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Characterization of Soybean Genome Based on Synteny Analysis with Lotus Japonicus

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Characterization of Soybean Genome Based on Synteny Analysis with Lotus Japonicus Breeding Science 58: 157–167 (2008) Characterization of soybean genome based on synteny analysis with Lotus japonicus Yasutaka Tsubokura†1), Ryutaku Onda†2), Shusei Sato†3), Zhengjun Xia1), Masaki Hayashi1), Yukie Fukushima2), Satoshi Tabata3) and Kyuya Harada*1) 1) National Institute of Agrobiological Sciences, 2-1-2 Kannondai, Tsukuba, Ibaraki 305-8602, Japan 2) Graduate School of Science and Technology, Chiba University, 648 Matsudo, Matsudo, Chiba 271-8510, Japan 3) Kazusa DNA Research Institute, 2-6-7 Kazusa-kamatari, Kisarazu, Chiba 292-0818, Japan To apply genomic information of the model legume Lotus japonicus to soybean, the characteristics of the soybean genome in reference to the genome of L. japonicus were investigated. Macrosynteny between soy- bean and L. japonicus was analyzed by mapping the same cDNA clones on the maps of both species by the RFLP method, and by identifying the positions of orthologs on the L. japonicus map for cDNA markers lo- cated on the soybean map. Relatively large synteny blocks were observed between a few linkage groups of L. japonicus and soybean. The major parts of the soybean linkage groups consisted of mosaics of smaller segments syntenic with the L. japonicus genome. The presence of many homoeologous regions on different soybean linkage groups was suggested from the distribution of paralogs and orthologs. To investigate the microsynteny between soybean and L. japonicus, three soybean BAC clones were selected for the GmNFR1a, GmNFR1b and Nts1 genes mapped on the macrosyntenic regions of the linkage groups D1b, B2 and H, re- spectively. We revealed a significantly high level of collinearity between these BAC clones and correspond- ing homologous genomic regions of L. japonicus. The information of L. japonicus could be used for the development of DNA markers, map-based cloning and assembling process of genome sequencing in soybean. Key Words: Glycine max (L) Merrill, Lotus japonicus (Regel) Larsen, macrosynteny, microsynteny, homoeologous region, genome duplication, paralog. Introduction and high transformability with Agrobacterium tumefaciense. The genome resources of L. japonicus, such as the The Fabaceae family is the third largest family of an- sequence and positional information of TAC/BAC clones giosperm plants including around 20000 species of legumes. (http://www.kazusa.or.jp/lotus/index.html), EST libraries The subfamily Papilionoideae includes agriculturally impor- (http://www.kazusa.or.jp/en/plant/lotus/EST/index.html), and tant species such as soybean, pea and common bean, and the complete sequence data of chloroplast and symbiotic model legumes, Lotus japonicus and Medicago truncatula. rhizobium bacteria Mesorhizobium loti (http://www. Additionally, legumes are able to fix nitrogen through sym- kazusa.or.jp/rhizobase/Mesorhizobium/index.html) has been biotic infection with rhizobium bacteria and are character- exploited. In addition to the linkage map of TAC/BAC istized by a high protein content in their seeds. The genomics clones (http://www.kazusa.or.jp/lotus), another linkage map of legumes enables to identify agriculturally useful genes of L. japonicus was also constructed using AFLP, SSR and for efficient breeding as well as accumulation of academic dCAPS markers (Hayashi et al. 2001). knowledge. Soybean is the most important leguminous crop in the L. japonicus is a model plant for the genomics of the world. The genome size of soybean is estimated at 1.12 Gb family Fabaceae, as well as M. truncatula. It displays appro- (Arumunganathan and Earle 1991), a value approximately priate features as a model plant (Handberg and Stougaard 2.5 times larger than that of L. japonicus. It was suggested 1992), including diploidy, self-fertility, small genome size that the soybean genome is the product of a diploid ancestor (432 Mb, Pedrosa et al. 2002, 442 Mb, Ito et al. 2000, 494 (n = 11), which underwent aneuploid loss (n = 10), and sub- Mb, Kawasaki and Murakami 2000), short life cycle (ap- sequent polyploidization (Lackey 1980). The occurrence of proximately 3 months), small number of chromosomes (n = 6) two rounds of genome duplications or hybridizations and rearrangements was estimated by many researchers Communicated by J. Abe (Shoemaker et al. 1996, Shoemaker et al. 2002, Blanc and Received December 27, 2007. Accepted March 25, 2008. Wolfe 2004, Schlueter et al. 2004). *Corresponding author (e-mail: [email protected]) The rapid accumulation of genome sequence informa- † These authors contributed equally to this work tion for L. japonicus and M. truncatula provides a unique 158 Tsubokura, Onda, Sato, Xia, Hayashi, Fukushima, Tabata and Harada opportunity for comparative studies between the model le- N-hydroxycinnamoyl / benzoyltransferase (HCBT) genes gumes and leguminous crops. Though syntenic relationships (Schlueter et al. 2006), fatty acid desaturase 2 (FAD2) genes within Fabaceae are less well characterized compared with (Schlueter et al. 2007a), and LysM kinase genes (Zhang et those of Gramineae, an increasing number of studies has be- al. 2007). gun to reveal extensive synteny between the species of the In the present study, we analyzed the synteny between family. A high level of synteny on entire linkage groups was soybean and L. japonicus to reveal the characteristics of the observed between mung bean (Vigna radiata) and cowpea genome structure of soybean, in reference to the genome of (Vigna unguiculata) (Menanciohautea et al. 1993). Though L. japonicus. comparable levels of synteny were identified between mung bean and common bean (Phaseolus vulgaris), synteny Materials and Methods blocks were more limited between these species and soy- bean (Boutin et al. 1995). Grant et al. (2000) revealed the Plant materials and DNA extraction presence of genome conservation between the soybean link- For L. japonicus, 127 F2 plants derived from a single age group A2 and chromosome 1 of Arabidopsis thaliana. cross between Gifu B-129 and Miyakojima MG-20 were uti- Lee et al. (2001) observed a high level of conservation be- lized as the mapping population. Total DNA from leaves tween the chromosomes of mung bean and common bean, was extracted and purified using a DNeasy Plant Mini Kit and chromosome segments of soybean, where A. thaliana (QIAGEN). The 94 RILs developed by the single seed de- also showed conserved regions to those of legumes which scent method from the same F2 population were also used as enabled to analyze duplicated regions in soybean. Choi et al. the mapping population. The genomic DNAs of RILs were (2004) reported genome-wide macrosynteny among le- extracted by the CTAB method (Murray and Thompson gumes (M. truncatula, M. sativa, L. japonicus, Pisum 1980). sativum, Cicer arietinum, mung bean, common bean and For soybean, 190 F2 plants derived from a single cross soybean), using a large set of cross-species gene-specific between Misuzudaizu and Moshidou Gong 503 or 156 RILs markers. Though the length of the synteny blocks was re- developed by the single seed descent method from the same duced by chromosomal rearrangements in some regions, cross were used as the mapping population. The genomic chromosomes from a variety of Papilionoid species could be DNA of these samples was extracted by the CTAB method aligned, based on the chromosomes of M. truncatula . How- (Murray and Thompson 1980). ever only small synteny blocks were observed between M. truncatula and soybean. Framework maps used and assignments of new markers Yan et al. (2003) analyzed the synteny between BAC The F2 and RIL framework markers of L. japonicus contigs of soybean and M. truncatula, based on hybridiza- were selected from the map of Miyakojima MG-20 previ- tion using soybean RFLP clones and BAC end-sequences as ously constructed (Hayashi et al. 2001). The F2 and RIL probes and observed a microsynteny in 54% of soybean con- framework maps of soybean used in the present study were tigs. Yan et al. (2004) further analyzed three homologous reported by Yamanaka et al. (2001) and Watanabe et al. BAC contig groups in detail by comparative physical map- (2004), respectively. Assignments of the loci detected by the ping and cross-hybridization and identified a microsynteny new markers to linkage groups were performed based on a between soybean and M. truncatula in six of the eight re- comparison between the segregation data of new loci and gions tested. The order and orientation of at least six genes those used for the construction of the framework maps. The was found to be conserved in a 70 kb region, including MAPMAKER/EXP. Ver 3.0b program was used for map apyrase genes from soybean and M. truncatula (Cannon construction. Map distance was estimated from recombi- et al. 2003). Choi et al. (2004) examined two BAC clones nation frequencies using the Kosambi function. The loci from the region containing the cyst nematode resistance detected by the new markers were added to the revised frame- gene, rhg1, of soybean and homologous BAC clones of work map using the try command. A LOD score of 3.0 and a M. truncatula, and revealed that the order and orientation of maximum distance of 32.0 cM were used as linkage criteria. fourteen genes were conserved between these genomes. They also analyzed ten homologous pairs of BAC clones Mapping of TAC/BAC clones of L. japonicus based on SSR from M. truncatula and TAC clones from L. japonicus and length polymorphisms and single nucleotide polymorphisms found that 72 genes (82%) were syntenic between the ge- For the generation of simple sequence repeat (SSR) nomes. Mudge et al. (2005) uncovered two large soybean re- markers, sequence repeats such as (AT)n, (GT)n and gions surrounding the cyst nematode resistance genes, rhg1 (AAT)n above 15 bp were sought on the TAC/BAC nucleo- and Rhg4, that exhibited a synteny with M. truncatula. tide sequences. Design of the primer pairs, PCR and poly- Microsynteny between homoeologous regions within morphism detection were performed as previously reported the soybean genome was also revealed, based on BAC fin- (Harada et al.
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