could coexist in phase. In our previous study, ≥19 bivalents could be observed in about 80% of PMCs of pentaploid hybrids (ArAnBcCcCn) (Li et al., 2004). This implies that 10 chromosomes of An subgenome and nine chromosomes of Cn subgenome from B. napus in the pentaploid could pair well with their 10 compatriots of Ar subgenome from B. rapa and nine compatriots of Cc subgenome from B. carinata, respectively. Further evidence for the successful incorporation of Ar/An/Cn/Cc subgenomes was obtained from the current studies with 38-chromosomed plants from which normal meiotic behavior of PMCs, good pollen germination, and good seed set were observed. It appears that the new-typed B. napus with ArAnCcCn constitution could have very high selective advantages as an allotetraploid (Osborn et al., 2003). The fact that some lines of partial new-typed B. napus show obvious yield improvement might imply that the introduction of Ar and Cc from B. rapa and B. carinata creates a kind of "fixed heterosis" as one advantage of the allotetraploid.

Genetic relationship between parents has been widely used to estimate hybrid seed yield in maize (Zea mays L.), rice, and other crops (Lee et al., 1989; Boppenmaier et al., 1992; Stuber et al., 1992; Buszza, 1995; Zhang et al., 1997; Li et al., 1998). It was found that there are strong correlations between genetic distance and midparent heterosis for seed yield in rapeseed (Ali et al., 1995; Diers et al., 1996). Thus, a high level of heterosis might be produced from the intersubgenomic hybrids (ArAnCcCn) because they combined four subgenomes, which were derived from three different species, that is, B. rapa, B. carinata, and B. napus, respectively. Just as expected, most of intersubgenomic crosses exceeded the yield of the elite cultivar in two successive years and half of the intersubgenomic hybrids showed high-parent heterosis in the third year. It seems that the intersubgenomic hybrids between new-typed B. napus and the natural type of B. napus has great potential in rapeseed heterosis breeding.

Correlation analysis showed that the ratio of subgenome Ar and Cc in new-typed B. napus was positively related to the seed yield of intersubgenomic hybrids. It should be mentioned that only a small number of donor accessions, seven in B. rapa and two in B. carinata, were involved in this experiment. Considering the quantity of available germplasm in the two species (Liu. 2000), the contribution of Ar and Cc to the intersubgenomic heterosis could be different with other accessions. Regardless, the combined effects of Ar and Cc contribute more to heterosis than either one alone since the value of the correlation coefficient was significantly greater when both subgenomes, Ar and Cc, were considered together.

In fact, the new-typed B. napus presented in this paper is only partially new-typed B. napus because the genomic composition of Ar + Cc only occupies 50% of the plant genome on average, as revealed by the value of ISG (Ar + Cc). Consequently, our intersubgenomic hybrids actually showed partial intersubgenomic heterosis due to partially replacement of Ar and Cc genomes in the new-typed B. napus. On the other hand, correlation analysis has shown that to increase the genomic portion of Ar and Cc in new-typed B. napus will favor the seed setting of corresponding intersubgenomic hybrids. Therefore, it would be desirable to increase the Ar and Cc genome compositions in the new-typed B. napus to achieve stronger intersubgenomic heterosis. Individual new-typed B. napus plants with a high value of ISG (Ar + Cc) have been crossed recently. Intensive selection for recombinants will be performed, which should have a higher value of ISG (Ar + Cc) as estimated with molecular markers in the segregating population.


   ACKNOWLEDGMENTS
 
This work was supported by High Project of Science and Technology in China (863) and Doctoral Foundation of Education Department in China. The authors are grateful to Drs. Zhun Yan and Ganlu for their critical reading of the manuscript.

Received for publication December 25, 2004.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 





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