ARTICLES Chinese Science Bulletin 2006 Vol. 51 No. 9 1078—1084

DOI: 10.1007/s11434-006-1078-4

Genetic contribution of foreign germplasm to elite Chinese soybean (Glycine max) cultivars revealed by SSR markers QIN Jun2, CHEN Weiyuan3, GUAN Rongxia1, JIANG Chengxi3, LI Yinghui1, FU Yashu3, LIU Zhangxiong1, ZHANG Mengchen2, CHANG Ruzhen1 & QIU Lijuan1 1. National Key Facility of Crop Gene Resources and Genetic Improvement, Key Lab of Crop Germplasm Resources & Biotechology (MOA), Institute of Crop Science, Chinese Agricultural Academy of Sciences, Beijing 100081, China; 2. Hebei Academy of Agricultural and Forestry Science, Shijiazhuang 050031, China; 3. Heilongjiang Academy of Agricultural Science, Suihua 152052, China Correspondence should be addressed to Qiu Lijuan (email: qiu_lijuan @263.net) Received October 8, 2005; accepted January 23, 2006

Abstract Simple sequence repeats (SSR) marker analysis, combined with pedigree analysis, was carried out to trace the genetic constitutes of Suinong 14 and Hefeng 25 in assessing the contribution of foreign germplasm to those elite cultivars. The overall goal is to accumulate information for further effective utilization of foreign germplasm in Chinese soybean breeding programs. SSR clustering results indicated that the genetic base of elite Chinese soybean cultivars, including Suinong 14 and Hefeng 25, were broadened and enhanced via introduction of Amsoy from the U.S. and Shishengchangye from Japan. The pedigree analysis showed a very high coefficient of parentage between Shishengchangye and Hefeng 25, between Shishengchangye and Suinong 14, and between Amsoy and Suinong 14. The genetic similarity between Suinong 14 and Hefeng 25 was 60.58%. Among 20 linkage groups, more genomic regions were transferred from Hefeng 25 to Suinong 14 in linkage group (LG) I, L and C2 than other LGs. Among the unique alleles of foreign parents, five specific loci in Amsoy were transferred to Suinong 14, and three loci from Shishengchangye to Suinong 14. Some SSR loci were proved to be correlated with phenotypes: two loci for seed size introgressed from Shishengchangye to Suinong 14, and one locus for 1078

protein content from Amsoy to Suinong 14. These results indicate that the two foreign parents might have important contributions in the development of Suinong 14 and Hefeng 25. Keywords: soybean, pedigree analysis, simple sequence repeats (SSR), genetic relationship.

Among 651 soybean (Glycine max) cultivars released from 1923 to 1995, most of the parents used in the breeding program of northeast China and Huanghuai-hai valley were cultivars well adapted to local ecologic areas. Narrow parentage and lack of genetic diversity will constrain the genetic basis and ultimately ― delay the progress breeding programs[1 4]. Recently, although exotic germplasm lines and cultivars adapted to different ecologic areas have been introduced and used as parents, the number and scope are still very limited[5]. It is important to broaden the genetic basis and enhance the gene pool of global soybean germplasm for current and future soybean breeding programs. Pedigree analysis of 130 improved cultivars in Canada showed that the core gene pool was enriched and developed in the process of developing high yielding soybean cultivar[6]. Similarly, the foreign germplasm in soybean breeding program plays an important role in increasing genetic diversity and yield. RAPD analyses indicated that significant genetic difference existed between Chinese and American soybean cultivars, thus offering molecular evidence for the application of foreign germplasm to broaden genetic basis in soybean breeding program[7]. By the year of 1995, 224 cultivars with foreign germplasm parentage had been released with a total of 46 foreign germplasms as parents[8]. However, those foreign parents were mostly several core germplasm lines. The number of cultivars derived from Japanese cultivar Shishengchangye and American cultivar Amsoy was 52 and 19, respectively. Genetic contribution of these two cultivars to released cultivars was 13.41% and 4.88%, respectively. Amsoy was one of the most frequently used ancestor lines in northeast China. Previous studies on the contribution of exotic germplasm were mainly focused on genetic contribution[1,4,6,9]. The genome-wide relationship between agonomic traits and molecular markers such as SSR should be investigated to facilitate the genetic manipulation of important traits in soybean breeding programs. Most of the economically important traits follow a complex inheritance pattern. Association study of these complex traits based on linkage disequilibrium (LD) Chinese Science Bulletin

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ARTICLES originally used in human genetics would help to reveal their genetic pattern. Both Hefeng 25 and Suinong 14 are typical elite soybean cultivars. Hefeng 25 has been cultivated for more than 20 years and its accumulative growing area is over 12 Mha. In 2003, its growing area was still over than 0.13 Mha, the fourth cultivar with the most growing-area. Suinong 14 is another cultivar with a large growing-area. From 1996 to 2002, its accumulative growing-area in Heilongjiang, Jilin, and Inner Mongolia exceeded 2 Mha, with a yield of more than 637.196 t. Both cultivars have foreign ancestry, and Hefeng 25 is the parent of Suinong 14. The objective of this study was to clarify the genetic pattern of exotic genes in typical elite background by using SSR marker and pedigree analyses, and to explore the potential of using exotic germplasm in soybean breeding program. 1 1.1

Materials and methods Plant materials

5236×Shishengchangye. The ancestor parents Sui 70-6, Amsoy and Suinong 4, are traced back to Suinong 8. Cultivar Shishengchangye has the characteristics of short stem internode, strong stalk, and good adaptability. Another exotic germplasm, Amsoy, possesses strong stalk trait, good adaptability, and desirable plant type. The parents of Hefeng 25, Sui 70-2, Ke 69-5236 and F1 of the cross Sui 70-2×Amsoy were not included because of their unavailability. 1.2

Field tests for morphological evaluation were conducted in a completely random block design with three replicates on the research farm at Institute of Agricultural Science of Suihua City, Heilongjiang Province. The morphological and agronomic traits included maturity, the first flowering date (R1 developmental stage), seed size (100-seed weight), plant height, crude protein content, and crude fat content. 1.3

A total of nine ancestor parents are involved in the development of Suinong 14 and Hefeng 25. They are Zihua 4, Yuanbaojin, Keshansilijia, Xiaolidou 9, Ke 69-5236, Shishengchangye, Sui 70-6, Amsoy and Suinong 4 (Fig. 1). Suinong 14 is a progeny of the cross Hefeng 25×Suinong 8. Hefeng 23, the female parent of Suinong 25, is a progeny of Xiaolidou 9×Fengshou 10. The ancestor parents Zihua 4, Yuanbaojin and Keshansilijia are traced to Fengshou 10. Ke 4430-20, the male parent of Hefeng 25, is a progeny of cross Ke 69-

Agronomic evaluation

SSR analysis

Genomic DNA was isolated with modified SDS method[10] and purified with phenol/chloroform extraction. PCR was conducted on PE9600 (Perkin-Elmer). Each 20 μL PCR reaction consisted of 30 ng of soybean genomic DNA as template, 2 μL 10× PCR buffer, 0.15 mmol/L dNTPs, 1 U Taq DNA polymerase, 0.15 μmol/L primers. Amplification conditions were 95℃ for 5 min, 35 cycles of denature at 94℃ for 30 s, annealing at 47℃ for 30 s, extension at 72℃ for 45 s, followed by a terminal extension at 72℃ for 5 min. The

Fig. 1. Pedigree of Suinong 14 soybean.

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ARTICLES PCR products were loaded and electrophoresesed on a denaturing gel containing 6% polyacrylamide. Gels were dried and photographed to collect data. 1.4

Data analysis

Polymorphic DNA segments amplified with SSR loci primer pair were scored as present (1) or absent (0). Cluster analysis was performed by using NTSYS (Version 2.1) based on binary code data matrix. A pedigree tree was constructed with UPGMA (Unweighted Pair Group Method with Arithmetic Mean) based on genetic similarity coefficient matrix. LD and its association with agronomic traits were evaluated with TASSEL. Mean square standard error and significant tests were analyzed by using SAS6.12 (SAS Institute). 2

Results

2.1 Analysis of genetic similarity among different germplasm lines Coefficient of parentage (CP) was calculated for 14 germplasm lines on the basis of parentage information (Table 1). CP for Hefeng 25 and its five parental lines ranged from 0.094 to 0.250; CP for Suinong 14 and its seven parents ranged from 0.047 to 0.250. Hefeng 25 had a CP of 0.25 with Shishengchangye, while Suinong 14 had a CP of 0.125 with both Shishengchangye and Amsoy, indicating that these two exotic germplasm lines contributed more to Suinong 14 and Hefeng 25 than other parents did. Cluster analysis of genetic distances showed that all sampled cultivars were clustered to four groups at the similarity coefficient of 0.5 (Fig. 2). The first group consisted of only Zihua 4; the second group consisted of Yuanbaojin, Keshansilijia, Xiaolidou 9, Hefeng 23 and Fengshou10; the third group consisted of Amsoy, Suinong 4, Suinong 8, Suinong 14 and Hefeng 25; and the fourth group consisted of Shishengchangye and Ke 4430-20. The dendrogram showed that no germplasm lines with exotic germplasm parentage were included in the first two groups. Through introgression of Japanese and American germplasm lines, Suinong 4, Suinong 8, Suinong 14 and Hefeng 25 significantly differed from these cultivars in groups 1 and 2, indicating that exotic Cultivar Hefeng 25 Suinong 14

Zihua 4 0.094 0.047

gene pool played an important role in enriching the genetic basis of Hefeng 25 and Suinong 14. A significant correlation (y=0.91) observed between CP and genetic similarity coefficient of Hefeng 25 showed an association between the two coefficients and the true genetic relatedness of the germplasm. SSR polymorphic variation analysis revealed that there were unique alleles at eight loci (Satt336, Satt467, Satt465, Satt628, Satt701, Satt682, Satt715 and Sct_065) in Shishengchangye and three loci (Satt440, Satt583 and Satt614) in Amsoy. These results indicated that there are significant genetic variation between exotic germplasm lines and domestic germplasm lines, which justifies the utilization of exotic germplasm sources in soybean improvement program. 2.2 Origins of genomic SSR marker variations in Suinong 14 and Hefeng 25 A total of 135 SSR loci covering 20 soybean linkage groups (LG) were used to evaluate the genetic similarity of all sampled cultivars. A genetic similarity estimate of 0.6058 between Suinong 14 and Hefeng 25 was found where 1.0 was defined as genetic identity. When the number of primers used increased to 280, the genetic similarity estimate changed to 0.6866, indicating that genetic variation occurred only at limited loci during the course of cultivar improvement. Among 280 polymorphic SSR markers, 43 specific SSR loci of Suinong 14 were transmitted from Hefeng 25. The distribution of these 43 loci on linkage groups was not uniform across different linkage groups: five loci on LG I, five loci on LG L, and five loci on LG C2; other 28 loci on other 17 LGs. Seventeen of the 43 SSR loci have been reported as QTLs associated with maturity, quality, and disease resistance, and eight of them were on LG I, L, and C2. These results implied that Hefeng 25 and Suinong 14 harbored longer similar genetic fragments on LG I, L and C2. Twenty-seven specific SSR loci of Hefeng 25 were derived from Shishengchangye; three of them were transmitted to Suinong 14 (Table 2). Satt190 and Satt455 were QTL associated with seed weight[11,12]. Five SSR loci associated with stem rot resistance, pod number per plant and seed weight were ― derived from Amsoy[13 17] and were transmitted to Su

Table 1 Coefficient of parentage (CP) of Suinong 14 and Hefeng 25 Parents Yuanbaojin Keshansilijia Xiaolidou 9 Shishengchangye 0.094 0.188 0.250 0.250 0.047 0.094 0.125 0.125

Amsoy a) ― 0.125

Suinong 4 a) ― 0.250

a) ―, Data not available.

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Fig. 2. UPGMA dendrogram for Suinong 14 and its parents determined on the basis of genetic similarity by means of 135 SSR markers.

Cultivar

Locus

AMSOY

Satt102 Satt545 Satt160 Satt192 Satt499 Satt499 Satt690 Satt690 Satt455 Satt455 Satt455 Satt455 Satt513

Shishengchangye

Table 2 Unique SSR loci in exotic germplasm associated with agronomic traits Related reports LG marker linked to genetic distance (cM) related agronomic trait specific locus K Seed weight A1 Sclerotinia stem rot F Sat_039 5.32 Pod maturity H Satt442 2.94 Sclerotinia stem rot K Satt046 7.58 Sclerotinia stem rot K OW13-900 7.58 Sclerotinia stem rot C1 Satt565 0.00 Seed weight C1 SOYPATA 4.64 Protein A2 K443-2 5.30 Seed weight A2 M0103-1 6.30 Aluminium Tolerance A2 A505-1 10.30 Protein A2 A505-1 10.30 Oil I Satt373 1.07 First flower（2）

inong 14 via Suinong 8 . No polymorphism was detected at 20 SSR loci covering 12 linkage groups between Suinong 14 and its domestic parents. These loci mainly distributed on LG B2 and F. It is very likely that conservative loci may contain important genetic information for specific agronomic traits. When exotic germplasm lines were included, 15 SSR loci still did not show polymorphism except two loci on LG B2, two loci on LG F, and one locus on LG D, indicating that certain genes on LG B2, F and O may have potential use value. Five of these 15 SSR loci were reported as agronomic-traits-related － QTL[13,16,18 20]. Satt306 was seed weight QTL[18]; Satt 310[19] and Satt178[13] were protein content QTL; Satt287 was QTL for leaf area, leaf width, maturity, and seed filling period[16], Satt492 was a QTL for rot stem www.scichina.com

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contribution ration (%) 2.80 19.00 8.00 6.50 9.60 15.10 12.00 10.80 10.00 11.20 8.90 16.74

ref. [13] [14] [15] [16] [17] [17] [11] [16] [12] [21] [22] [22] [16]

resistance[20]. It was presumed that these conservative fragments contained important genetic information. 2.3

Linkage disequilibrium between SSR markers

A total of 120 SSR polymorphic loci consisting of 7200 marker paires were identified. LD was significant at a comparison-wise 0.01 level in nearly 1.64% of SSR marker pairs when all cultivars were included. Based on linkage distance of all SSR loci, five loci were considered to be tightly linked (<1.5 cM), eight loosely linked (>1.5 cM within one LG), and 105 unlinked. LD between pairs of SSR loci are summarized in Table 3. Three of 144 specific SSR marker pairs at 17 SSR loci shared by Suinong 14 and Hefeng 25 showed LD. They were Satt557-Satt134, Satt186- Satt301, and Satt186-Satt413. 1081

ARTICLES Locus Satt348 Satt557 Satt529 Satt420 Satt583 Satt703 Satt347 Satt615 Satt476 Satt413 Satt259 Satt301 Satt684

LG F C2 J O B1 D1b O D2 C1 D2 O D2 A1

Table 3 LD among SSR markers of Suinong 14 and its parents Position Locus LG Position 15.29 Satt269 F 11.37 112.09 Satt134 C2 112.84 41.90 Satt380 J 43.01 49.71 Sat_221 O 51.01 84.19 Satt415 B1 82.89 98.75 Satt172 D1b 100.89 42.29 Satt259 O 39.82 91.21 Satt301 D2 93.71 80.62 Satt195 C1 84.81 113.61 Satt186 D2 105.45 39.82 Sat_221 O 51.01 93.71 Satt186 D2 105.45 0.00 Satt155 A1 32.68

2.4 Association analysis of SSR loci and agronomic traits In association analysis of six SSR loci with LD and agronomic traits, significant correlations were observed between two pair of LD loci and agronomic traits (p<0.01). Satt380-Satt529 on LG J were associated with 100-seed weight, Satt415-Satt583 on LG B1 were associated with the first flowering. A correlation analysis between 120 SSR polymorphism loci and six agronomic traits (maturity, the first flowering, 100-seed weight, plant height, crude protein content, and crude fat content) was performed. Significant correlation was found between 59 SSR loci and agronomic traits. Almost 49.7% of SSR loci tested showed correlation with agronomic traits. Three of them were associated with maturity, 11 loci with 100-seed weight, seven loci with plant height, nine with crude protein content, 19 with crude fat content, and ten with the first flowering. Among 17 SSR loci shared by Hefeng 25 and Suinong 14, one locus was associated with plant height, four loci with 100-grain weight, six loci with oil content, three loci with first flowering date, and four with protein content (Table 4). Satt291[16] and Sat_089[16] have been shown to be QTL associated with seed weight and plant height, respectively, in accord with this study. 3

Discussion

3.1

CP and origin of genomic SSR marker

CP is a commonly used index in pedigree analy― sis[2,8,23 25]. A genetic diversity analysis of bread wheat using SSR, AFLP and CP revealed a correlation (γ=0.41) between molecular marker results and pedigree information. When pedigree information is not available, molecular data could provide useful reference[11]. In 1082

R2 0.328 0.632 0.827 0.460 0.368 0.389 0.378 0.327 0.377 0.161 0.312 0.230 0.293

D′ 0.893 1.000 1.000 1.000 1.000 0.875 0.856 1.000 0.929 0.665 0.804 0.833 1.000

p 0.008 0.006 0.001 0.001 0.007 0.000 0.007 0.000 0.000 0.009 0.008 0.000 0.006

this study, a significant correlation was observed between CP and SSR data based on genetic similarity coefficient of Suinong 14 and Hefeng 25. This result confirmed the close correlation of pedigree analysis and molecular data. An SSR analysis of Ppd-D1 on the short arm of chromosome 2D fragment in 59 wheat cultivars indicated that it was feasible to study the genetic relationship among lines by using SSR markers[26]. In a pedigree analysis of Europe barley cultivar “Cooper” by using SSR marker, four critical loci were identified on chromosome H3 and H5[27]. In this study, we found that several SSR loci associating with maturity, ― quality and disease resistance[11 17,21,22] might have been transmitted to Suinong 14 via Hefeng 25. These loci were important genetic component for the elite cultivars. The number of conservative loci on LG B2 or F was obviously higher than those on other LGs, which indicated that the distribution of conservative loci was not completely random. These fragments and related SSR are to be further studied to evaluate the potential of application in marker assisted selection (MAS). 3.2 The trace of foreign germplasm and their relationship with domestic cultivar/lines American cultivar Amsoy was selected from the cross Adams ((Illini A.K. select)×Dunfield)×Harosoy (Mandarin×AK) in 1965[28]. A.K., Mandrin and Dunfield were introduced in 1913 from Suihua, Heilongjiang Province and Fanjiatun, Jilin Province, respectively. A.K. was introduced from Northeast China in 1917. Shishengchangye, a Japanese cultivar released in 1947, was selected from the cross Benyu 65×Bendi 326 under island environment. Benyu 65 was selected from local cultivar Dagudi in 1928[29]. Soybean growing in Japan has a history of more than 2000 years. It is presumed that Shishengchangye has little or no Chinese ancChinese Science Bulletin

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ARTICLES Locus

LG

Sat_096 Sat_351 Satt291 Satt159 Satt490 Satt475 Sat_230 Satt318 Satt383

D1b D1b C2 N F K B2 B2 D1a

Table 4 SSR loci shared by Hefeng 25 and Suinong 14 associated with agronomic traits Related Position r p Locus LG Position r agronomic trait 0.000 0.034 Height Satt331 O 93.369 −0.568 −0.617 20.610 0.025 100-grain weight Satt316 C2 127.668 0.581 −0.594 45.757 0.642 0.013 100-grain weight Satt715 K 0.912 0.546 27.132 0.040 100-grain weight Satt583 B1 84.189 −0.553 −0.607 97.966 0.569 0.049 100-grain weight Satt172 D1b 100.89 −0.546 78.683 0.041 Oil Sat_150 L 53.671 0.683 −0.551 72.076 0.015 Oil Sat_229 F 62.790 −0.633 −0.677 70.120 0.019 Oil Satt241 O 59.489 0.645 −0.617 56.666 0.654 0.011 Oil Satt335 F 77.704 −0.677

estry. Soybean is a short day plant, and hence photoperiod and temperature responses are important in determining areas of cultivar adaptation. The level of soil fertility in American is higher than that of Northeast China. Many changes would have taken place after soybean germplasm lines had been introduced from China to the U.S. under different environmental conditions. Qiu et al.[7] studied 18 parental lines of American soybean cultivars including A.K., Mandarin and Dunfield and 57 Chinese cultivars (including Yuanbaojin, Fengshou 6, Fengshou 10 and Hefeng 23) by using RAPD marker. Results showed these germplasm lines from American differed from those Chinese materials and clustered to a different group, although they, or at least one of their parents, originated from China. These results demonstrated that it was feasible to broaden genetic basis by using exotic germplasm resources. 3.3 Genetic contribution of exotic germplasm in enriching the genetic resources of Chinese soybean breeding With similar objectives and materials used in development of new cultivars, the genetic basis among the released cultivars was rather narrow. It is essential to broaden the genetic basis in order to obtain a high yield cultivar with excellent quality[30]. A survey by Qiu[31] on “China Soybean Cultivar Collections” showed that a total 121 of cultivars with exotic parentage have been developed, of which 59 were developed in northeast China. Amsoy and Shishengchangye were widely used parents in breeding programs of northeast China. The excellent agronomic traits of Shishengchangye and Amsoy indicated that in the middle period of the 20th century, Japanese and American breeders developed elite cultivars with valuable genes for disease resistance, stress tolerance, and excellent quality. Through introgression of foreign germplasm, Suinong 14 and Hefeng 25 significantly differed from cultivars released earlier. www.scichina.com

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P 0.019 0.029 0.044 0.021 0.016 0.007 0.008 0.013 0.008

Related agronomic trait Oil First flower First flower First flower First flower Protein Protein Protein Protein

Three loci derived from Shishengchangye were proved to be QTL associated with seed weight, protein content, ― and oil content[11,12,21 24]; five QTL loci derived from Amsoy were associated with rot stem resistance, grain ― weight, and the number of pod[13 17]. There were also some allele variations with potential value of utilization within these exotic germplasm lines. In this study, significant correlations were observed between Satt513[16] and 100-seed weight, between Satt192[16], Satt545[14] and oil content, and between Satt499[17] and seed weight. These results differed from those previously reported, probably due to the difference in number and specificity of cultivars used. Based on clustering arrangement of specific genes on chromosome, these QTL fragments were presumed to be important and will be studied in the near future. 3.4 LD in SSR marker tested in Suinong 14 and its pedigree Sjakste et al.[32] analyzed TCR α/δ gene loci on chromosome q14 of 159 human families and showed that LD typically extends 0―150 kb, with different LD structures among various genomes. Reich et al.[33] found that LD typically extends 60kb in north European American populations, and may extend much farther. It may extent closely in African Nigerian populations. LD study was primarily performed in human genetics, but is underway in plant genetics. Remington et al.[34] were the first to report patterns of genome-wide LD of six genes using a set of 47 SSR loci in 102 maize inbred lines. The SSR loci they studied showed stronger evidence of genome-wider LD than did SNPs. In our study, LD was also found in several agronomictrait-related SSR loci. This implies that LD may influence the use of SSR maker in molecular assisted selection for these agronomic traits. Association studies based on LD can provide valuable genetic information, which is helpful to revealing genetic pattern of complex 1083

ARTICLES agronomic traits, and provide a reliable strategy in molecular assisted selection. Acknowledgements This work was supported by the National Scientific Research Program (Grant No. 2004BA525 B06), High-Tech Plan (863) (Grant No. 2004AA211111), the National Basic Research Program (973) (Grant No. 2004 CB117213) and the National Natural Science Foundation of China (Grant No. 30490250).

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