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1.  Gene divergence of homeologous regions associated with a major seed protein content QTL in soybean 
Understanding several modes of duplication contributing on the present genome structure is getting an attention because it could be related to numerous agronomically important traits. Since soybean serves as a rich protein source for animal feeds and human consumption, breeding efforts in soybean have been directed toward enhancing seed protein content. The publicly available soybean sequences and its genomically featured elements facilitate comprehending of quantitative trait loci (QTL) for seed protein content in concordance with homeologous regions in soybean genome. Although parts of chromosome (Chr) 20 and Chr 10 showed synteny, QTLs for seed protein content present only on Chr 20. Using comparative analysis of gene contents in recently duplicated genomic regions harboring QTL for protein/oil content on Chrs 20 and 10, a total of 27 genes are present in duplicated regions of both Chrs. Notably, 4 tandem duplicates of the putative homeobox protein 22 (HB22) are present only on Chr 20 and this Medicago truncatula homolog expressed in endosperm at seed filling stage. These tandem duplicates could contribute on the protein/oil QTL of Chr 20. Our study suggests that non-shared gene contents within the duplicated genomic regions might lead to absence/presence of QTL related to protein/oil content.
PMCID: PMC3672674  PMID: 23761803
genome duplication; QTL; seed protein content; soybean; sequence divergence
2.  Stem Rot on Adzuki Bean (Vigna angularis) Caused by Rhizoctonia solani AG 4 HGI in China 
The Plant Pathology Journal  2015;31(1):67-71.
During late August and early September 2011, stem rot symptoms were observed on adzuki bean plants (Vigna angularis) growing in fields located in Beijing and Hebei Province, China, respectively. In this study, four isolates were obtained from infected stems of adzuki bean plants. Based on their morphology, and sequence and polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP) analyses of the ribosomal DNA internal transcribed spacers (rDNA-ITS) region, the four isolates were identified as Rhizoctonia solani in anastomosis group (AG) 4 HGI. Pathogenicity tests showed that all isolates were strongly pathogenic to adzuki bean and resulted in serious wilt symptoms which was similar to observations in the fields. Additionally, the isolates infected several other crops and induced related rot on the roots and basal stems. To our knowledge, this is the first report of Rhizoctonia solani AG 4 HGI causing stem rot on adzuki bean.
PMCID: PMC4356607  PMID: 25774112
adzuki bean; anastomosis group; PCR-RFLP; Rhizoctonia solani; stem rot
3.  A Cytosolic Thioredoxin Acts as a Molecular Chaperone for Peroxisome Matrix Proteins as Well as Antioxidant in Peroxisome 
Molecules and Cells  2015;38(2):187-194.
Thioredoxin (TRX) is a disulfide reductase present ubiquitously in all taxa and plays an important role as a regulator of cellular redox state. Recently, a redox-independent, chaperone function has also been reported for some thioredoxins. We previously identified nodulin-35, the subunit of soybean uricase, as an interacting target of a cytosolic soybean thioredoxin, GmTRX. Here we report the further characterization of the interaction, which turns out to be independent of the disulfide reductase function and results in the co-localization of GmTRX and nodulin-35 in peroxisomes, suggesting a possible function of GmTRX in peroxisomes. In addition, the chaperone function of GmTRX was demonstrated in in vitro molecular chaperone activity assays including the thermal denaturation assay and malate dehydrogenase aggregation assay. Our results demonstrate that the target of GmTRX is not only confined to the nodulin-35, but many other peroxisomal proteins, including catalase (AtCAT), transthyretin-like protein 1 (AtTTL1), and acyl-coenzyme A oxidase 4 (AtACX4), also interact with the GmTRX. Together with an increased uricase activity of nodulin-35 and reduced ROS accumulation observed in the presence of GmTRX in our results, especially under heat shock and oxidative stress conditions, it appears that GmTRX represents a novel thioredoxin that is co-localized to the peroxisomes, possibly providing functional integrity to peroxisomal proteins.
PMCID: PMC4332030  PMID: 26013260
chaperone; peroxisome; thioredoxin; uricase
4.  Genome sequence of mungbean and insights into evolution within Vigna species 
Nature Communications  2014;5:5443.
Mungbean (Vigna radiata) is a fast-growing, warm-season legume crop that is primarily cultivated in developing countries of Asia. Here we construct a draft genome sequence of mungbean to facilitate genome research into the subgenus Ceratotropis, which includes several important dietary legumes in Asia, and to enable a better understanding of the evolution of leguminous species. Based on the de novo assembly of additional wild mungbean species, the divergence of what was eventually domesticated and the sampled wild mungbean species appears to have predated domestication. Moreover, the de novo assembly of a tetraploid Vigna species (V. reflexo-pilosa var. glabra) provides genomic evidence of a recent allopolyploid event. The species tree is constructed using de novo RNA-seq assemblies of 22 accessions of 18 Vigna species and protein sets of Glycine max. The present assembly of V. radiata var. radiata will facilitate genome research and accelerate molecular breeding of the subgenus Ceratotropis.
Mungbean is a fast-growing and warm-season legume crop, cultivated mainly in Asia. Here, the authors sequence the genomes of both wild and domesticated mungbean varieties and, together with detailed transcriptome data, provide insight into mungbean domestication, polyploidization and speciation.
PMCID: PMC4241982  PMID: 25384727
5.  Genome Re-Sequencing of Semi-Wild Soybean Reveals a Complex Soja Population Structure and Deep Introgression 
PLoS ONE  2014;9(9):e108479.
Semi-wild soybean is a unique type of soybean that retains both wild and domesticated characteristics, which provides an important intermediate type for understanding the evolution of the subgenus Soja population in the Glycine genus. In this study, a semi-wild soybean line (Maliaodou) and a wild line (Lanxi 1) collected from the lower Yangtze regions were deeply sequenced while nine other semi-wild lines were sequenced to a 3-fold genome coverage. Sequence analysis revealed that (1) no independent phylogenetic branch covering all 10 semi-wild lines was observed in the Soja phylogenetic tree; (2) besides two distinct subpopulations of wild and cultivated soybean in the Soja population structure, all semi-wild lines were mixed with some wild lines into a subpopulation rather than an independent one or an intermediate transition type of soybean domestication; (3) high heterozygous rates (0.19–0.49) were observed in several semi-wild lines; and (4) over 100 putative selective regions were identified by selective sweep analysis, including those related to the development of seed size. Our results suggested a hybridization origin for the semi-wild soybean, which makes a complex Soja population structure.
PMCID: PMC4181298  PMID: 25265539
6.  Variation block-based genomics method for crop plants 
BMC Genomics  2014;15:477.
In contrast with wild species, cultivated crop genomes consist of reshuffled recombination blocks, which occurred by crossing and selection processes. Accordingly, recombination block-based genomics analysis can be an effective approach for the screening of target loci for agricultural traits.
We propose the variation block method, which is a three-step process for recombination block detection and comparison. The first step is to detect variations by comparing the short-read DNA sequences of the cultivar to the reference genome of the target crop. Next, sequence blocks with variation patterns are examined and defined. The boundaries between the variation-containing sequence blocks are regarded as recombination sites. All the assumed recombination sites in the cultivar set are used to split the genomes, and the resulting sequence regions are termed variation blocks. Finally, the genomes are compared using the variation blocks. The variation block method identified recurring recombination blocks accurately and successfully represented block-level diversities in the publicly available genomes of 31 soybean and 23 rice accessions. The practicality of this approach was demonstrated by the identification of a putative locus determining soybean hilum color.
We suggest that the variation block method is an efficient genomics method for the recombination block-level comparison of crop genomes. We expect that this method will facilitate the development of crop genomics by bringing genomics technologies to the field of crop breeding.
PMCID: PMC4229737  PMID: 24929792
Comparative genomics; Recombination; Whole-genome sequencing; Soybean; Crop plants
7.  RNA Interference-Mediated Repression of S6 Kinase 1 Impairs Root Nodule Development in Soybean 
Molecules and Cells  2013;35(3):243-248.
Symbiotic nodule formation on legume roots is characterized with a series of developmental reprograming in root tissues, including extensive proliferation of cortical cells. We examined a possible involvement of the target of rapamycin (TOR) pathway, a central regulator of cell growth and proliferation in animals and yeasts, during soybean nodule development. Our results show that transcription of both GmTOR and its key downstream effector, GmS6K1, are activated during nodulation, which is paralleled with higher kinase activities of these gene products as well. RNAi-mediated knockdown of GmS6K1 impaired the nodule development with severely reduced nodule weight and numbers. In addition, expression of a few nodulins including leghemoglobin was also decreased, and consequently nitrogen fixation was found to be reduced by half. Proteomic analysis of the GmS6K1-RNAi nodules identified glutamine synthetase (GS), an essential enzyme for nitrogen assimilation in nodules, as one of the proteins that are significantly down regulated. These results appear to provide solid evidence for a functional link between GmS6K1 and nodule development.
PMCID: PMC3887909  PMID: 23475423
kinase; nodulation; RNAi; TOR
8.  Genomic differences between cultivated soybean, G. max and its wild relative G. soja 
BMC Genomics  2013;14(Suppl 1):S5.
Glycine max is an economically important crop and many different varieties of soybean exist around the world. The first draft sequences and gene models of G. max (domesticated soybean) as well as G. soja (wild soybean), both became available in 2010. This opened the door for comprehensive comparative genomics studies between the two varieties.
We have further analysed the sequences and identified the 425 genes that are unique to G. max and unavailable in G. soja. We further studied the genes with significant number of non-synonymous SNPs in their upstream regions. 12 genes involved in seed development, 3 in oil and 6 in protein concentration are unique to G. max. A significant number of unique genes are seen to overlap with the QTL regions of the three traits including seed, oil and protein. We have also developed a graphical chromosome visualizer as part of the Soybean Knowledge Base (SoyKB) tools for molecular breeding, which was used in the analysis and visualization of overlapping QTL regions for multiple traits with the deletions and SNPs in G. soja.
The comparisons between genome sequences of G. max and G. soja show significant differences between the genomic compositions of the two. The differences also highlight the phenotypic differences between the two in terms of seed development, oil and protein traits. These significant results have been integrated into the SoyKB resource and are publicly available for users to browse at
PMCID: PMC3549820  PMID: 23368680
9.  Comparative sequence analysis of nitrogen fixation-related genes in six legumes 
Legumes play an important role as food and forage crops in international agriculture especially in developing countries. Legumes have a unique biological process called nitrogen fixation (NF) by which they convert atmospheric nitrogen to ammonia. Although legume genomes have undergone polyploidization, duplication and divergence, NF-related genes, because of their essential functional role for legumes, might have remained conserved. To understand the relationship of divergence and evolutionary processes in legumes, this study analyzes orthologs and paralogs for selected 20 NF-related genes by using comparative genomic approaches in six legumes i.e., Medicago truncatula (Mt), Cicer arietinum, Lotus japonicus, Cajanus cajan (Cc), Phaseolus vulgaris (Pv), and Glycine max (Gm). Subsequently, sequence distances, numbers of synonymous substitutions per synonymous site (Ks) and non-synonymous substitutions per non-synonymous site (Ka) between orthologs and paralogs were calculated and compared across legumes. These analyses suggest the closest relationship between Gm and Cc and the highest distance between Mt and Pv in six legumes. Ks proportional plots clearly showed ancient genome duplication in all legumes, whole genome duplication event in Gm and also speciation pattern in different legumes. This study also reports some interesting observations e.g., no peak at Ks 0.4 in Gm-Gm, location of two independent genes next to each other in Mt and low Ks values for outparalogs for three genes as compared to other 12 genes. In summary, this study underlines the importance of NF-related genes and provides important insights in genome organization and evolutionary aspects of six legume species analyzed.
PMCID: PMC3749373  PMID: 23986765
nitrogen fixation; legume; comparative analysis; Ks; evolution
10.  Genome-wide mapping of NBS-LRR genes and their association with disease resistance in soybean 
BMC Plant Biology  2012;12:139.
R genes are a key component of genetic interactions between plants and biotrophic bacteria and are known to regulate resistance against bacterial invasion. The most common R proteins contain a nucleotide-binding site and a leucine-rich repeat (NBS-LRR) domain. Some NBS-LRR genes in the soybean genome have also been reported to function in disease resistance. In this study, the number of NBS-LRR genes was found to correlate with the number of disease resistance quantitative trait loci (QTL) that flank these genes in each chromosome. NBS-LRR genes co-localized with disease resistance QTL. The study also addressed the functional redundancy of disease resistance on recently duplicated regions that harbor NBS-LRR genes and NBS-LRR gene expression in the bacterial leaf pustule (BLP)-induced soybean transcriptome.
A total of 319 genes were determined to be putative NBS-LRR genes in the soybean genome. The number of NBS-LRR genes on each chromosome was highly correlated with the number of disease resistance QTL in the 2-Mb flanking regions of NBS-LRR genes. In addition, the recently duplicated regions contained duplicated NBS-LRR genes and duplicated disease resistance QTL, and possessed either an uneven or even number of NBS-LRR genes on each side. The significant difference in NBS-LRR gene expression between a resistant near-isogenic line (NIL) and a susceptible NIL after inoculation of Xanthomonas axonopodis pv. glycines supports the conjecture that NBS-LRR genes have disease resistance functions in the soybean genome.
The number of NBS-LRR genes and disease resistance QTL in the 2-Mb flanking regions of each chromosome was significantly correlated, and several recently duplicated regions that contain NBS-LRR genes harbored disease resistance QTL for both sides. In addition, NBS-LRR gene expression was significantly different between the BLP-resistant NIL and the BLP-susceptible NIL in response to bacterial infection. From these observations, NBS-LRR genes are suggested to contribute to disease resistance in soybean. Moreover, we propose models for how NBS-LRR genes were duplicated, and apply Ks values for each NBS-LRR gene cluster.
PMCID: PMC3493331  PMID: 22877146
Genome duplication; NBS-LRR; Soybean; Transcriptome analysis
11.  Tracing soybean domestication history: From nucleotide to genome 
Breeding Science  2012;61(5):445-452.
Since the genome sequences of wild species may provide key information about the genetic elements involved in speciation and domestication, the undomesticated soybean (Glycine soja Sieb. and Zucc.), a wild relative of the current cultivated soybean (G. max), was sequenced. In contrast to the current hypothesis of soybean domestication, which holds that the current cultivated soybean was domesticated from G. soja, our previous work has suggested that soybean was domesticated from the G. soja/G. max complex that diverged from a common ancestor of these two species of Glycine. In this review, many structural genomic differences between the two genomes are described and a total of 705 genes are identified as structural variations (SVs) between G. max and G. soja. After protein families database of alignments and hidden Markov models IDs and gene ontology terms were assigned, many interesting genes are discussed in detail using four domestication related traits, such as flowering time, transcriptional factors, carbon metabolism and disease resistance. Soybean domestication history is explored by studying these SVs in genes. Analysis of SVs in genes at the population-level may clarify the domestication history of soybean.
PMCID: PMC3406779  PMID: 23136484
cultivated soybean; domestication; next-generation sequencing technology; structural variations; wild soybean
12.  RNA-Seq Analysis of a Soybean Near-Isogenic Line Carrying Bacterial Leaf Pustule-Resistant and -Susceptible Alleles 
Bacterial leaf pustule (BLP) disease is caused by Xanthomonas axonopodis pv. glycines (Xag). To investigate the plant basal defence mechanisms induced in response to Xag, differential gene expression in near-isogenic lines (NILs) of BLP-susceptible and BLP-resistant soybean was analysed by RNA-Seq. Of a total of 46 367 genes that were mapped to soybean genome reference sequences, 1978 and 783 genes were found to be up- and down-regulated, respectively, in the BLP-resistant NIL relative to the BLP-susceptible NIL at 0, 6, and 12h after inoculation (hai). Clustering analysis revealed that these genes could be grouped into 10 clusters with different expression patterns. Functional annotation based on gene ontology (GO) categories was carried out. Among the putative soybean defence response genes identified (GO:0006952), 134 exhibited significant differences in expression between the BLP-resistant and -susceptible NILs. In particular, pathogen-associated molecular pattern (PAMP) and damage-associated molecular pattern (DAMP) receptors and the genes induced by these receptors were highly expressed at 0 hai in the BLP-resistant NIL. Additionally, pathogenesis-related (PR)-1 and -14 were highly expressed at 0 hai, and PR-3, -6, and -12 were highly expressed at 12 hai. There were also significant differences in the expression of the core JA-signalling components MYC2 and JASMONATE ZIM-motif. These results indicate that powerful basal defence mechanisms involved in the recognition of PAMPs or DAMPs and a high level of accumulation of defence-related gene products may contribute to BLP resistance in soybean.
PMCID: PMC3223079  PMID: 21987089
bacterial leaf pustules; disease resistance; RNA-Seq analysis; soybean
13.  The lipoxygenase gene family: a genomic fossil of shared polyploidy between Glycine max and Medicago truncatula 
BMC Plant Biology  2008;8:133.
Soybean lipoxygenases (Lxs) play important roles in plant resistance and in conferring the distinct bean flavor. Lxs comprise a multi-gene family that includes GmLx1, GmLx2 and GmLx3, and many of these genes have been characterized. We were interested in investigating the relationship between the soybean lipoxygenase isozymes from an evolutionary perspective, since soybean has undergone two rounds of polyploidy. Here we report the tetrad genome structure of soybean Lx regions produced by ancient and recent polyploidy. Also, comparative genomics with Medicago truncatula was performed to estimate Lxs in the common ancestor of soybean and Medicago.
Two Lx regions in Medicago truncatula showing synteny with soybean were analyzed. Differential evolutionary rates between soybean and Medicago were observed and the median Ks values of Mt-Mt, Gm-Mt, and Gm-Gm paralogs were determined to be 0.75, 0.62, and 0.46, respectively. Thus the comparison of Gm-Mt paralogs (Ks = 0.62) and Gm-Mt orthologs (Ks = 0.45) supports the ancient duplication of Lx regions in the common ancestor prior to the Medicago-Glycine split. After speciation, no Lx regions generated by another polyploidy were identified in Medicago. Instead tandem duplication of Lx genes was observed. On the other hand, a lineage-specific duplication occurred in soybean resulting in two pairs of Lx regions. Each pair of soybean regions was co-orthologous to one Lx region in Medicago. A total of 34 Lx genes (15 MtLxs and 19 GmLxs) were divided into two groups by phylogenetic analysis. Our study shows that the Lx gene family evolved from two distinct Lx genes in the most recent common ancestor.
This study analyzed two pairs of Lx regions generated by two rounds of polyploidy in soybean. Each pair of soybean homeologous regions is co-orthologous to one region of Medicago, demonstrating the quartet structure of the soybean genome. Differential evolutionary rates between soybean and Medicago were observed; thus optimized rates of Ks per year should be applied for accurate estimation of coalescence times to each case of comparison: soybean-soybean, soybean-Medicago, or Medicago-Medicago. In conclusion, the soybean Lx gene family expanded by ancient polyploidy prior to taxon divergence, followed by a soybean- specific duplication and tandem duplications, respectively.
PMCID: PMC2644698  PMID: 19105811
14.  Three-level anterior cervical discectomy and fusion in elderly patients with wedge shaped tricortical autologous graft: A consecutive prospective series 
Indian Journal of Orthopaedics  2008;42(4):460-465.
Treatment of multilevel cervical spondylotic myelopathy/radiculopathy is a matter of debate, more so in elderly patients due to compromised physiology. We evaluated the clinical and radiological results of cervical fusion, using wedge-shaped tricortical autologous iliac graft and Orion plate for three-level anterior cervical discectomy in elderly patients.
Materials and Methods:
Twelve elderly patients with mean age of 69.7 years (65–76 years) were treated between April 2000 and March 2005, for three-level anterior cervical discectomy and fusion, using wedge-shaped tricortical autologous iliac graft and Orion plate. Outcome was recorded clinically according to Odom's criteria and radiologically in terms of correction of lordosis angle and intervertebral disc height span at the time of bony union. The mean follow-up was 29.8 months (12–58 months).
All the patients had a complete recovery of clinical symptoms after surgery. Postoperative score according to Odom's criteria was excellent in six patients and good in remaining six. Bony union was achieved in all the patients with average union time of 12 weeks (8–20 weeks). The mean of sum of three segment graft height collapse was 2.50 mm (SD = 2.47). The average angle of lordosis was corrected from 18.2° (SD = 2.59°) preoperatively to 24.9° (SD = 4.54°) at the final follow-up. This improvement in the radiological findings is statistically significant (P < 0.05).
Cervical fusion with wedge-shaped tricortical autologous iliac graft and Orion plate for three-level anterior cervical discectomy is an acceptable technique in elderly patients. It gives satisfactory results in terms of clinical outcome, predictable early solid bony union, and maintenance of disc space height along with restoration of cervical lordosis.
PMCID: PMC2740358  PMID: 19753236
Anterior discectomy; elderly patients; plating; three-level cervical spine disease; wedge-shaped autograft
15.  Sequence Level Analysis of Recently Duplicated Regions in Soybean [Glycine max (L.) Merr.] Genome 
A single recessive gene, rxp, on linkage group (LG) D2 controls bacterial leaf-pustule resistance in soybean. We identified two homoeologous contigs (GmA and GmA′) composed of five bacterial artificial chromosomes (BACs) during the selection of BAC clones around Rxp region. With the recombinant inbred line population from the cross of Pureunkong and Jinpumkong 2, single-nucleotide polymorphism and simple sequence repeat marker genotyping were able to locate GmA′ on LG A1. On the basis of information in the Soybean Breeders Toolbox and our results, parts of LG A1 and LG D2 share duplicated regions. Alignment and annotation revealed that many homoeologous regions contained kinases and proteins related to signal transduction pathway. Interestingly, inserted sequences from GmA and GmA′ had homology with transposase and integrase. Estimation of evolutionary events revealed that speciation of soybean from Medicago and the recent divergence of two soybean homoeologous regions occurred at 60 and 12 million years ago, respectively. Distribution of synonymous substitution patterns, Ks, yielded a first secondary peak (mode Ks = 0.10–0.15) followed by two smaller bulges were displayed between soybean homologous regions. Thus, diploidized paleopolyploidy of soybean genome was again supported by our study.
PMCID: PMC2650623  PMID: 18334514
BAC; divergence time; duplication; Ks; Rxp; soybean

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