Publications by authors named "Won Kyong Cho"

83 Publications

Transcriptome Assembly of Two Fern Species Identifies Enzymes Required for Two Upstream Pathways of Phytoecdysteroids.

Int J Mol Sci 2021 Feb 19;22(4). Epub 2021 Feb 19.

Department of Integrative Biotechnology, Sungkyunkwan University, Suwon 16419, Korea.

species produce a high amount of phytoecdysteroids (PEs), which are widely used in traditional medicine in the Pacific islands. The PEs in two different species, (MP) and (MS), were examined using high-performance liquid chromatography (HPLC). In particular, MS produces a high amount of 20-hydroxyecdysone, which is the main active compound in PEs. To identify genes for PE biosynthesis, we generated reference transcriptomes from sterile frond tissues using the NovaSeq 6000 system. De novo transcriptome assembly after deleting contaminants resulted in 57,252 and 54,618 clean transcripts for MP and MS, respectively. The clean transcripts for each species were annotated according to gene ontology terms, UniProt pathways, and the clusters of the orthologous group protein database using the MEGAN6 and Sma3s programs. In total, 1852 and 1980 transcription factors were identified for MP and MS, respectively. We obtained transcripts encoding for 38 and 32 enzymes for MP and MS, respectively, potentially involved in mevalonate and sterol biosynthetic pathways, which produce precursors for PE biosynthesis. Phylogenetic analyses revealed many redundant and unique enzymes between the two species. Overall, this study provides two reference transcriptomes that might be useful for further studies regarding PE biosynthesis in species.
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http://dx.doi.org/10.3390/ijms22042085DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7923240PMC
February 2021

Analysis of the transcriptomic, metabolomic, and gene regulatory responses to Puccinia sorghi in maize.

Mol Plant Pathol 2021 Apr 28;22(4):465-479. Epub 2021 Feb 28.

Department of Entomology and Plant Pathology, NC State University, Raleigh, North Carolina, USA.

Common rust, caused by Puccinia sorghi, is a widespread and destructive disease of maize. The Rp1-D gene confers resistance to the P. sorghi IN2 isolate, mediating a hypersensitive cell death response (HR). To identify differentially expressed genes (DEGs) and metabolites associated with the compatible (susceptible) interaction and with Rp1-D-mediated resistance in maize, we performed transcriptomics and targeted metabolome analyses of P. sorghi IN2-infected leaves from the near-isogenic lines H95 and H95:Rp1-D, which differed for the presence of Rp1-D. We observed up-regulation of genes involved in the defence response and secondary metabolism, including the phenylpropanoid, flavonoid, and terpenoid pathways. Metabolome analyses confirmed that intermediates from several transcriptionally up-regulated pathways accumulated during the defence response. We identified a common response in H95:Rp1-D and H95 with an additional H95:Rp1-D-specific resistance response observed at early time points at both transcriptional and metabolic levels. To better understand the mechanisms underlying Rp1-D-mediated resistance, we inferred gene regulatory networks occurring in response to P. sorghi infection. A number of transcription factors including WRKY53, BHLH124, NKD1, BZIP84, and MYB100 were identified as potentially important signalling hubs in the resistance-specific response. Overall, this study provides a novel and multifaceted understanding of the maize susceptible and resistance-specific responses to P. sorghi.
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http://dx.doi.org/10.1111/mpp.13040DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7938627PMC
April 2021

Transcriptome Profiling of Human Follicle Dermal Papilla Cells in response to Porphyra-334 Treatment by RNA-Seq.

Evid Based Complement Alternat Med 2021 13;2021:6637513. Epub 2021 Jan 13.

Anti-aging Research Institute of BIO-FD&C Co., Ltd., Incheon 21990, Republic of Korea.

Porphyra-334 is a kind of mycosporine-like amino acid absorbing ultraviolet-A. Here, we characterized porphyra-334 as a potential antiaging agent. An assay revealed that porphyra-334 dramatically promoted collagen synthesis in fibroblast cells. The effect of porphyra-334 on cell proliferation was dependent on the cell type, and the increase of cell viability by porphyra-334 was the highest in keratinocyte cells among the three tested cell types. An clinical test with 22 participants demonstrated the possible role of porphyra-334 in the improvement of periorbital wrinkles. RNA-sequencing using human follicle dermal papilla (HFDP) cells upon porphyra-334 treatment identified the upregulation of metallothionein- (MT-) associated genes, confirming the antioxidant role of porphyra-334 with MT. Moreover, the expression of genes involved in nuclear chromosome segregation and the encoding of components of kinetochores was upregulated by porphyra-334 treatment. Furthermore, we found that several genes associated with the hair follicle cycle, the hair follicle structure, the epidermal structure, and stem cells were upregulated by porphyra-334 treatment, suggesting the potential role of porphyra-334 in hair follicle growth and maintenance. In summary, we provided several new pieces of evidence of porphyra-334 as a potential antiaging cosmetic agent and elucidated the expression network in HFDP cells upon porphyra-334.
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http://dx.doi.org/10.1155/2021/6637513DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7817261PMC
January 2021

Gene expression profile of human follicle dermal papilla cells in response to Camellia japonica phytoplacenta extract.

FEBS Open Bio 2021 Mar 14;11(3):633-651. Epub 2021 Feb 14.

Anti-aging Research Institute of BIO-FD&C Co., Ltd., Incheon, Korea.

Camellia japonica L. is a flowering tree with several medicinal and cosmetic applications. Here, we investigated the efficacy of C. japonica placenta extract (CJPE) as a potential therapeutic agent for promotion of hair growth and scalp health by using various in vitro and in vivo assays. Moreover, we performed transcriptome analysis to examine the relative expression of human follicle dermal papilla cells (HFDPC) in response to CJPE by RNA-sequencing (RNA-seq). In vitro assays revealed upregulation of the expression of hair growth marker genes in HFDPC after CJPE treatment. Moreover, in vivo clinical tests with 42 adult female participants showed that a solution containing 0.5% CJPE increased the moisture content of the scalp and decreased the scalp's sebum content, dead scalp keratin, and erythema. Furthermore, RNA-seq analysis revealed key genes in HFDPC which are associated with CJPE. Interestingly, genes associated with lipid metabolism and cholesterol efflux were upregulated. Genes upregulated by CJPE are associated with several hormones, including parathyroid, adrenocorticotropic hormone, α-melanocyte-stimulating hormone (alpha-MSH), and norepinephrine, which are involved in hair follicle biology. Furthermore, some upregulated genes are associated with the regulation of axon guidance. In contrast, many genes downregulated by CJPE are associated with structural components of the cytoskeleton. In addition, CJPE suppressed genes associated with muscle structure and development. Taken together, this study provides extensive evidence that CJPE may have potential as a therapeutic agent for scalp treatment and hair growth promotion.
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http://dx.doi.org/10.1002/2211-5463.13076DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7931240PMC
March 2021

Soybean Viromes in the Republic of Korea Revealed by RT-PCR and Next-Generation Sequencing.

Microorganisms 2020 Nov 12;8(11). Epub 2020 Nov 12.

Research Institute of Agriculture and Life Sciences, College of Agriculture and Life Sciences, Seoul National University, Seoul 08826, Korea.

Soybean ( L.) is one of the most important crop plants in the Republic of Korea. Here, we conducted a soybean virome study. We harvested a total of 172 soybean leaf samples showing disease symptoms from major soybean-growing regions in the Republic of Korea. Individual samples were examined for virus infection by RT-PCR. Moreover, we generated eight libraries representing eight provinces by pooling samples and four libraries from single samples. RNA-seq followed by bioinformatics analyses revealed 10 different RNA viruses infecting soybean. The proportion of viral reads in each transcriptome ranged from 0.2 to 31.7%. Coinfection of different viruses in soybean plants was very common. There was a single dominant virus in each province, and this geographical difference might be related to the soybean seeds that transmit viruses. In this study, 32 viral genome sequences were assembled and successfully used to analyze the phylogenetic relationships and quasispecies nature of the identified RNA viruses. Moreover, RT-PCR with newly developed primers confirmed infection of the identified viruses in each library. Taken together, our soybean virome study provides a comprehensive overview of viruses infecting soybean in eight geographical regions in the Republic of Korea and four single soybean plants in detail.
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http://dx.doi.org/10.3390/microorganisms8111777DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7698195PMC
November 2020

First report of Cherry virus F infecting Japanese plum in Korea.

Plant Dis 2020 Nov 3. Epub 2020 Nov 3.

Seoul National University, Department of Agricultural Biotechnology, 5103-ho, 200-dong, Daehak-dong, Kwanak-gu, Seoul, Korea (the Republic of), 08826;

Cherry virus F (CVF) is a tentative member of the genus Fabavirus in the family Secoviridae, consisting of two RNA segments (Koloniuk et al. 2018). To date, CVF has been documented in only sweet cherry (Prunus avium) in the Czech Republic (Koloniuk et al. 2018), Canada, and Greece. In May 2014, we collected leaf samples from four symptomatic (leaf spots and dapple fruits) and two asymptomatic Japanese plum cultivars (Sun and Gadam) grown in an orchard in Hoengseong, South Korea, to identify viruses and viroids infecting plum trees. Total RNA from individual plum trees was extracted using two commercial kits: Fruit-mate for RNA Purification Kit (Takara, Shiga, Japan) and RNeasy Plant Mini Kit (Qiagen, Hilden, Germany). We generated six mRNA libraries from the six different plum cultivars for RNA-sequencing using the TruSeq RNA Library Preparation Kit v2 (Illumina, CA, U.S.A.) as described previously (Jo et al. 2017). The mRNA libraries were paired-end (2 X 100 bp) sequenced with a HiSeq 2000 system (Macrogen, Seoul, Korea). The raw sequence reads were de novo assembled by Trinity program v. 2.8.6, with default parameters (Haas et al. 2013). The assembled contigs were subjected to BLASTX search against the non-redundant protein database in NCBI. Of the two asymptomatic cultivars, the transcriptome of asymptomatic plum cv. Gadam contained five contigs specific to CVF. Two and three contigs were specific to CVF RNA1 (2,571 reads, coverage 42.15%) and RNA2 (2,025 reads, coverage 53.04%), respectively. The size of these five contigs ranged from 241 to 5,986 bp. Contigs of 5,986 and 3,867 bp in length, referred to as CVF isolate Gadam RNA1 (GenBank MN896996) and RNA2 (GenBank MN896995), respectively, were subjected to BLASTP search against NCBI's non-redundant protein database. The results showed that the polyprotein sequences of RNA1 and RNA2 shared 95.3% and 93.11% amino acid identities with isolates SwC-H_1a from the Czech Republic (GenBank acc. no. AWB36326) and Stac-3B_c8 from Canada (AZZ10055), respectively. To confirm the infection of CVF in cv. Gadam, RT-PCR was conducted using CVF RNA1-specific primers designed based on the CVF reference genome sequences (MH998210 and MH998216), including 5'-CCACCAAATAGGCAAGAGGTCAC-3' (position 3190-3212) and 5'-CACAATCACCATCAATGGTCTCTGC-3' (position 3742-3766), and CVF RNA2-specific primers, including 5'-CTGCTTTATGATGCTAGACATCAAGATG-3' (position 1015-1042) and 5'-ACAATAGGCATGCTCATCTCAACCTC-3' (position 1594-1619). We amplified 577-bp RNA1-specific and 605-bp RNA2-specific amplicons that were cloned and then performed Sanger sequencing. Sequencing of the cloned amplicons for isolate Gadam RNA1 (GenBank MN896993) and RNA2 (GenBank MN896994) revealed values of 99.48% and 99.17% nucleotide identity to that of RNA1 and RNA2 determined by high-throughput sequencing, respectively. Additionally, we tested five plants for each of the six plum cultivars grown in the same orchard. The detection of CVF was carried out through PCR using the primers and protocol described above. Of the 30 trees, CVF was detected in three trees of cv. Gadam by both primer pairs. To our knowledge, this is the first report of CVF infecting Japanese plum and the first report of the virus in Korea. However, its prevalence in other Prunus species, including apricot, European plum, and peach, should be further elucidated.
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http://dx.doi.org/10.1094/PDIS-08-20-1725-PDNDOI Listing
November 2020

Identification of Viruses and Viroids Infecting Tomato and Pepper Plants in Vietnam by Metatranscriptomics.

Int J Mol Sci 2020 Oct 13;21(20). Epub 2020 Oct 13.

Research Institute of Agriculture and Life Sciences, Seoul National University, Seoul 08826, Korea.

Tomato ( L.) and pepper ( L.) plants belonging to the family are cultivated worldwide. The rapid development of next-generation sequencing (NGS) technology facilitates the identification of viruses and viroids infecting plants. In this study, we carried out metatranscriptomics using RNA sequencing followed by bioinformatics analyses to identify viruses and viroids infecting tomato and pepper plants in Vietnam. We prepared a total of 16 libraries, including eight tomato and eight pepper libraries derived from different geographical regions in Vietnam. We identified a total of 602 virus-associated contigs, which were assigned to 18 different virus species belonging to nine different viral genera. We identified 13 different viruses and two viroids infecting tomato plants and 12 viruses and two viroids infecting pepper plants with viruses as dominantly observed pathogens. Our results showed that multiple infection of different viral pathogens was common in both plants. Moreover, geographical region and host plant were two major factors to determine viral populations. Taken together, our results provide the comprehensive overview of viral pathogens infecting two important plants in the family grown in Vietnam.
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http://dx.doi.org/10.3390/ijms21207565DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7593927PMC
October 2020

Comparative Microbiome Study of Mummified Peach Fruits by Metagenomics and Metatranscriptomics.

Plants (Basel) 2020 Aug 18;9(8). Epub 2020 Aug 18.

Research Institute of Agriculture and Life Sciences, College of Agriculture and Life Sciences, Seoul National University, Seoul 08826, Korea.

The dried peach fruits clinging to peach trees or lying on the ground nearby are known as mummified peach fruits. Here, we examined the microbiome communities of three different mummified peach fruits from the nectarine cultivar "Hahong" by DNA- and RNA-sequencing. We found the dominance of followed by , , and in the mummified peach fruits. Moreover, we found a high number of Proteobacteria, including , , , and . Furthermore, we identified several viruses and viroids. Bacteriophages were identified by DNA- and RNA-sequencing, while viruses and viroids with RNA genomes were identified by only RNA-sequencing. Moreover, we identified a novel mycovirus referred to as umbra-like virus 1 (MULV1) from . Our results revealed the co-inhabitance of fungi and bacteria in the mummified peach fruits, although dominant microorganisms were present. RNA-sequencing revealed that several fungal and bacterial genes were actively transcribed. Comparative analyses suggested that RNA-sequencing provides more detailed information on microbial communities; however, combining DNA- and RNA-sequencing results increased the diversity of microorganisms, suggesting the importance of databases and analysis tools for microbiome studies. Taken together, our study provides a comprehensive overview of microbial communities in mummified peach fruits by DNA shotgun sequencing and RNA-sequencing.
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http://dx.doi.org/10.3390/plants9081052DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7464454PMC
August 2020

Identification of viruses infecting six plum cultivars in Korea by RNA-sequencing.

PeerJ 2020 29;8:e9588. Epub 2020 Jul 29.

Research Institute of Agriculture and Life Sciences, College of Agriculture and Life Sciences, Seoul National University, Seoul, Republic of Korea.

Background: Plums are a kind of stone fruit, a category that includes peaches, cherries, apricots, and almonds. In Korea, Japanese plum trees are usually cultivated as they best suit the climate. To date, there have been few studies in Korea on viruses infecting plum trees compared to those infecting peach trees.

Methods: To identify viruses and viroids infecting plum trees, we collected leaf samples from six different plum cultivars and subjected them to RNA-sequencing (RNA-seq). Six different plum transcriptomes were de novo assembled using the Trinity assembler followed by BLAST searching against a viral reference database.

Results: We identified hop stunt viroid (HSVd) and six viruses, including apple chlorotic leaf spot virus (ACLSV), little cherry virus-1 (LChV-1), peach virus D (PeVD), peach leaf pitting-associated virus (PLPaV), plum bark necrosis stem pitting-associated virus (PBNSPaV), and prunus necrotic ringspot virus (PNRSV), from six plum cultivars by RNA-seq. RT-PCR confirmed the infection of HSVd and three viruses-ACLSV, PBNSPaV, and PNRSV-in plum trees. However, RT-PCR demonstrated that plum trees in this study were not infected by LChV-1, PeVD, or PLPaV. It is likely that the three viruses LChV-1, PeVD, and PLPaV as identified by RNA-seq were contaminants from other peach libraries caused by index misassignment, which suggests that careful confirmation by other methods should be carried out in next-generation sequencing (NGS)-based virus identification. Taken together, we identified a viroid and three viruses infecting plum trees in Korea.
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http://dx.doi.org/10.7717/peerj.9588DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7395596PMC
July 2020

Anti-Aging Effects of (Edelweiss) Callus Culture Extract Through Transcriptome Profiling.

Genes (Basel) 2020 02 21;11(2). Epub 2020 Feb 21.

Anti-Aging Research Institute of BIO-FD&C Co., Ltd., Incheon 21990, Korea.

Edelweiss () in the family is a wildflower that grows in rocky limestone places. Here, we investigated the efficacy of edelweiss callus culture extract ( callus culture extract; LACCE) using multiple assays from to as well as transcriptome profiling. Several assay results showed the strong antioxidant activity of LACCE in response to UVB treatment. Moreover, LACCE suppressed inflammation and wrinkling; however, moisturizing activity was increased by LACCE. The clinical test demonstrated that constant application of LACCE on the face and skin tissues improved anti-periorbital wrinkles, skin elasticity, dermal density, and skin thickness compared with the placebo. The RNA-Sequencing results showed at least 16.56% of human genes were expressed in keratinocyte cells. LACCE up-regulated genes encoding several KRT proteins; DDIT4, BNIP3, and IGFBP3 were involved in the positive regulation of the developmental process, programmed cell death, keratinization, and cornification forming skin barriers, which provide many advantages in the human skin. By contrast, down-regulated genes were stress-responsive genes, including metal, oxidation, wounding, hypoxia, and virus infection, suggesting LACCE did not cause any harmful stress on the skin. Our comprehensive study demonstrated LACCE is a promising agent for anti-aging cosmetics.
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http://dx.doi.org/10.3390/genes11020230DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7074254PMC
February 2020

Sweet potato viromes in eight different geographical regions in Korea and two different cultivars.

Sci Rep 2020 02 13;10(1):2588. Epub 2020 Feb 13.

Research Institute of Agriculture and Life Sciences, College of Agriculture and Life Sciences, Seoul National University, Seoul, 08826, Republic of Korea.

The sweet potato in the family Convolvulaceae is a dicotyledonous perennial plant. Here, we conducted a comprehensive sweet potato virome study using 10 different libraries from eight regions in Korea and two different sweet potato cultivars by RNA-Sequencing. Comprehensive bioinformatics analyses revealed 10 different virus species infecting sweet potato. Moreover, we identified two novel viruses infecting sweet potato referred to as Sweet potato virus E (SPVE) in the genus Potyvirus and Sweet potato virus F (SPVF) in the genus Carlavirus. Of the identified viruses, Sweet potato feathery mottle virus (SPFMV) was the dominant virus followed by Sweet potato virus C (SPVC) and SPVE in Korea. We obtained a total of 30 viral genomes for eight viruses. Our phylogenetic analyses showed many potyvirus isolates are highly correlated with geographical regions. However, two isolates of SPFMV and a single isolate of Sweet potato virus G (SPVG) were genetically distant from other known isolates. The mutation rate was the highest in SPFMV followed by SPVC and SPVG. Two different sweet potato cultivars, Beni Haruka and Hogammi, were infected by seven and five viruses, respectively. Taken together, we provide a complete list of viruses infecting sweet potato in Korea and diagnostic methods.
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http://dx.doi.org/10.1038/s41598-020-59518-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7018812PMC
February 2020

Genome-wide identification of long non-coding RNAs in tomato plants irradiated by neutrons followed by infection with .

PeerJ 2019 28;7:e6286. Epub 2019 Jan 28.

Department of Physics, Sungkyunkwan University, Suwon, South Korea.

Long non-coding RNAs (lncRNAs) play an important role in regulating many biological processes. In this study, tomato seeds were first irradiated by neutrons. Eight tomato mutants were then selected and infected by (TYLCV). RNA sequencing followed by bioinformatics analyses identified 1,563 tomato lncRNAs. About half of the lncRNAs were derived from intergenic regions, whereas antisense lncRNAs accounted for 35%. There were fewer lncRNAs identified in our study than in other studies identifying tomato lncRNAs. Functional classification of 794 lncRNAs associated with tomato genes showed that many lncRNAs were associated with binding functions required for interactions with other molecules and localized in the cytosol and membrane. In addition, we identified 19 up-regulated and 11 down-regulated tomato lncRNAs by comparing TYLCV infected plants to non-infected plants using previously published data. Based on these results, the lncRNAs identified in this study provide important resources for characterization of tomato lncRNAs in response to TYLCV infection.
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http://dx.doi.org/10.7717/peerj.6286DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6354667PMC
January 2019

Transcriptome profiles of tomato plants after neutron irradiation and infection with TYLCV.

Physiol Plant 2019 Feb;165(2):427-441

Department of Physics, Sungkyunkwan University, Suwon 16419, Republic of Korea.

Ionizing radiation is ubiquitous in the environment and can cause mutagenesis in living organisms. In this study, we examined the effects of neutron irradiation on tomato plants. Neutron irradiation decreased tomato germination rates, but most irradiated tomato plants did not show any significant phenotype. However, tomato mutants infected by Tomato yellow leaf curl virus (TYLCV) displayed resistance against TYLCV compared to the wild type (WT), which showed disease symptoms. RNA-Seq data demonstrated that the expression profiles of eight tomato mutants were significantly different from that of the WT. The transcriptomes obtained from presoaked seeds were highly altered compared to those of dry seeds. Increased irradiation time resulted in severe changes in the tomato transcriptome; however, different neutron irradiation intensities affected the expressions of different sets of genes. A high number of single-nucleotide polymorphisms in tomato transcriptomes suggest that neutron irradiation strongly impacts plant transcriptomes. The transition/transversion values among mutants were almost constant and were lower than that of the non-irradiated sample (WT), suggesting that neutron irradiation caused an effect. Taken together, this is the first report showing the effects of neutron irradiation on tomato plants by transcriptome analyses.
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http://dx.doi.org/10.1111/ppl.12913DOI Listing
February 2019

RNA viromes of the oriental hybrid lily cultivar "Sorbonne".

BMC Genomics 2018 Oct 13;19(1):748. Epub 2018 Oct 13.

Research Institute of Agriculture and Life Sciences, College of Agriculture and Life Sciences, Seoul National University, Seoul, 08826, Republic of Korea.

Background: The lily is a perennial flowering plant belonging to the genus Lilium in the family Liliaceae. Most cultivated lily plants are propagated by bulbs. Therefore, numerous lily bulbs are frequently infected by diverse viruses causing viral diseases. To date, no study has examined the viromes of plants of one type with identical genetic backgrounds collected from different geographical regions.

Results: Here, we examined different viromes of the lily cultivar "Sorbonne" using 172 gigabytes of transcriptome data composed of 23 libraries from four different projects for the cultivar "Sorbonne." We identified 396 virus-associated contigs from all but one library. We identified six different viruses, including Plantago asiatica mosaic virus (PlAMV), Cucumber mosaic virus (CMV), Lily symptomless virus (LSV), Tulip virus X (TVX), Lily mottle virus (LMoV), and Tobacco rattle virus (TRV). Of them, PlAMV was the most common virus infecting the lily. Scale and flower samples possessed a high number of virus-associated reads. We assembled 32 nearly complete genomes for the six identified viruses possessing the polyadenylate tails. Genomes of all six viruses were highly conserved in the lily cultivar "Sorbonne" based on mutation analysis. We identified defective RNAs from LSV, TVX, and PlAMV localized in the triple gene block region. Phylogenetic analyses showed that virus genomes are highly correlated with geographical regions and host plants.

Conclusions: We conducted comprehensive virome analyses of a single lily cultivar, "Sorbonne," using transcriptome data. Our results shed light on an array of lily virome-associated topics, including virus identification, the dominant virus, virus accumulation in different plant tissues, virus genome assembly, virus mutation, identification of defective RNAs, and phylogenetic relationships of identified viruses. Taken together, we provide very useful methods and valuable results that can be applied in other virome-associated studies.
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http://dx.doi.org/10.1186/s12864-018-5138-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6186116PMC
October 2018

Barley RNA viromes in six different geographical regions in Korea.

Sci Rep 2018 09 5;8(1):13237. Epub 2018 Sep 5.

Research Institute of Agriculture and Life Sciences, College of Agriculture and Life Sciences, Seoul National University, Seoul, 08826, Republic of Korea.

Barley is a kind of cereal grass belonging to the family Poaceae. To examine viruses infecting winter barley in Korea, we carried out a comprehensive study of barley RNA viromes using next-generation sequencing (NGS). A total of 110 barley leaf samples from 17 geographical locations were collected. NGS followed by extensive bioinformatics analyses revealed six different barley viromes: Barley yellow mosaic virus (BaYMV), Barley mild mosaic virus (BaMMV), Barley yellow dwarf virus (BYDV), Hordeum vulgare endornavirus (HvEV), and Barley virus G (BVG). BaYMV and HvEV were identified in all libraries, while other viruses were identified in some specific library. Based on the number of virus-associated reads, BaYMV was a dominant virus infecting winter barley in Korea causing yellow disease symptoms. We obtained nearly complete genomes of six BaYMV isolates and two BaMMV isolates. Phylogenetic analyses indicate that BaYMV and BaMMV were largely grouped based on geographical regions such as Asia and Europe. Single nucleotide polymorphisms analyses suggested that most BaYMV and BaMMV showed strong genetic variations; however, BaYMV isolate Jeonju and BaMMV isolate Gunsan exhibited a few and no SNPs, respectively, suggesting low level of genetic variation. Taken together, this is the first study of barley RNA viromes in Korea.
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http://dx.doi.org/10.1038/s41598-018-31671-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6125401PMC
September 2018

Identification of viral domains integrated into Arabidopsis proteome.

Mol Phylogenet Evol 2018 11 17;128:246-257. Epub 2018 Aug 17.

Research Institute of Agriculture and Life Sciences, College of Agriculture and Life Sciences, Seoul National University, Seoul 08826, Republic of Korea; The Taejin Genome Institute, Gadam-gil 61, Hoeongseong 25239, Republic of Korea. Electronic address:

Horizontal gene transfer (HGT) contributes to the genome evolution of living organisms. In particular, several recent studies provide convincing data on the integration of viral sequences into diverse organisms. Here, we identified 101 viral domains integrated into the model plant Arabidopsis proteome. Functional analysis based on gene ontology (GO) terms indicates that viral domains in the Arabidopsis proteome were involved in various stress responses with binding functions. Protein interaction networks support the strong protein interactions of viral domains with other Arabidopsis proteins. A proteome-wide analysis gave a comprehensive evolutionary view of viral domains integrated into 41 plant proteomes, revealing the specific and conserved integration of viral domains into plant proteomes. Phylogenetic analyses revealed the possible HGT between viral domains and plant proteomes. Our results provide an overview of the integration of viral domains into plant proteomes and their possible functional roles associated with plant defense mechanisms.
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http://dx.doi.org/10.1016/j.ympev.2018.08.009DOI Listing
November 2018

Probiotic Expressing a Nucleic Acid-Hydrolyzing Minibody (3D8 Scfv) Enhances Probiotic Activities in Mice Intestine as Revealed by Metagenomic Analyses.

Genes (Basel) 2018 May 29;9(6). Epub 2018 May 29.

Department of Genetic Engineering, Sungkyunkwan University, 2066, Seobu-ro, Jangan-gu, Suwon 16419, Korea.

Probiotics are well known for their beneficial effects for animals, including humans and livestock. Here, we tested the probiotic activity of expressing 3D8 scFv, a nucleic acid-hydrolyzing mini-antibody, in mice intestine. A total of 18 fecal samples derived from three different conditions at two different time points were subjected to high-throughput 16S ribosomal RNA (rRNA) metagenomic analyses. Bioinformatic analyses identified an average of 290 operational taxonomic units. After administration of , populations of the probiotics , , and increased, whereas the population of harmful bacteria such as species decreased. Furthermore, continuous administration of resulted in emerging as the dominant probiotic after competition with other existing probiotics. Expression of 3D8 scFv protein specifically increased the population of , which is another probiotic. In summary, our results showed that expressing 3D8 scFv protein enhanced probiotic activity in mice intestine with no observable side effects. Thus, the system developed in this study may be a good tool for the expression of recombinant protein using probiotics.
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http://dx.doi.org/10.3390/genes9060276DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6027128PMC
May 2018

Differential Contribution of RNA Interference Components in Response to Distinct Fusarium graminearum Virus Infections.

J Virol 2018 05 13;92(9). Epub 2018 Apr 13.

Department of Agricultural Biotechnology and Center for Fungal Pathogenesis, Seoul National University, Seoul, Republic of Korea

The mechanisms of RNA interference (RNAi) as a defense response against viruses remain unclear in many plant-pathogenic fungi. In this study, we used reverse genetics and virus-derived small RNA profiling to investigate the contributions of RNAi components to the antiviral response against Fusarium graminearum viruses 1 to 3 (FgV1, -2, and -3). Real-time reverse transcription-quantitative PCR (qRT-PCR) indicated that infection of by FgV1, -2, or -3 differentially induces the gene expression of RNAi components in Transcripts of the and genes of ( and ) accumulated at lower levels following FgV1 infection than following FgV2 or FgV3 infection. We constructed gene disruption and overexpression mutants for each of the Argonaute and dicer genes and for two RNA-dependent RNA polymerase (RdRP) genes and generated virus-infected strains of each mutant. Interestingly, mycelial growth was significantly faster for the FgV1-infected overexpression mutant than for the FgV1-infected wild type, while neither FgV2 nor FgV3 infection altered the colony morphology of the gene deletion and overexpression mutants. FgV1 RNA accumulation was significantly decreased in the overexpression mutant. Furthermore, the levels of induction of , , and some of the genes caused by FgV2 and FgV3 infection were similar to those caused by hairpin RNA-induced gene silencing. Using small RNA sequencing analysis, we documented different patterns of virus-derived small interfering RNA (vsiRNA) production in strains infected with FgV1, -2, and -3. Our results suggest that the Argonaute protein encoded by is required for RNAi in , that induction differs in response to FgV1, -2, and -3, and that might contribute to the accumulation of vsiRNAs in FgV1-infected To increase our understanding of how RNAi components in react to mycovirus infections, we characterized the role(s) of RNAi components involved in the antiviral defense response against Fusarium graminearum viruses (FgVs). We observed differences in the levels of induction of RNA silencing-related genes, including and , in response to infection by three different FgVs. can efficiently induce a robust RNAi response against FgV1 infection, but genes might be relatively redundant to with respect to antiviral defense. However, the contribution of this gene in the response to the other FgV infections might be small. Compared to previous studies of , which showed dicer-like protein 2 and Argonaute-like protein 2 to be important in antiviral RNA silencing, our results showed that developed a more complex and robust RNA silencing system against mycoviruses and that FgDICER-1 and FgDICER-2 and FgAGO-1 and FgAGO-2 had redundant roles in antiviral RNA silencing.
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http://dx.doi.org/10.1128/JVI.01756-17DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5899199PMC
May 2018

Peach RNA viromes in six different peach cultivars.

Sci Rep 2018 01 30;8(1):1844. Epub 2018 Jan 30.

Research Institute of Agriculture and Life Sciences, College of Agriculture and Life Sciences, Seoul National University, Seoul, 08826, Republic of Korea.

Many recent studies have demonstrated that several known and unknown viruses infect many horticultural plants. However, the elucidation of a viral population and the understanding of the genetic complexity of viral genomes in a single plant are rarely reported. Here, we conducted metatranscriptome analyses using six different peach trees representing six individual peach cultivars. We identified six viruses including five viruses in the family Betaflexiviridae and a novel virus belonging to the family Tymoviridae as well as two viroids. The number of identified viruses and viroids in each transcriptome ranged from one to six. We obtained 18 complete or nearly complete genomes for six viruses and two viroids using transcriptome data. Furthermore, we analyzed single nucleotide variations for individual viral genomes. In addition, we analyzed the amount of viral RNA and copy number for identified viruses and viroids. Some viruses or viroids were commonly present in different cultivars; however, the list of infected viruses and viroids in each cultivar was different. Taken together, our study reveals the viral population in a single peach tree and a comprehensive overview for the diversities of viral communities in different peach cultivars.
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http://dx.doi.org/10.1038/s41598-018-20256-wDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5789896PMC
January 2018

Genome Assembly and Single Nucleotide Variations for Soybean Mosaic Virus Using Soybean Seed Transcriptome Data.

Plant Pathol J 2017 Oct 1;33(5):478-487. Epub 2017 Oct 1.

Department of Agricultural Biotechnology, Research Institute of Agriculture and Life Sciences, and Plant Genomics and Breeding Institute, College of Agriculture and Life Sciences, Seoul National University, Seoul 08826, Korea.

Soybean is the most important legume crop in the world. Several diseases in soybean lead to serious yield losses in major soybean-producing countries. Moreover, soybean can be infected by diverse viruses. Recently, we carried out a large-scale screening to identify viruses infecting soybean using available soybean transcriptome data. Of the screened transcriptomes, a soybean transcriptome for soybean seed development analysis contains several virus-associated sequences. In this study, we identified five viruses, including soybean mosaic virus (SMV), infecting soybean by transcriptome assembly followed by blast search. We assembled a nearly complete consensus genome sequence of SMV China using transcriptome data. Based on phylogenetic analysis, the consensus genome sequence of SMV China was closely related to SMV isolates from South Korea. We examined single nucleotide variations (SNVs) for SMVs in the soybean seed transcriptome revealing 780 SNVs, which were evenly distributed on the SMV genome. Four SNVs, C-U, U-C, A-G, and G-A, were frequently identified. This result demonstrated the quasispecies variation of the SMV genome. Taken together, this study carried out bioinformatics analyses to identify viruses using soybean transcriptome data. In addition, we demonstrated the application of soybean transcriptome data for virus genome assembly and SNV analysis.
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http://dx.doi.org/10.5423/PPJ.OA.03.2017.0060DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5624490PMC
October 2017

Genome Sequence of Grapevine Virus T, a Novel Foveavirus Infecting Grapevine.

Genome Announc 2017 Sep 14;5(37). Epub 2017 Sep 14.

Department of Agricultural Biotechnology, College of Agriculture and Life Sciences, Seoul National University, Seoul, Republic of Korea

Here, we report the genome sequence of grapevine virus T (GVT), a novel single-stranded RNA virus identified from a transcriptome of grapevine. The genome of GVT is 8,701 nucleotides in length and encodes five open reading frames. GVT is a putative member of the genus in the family .
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http://dx.doi.org/10.1128/genomeA.00995-17DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5597771PMC
September 2017

Genome Sequence of Grapevine Virus K, a Novel Vitivirus Infecting Grapevine.

Genome Announc 2017 Sep 14;5(37). Epub 2017 Sep 14.

Department of Agricultural Biotechnology, College of Agriculture and Life Sciences, Seoul National University, Seoul, Republic of Korea

Here, we report the genome sequence of grapevine virus K (GVK), a novel single-stranded RNA virus identified from a transcriptome of grapevine. The genome of GVK is 7,476 nucleotides in length and encodes 5 open reading frames. GVK is a putative member of the genus in the family .
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http://dx.doi.org/10.1128/genomeA.00994-17DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5597770PMC
September 2017

The pepper virome: natural co-infection of diverse viruses and their quasispecies.

BMC Genomics 2017 06 8;18(1):453. Epub 2017 Jun 8.

Department of Agricultural Biotechnology, College of Agriculture and Life Sciences, Seoul National University, Seoul, 151-921, Republic of Korea.

Background: The co-infection of diverse viruses in a host plant is common; however, little is known about viral populations and their quasispecies in the host.

Results: Here, we report the first pepper viromes that were co-infected by different types of viral genomes. The pepper viromes are dominated by geminivirus DNA-A followed by a novel carlavirus referred to as Pepper virus A. The two pepper cultivars share similar viral populations and replications. However, the quasispecies for double-stranded RNA virus and two satellite DNAs were heterogeneous and homogenous in susceptible and resistant cultivars, respectively, indicating the quasispecies of an individual virus depends on the host.

Conclusions: Taken together, we provide the first evidence that the host plant resistant to viruses has an unrevealed antiviral system, affecting viral quasispecies, not replication.
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http://dx.doi.org/10.1186/s12864-017-3838-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5465472PMC
June 2017

Identification of residues or motif(s) of the rice stripe virus NS3 protein required for self-interaction and for silencing suppressor activity.

Virus Res 2017 05 6;235:14-23. Epub 2017 Apr 6.

Department of Agricultural Biotechnology, Research Institute of Agriculture and Life Sciences, and Plant Genomics and Breeding Institute, College of Agriculture and Life Sciences, Seoul National University, Seoul 08826, Republic of Korea. Electronic address:

Rice stripe virus (RSV) is an important pathogen of rice. The RSV genome consists of four single-stranded RNA segments that encode seven viral proteins. A previous report found that NS3 is a viral suppressor of RNA silencing and self interacts. Using a model that predicts protein structure, we identified amino acid residues or motifs, including four α-helix motifs, required for NS3 self-interaction. We then used yeast two-hybrid (Y2H) and bimolecular fluorescence complementation (BiFC) assays to study the interactions between full-length NS3 and its truncated and alanine substitution mutants. Y2H and BiFC results showed that the N-terminal region of NS3 is essential for self-interaction. All α-helix deletion mutants and substitution mutants lost the ability to self-interact. To identify the relationship between NS3 self-interaction and silencing suppressor activity, we used a GFP silencing system in Nicotiana benthamiana with Agrobacterium-mediated transient overexpression of each mutated NS3 protein. All of the deletion and the α-helix substitution mutants that had lost the ability to self-interact also lost their silencing suppressor ability. The substitution of amino acids with alanine at positions 70-75, 76-83, and 173-177, however, resulted in mutants that were able to self-interact but were unable to function as silencing suppressors. These results suggest that RSV requires NS3 self-interaction to suppress RNA silencing and to thereby counter host defenses.
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http://dx.doi.org/10.1016/j.virusres.2017.03.022DOI Listing
May 2017

Sequence variability of in different chrysanthemum cultivars.

PeerJ 2017 26;5:e2933. Epub 2017 Jan 26.

Department of Agricultural Biotechnology, College of Agriculture and Life Sciences, Seoul National University, Seoul, Republic of Korea.

Viroids are the smallest infectious agents, and their genomes consist of a short single strand of RNA that does not encode any protein. (CSVd), a member of the family , causes chrysanthemum stunt disease. Here, we report the genomic variations of CSVd to understand the sequence variability of CSVd in different chrysanthemum cultivars. We randomly sampled 36 different chrysanthemum cultivars and examined the infection of CSVd in each cultivar by reverse transcription polymerase chain reaction (RT-PCR). Eleven cultivars were infected by CSVd. Cloning followed by Sanger sequencing successfully identified a total of 271 CSVd genomes derived from 12 plants from 11 cultivars. They were further classified into 105 CSVd variants. Each single chrysanthemum plant had a different set of CSVd variants. Moreover, different single plants from the same cultivar had different sets of CSVd variants but identical consensus genome sequences. A phylogenetic tree using 12 consensus genome sequences revealed three groups of CSVd genomes, while six different groups were defined by the phylogenetic analysis using 105 variants. Based on the consensus CSVd genome, by combining all variant sequences, we identified 99 single-nucleotide variations (SNVs) as well as three nucleotide positions showing high mutation rates. Although 99 SNVs were identified, most CSVd genomes in this study were derived from variant 1, which is identical to known CSVd SK1 showing pathogenicity.
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http://dx.doi.org/10.7717/peerj.2933DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5274516PMC
January 2017

Time-Course Small RNA Profiling Reveals Rice miRNAs and Their Target Genes in Response to Rice Stripe Virus Infection.

PLoS One 2016 14;11(9):e0162319. Epub 2016 Sep 14.

Department of Agricultural Biotechnology, Research Institute of Agriculture and Life Sciences, and Plant Genomics and Breeding Institute, College of Agriculture and Life Sciences, Seoul National University, Seoul, 08826, Republic of Korea.

It has been known that many microRNAs (miRNAs) are involved in the regulation for the plant development and defense mechanism by regulating the expression of the target gene. Several previous studies has demonstrated functional roles of miRNAs in antiviral defense mechanisms. In this study, we employed high-throughput sequencing technology to identify rice miRNAs upon rice stripe virus (RSV) infection at three different time points. Six libraries from mock and RSV-infected samples were subjected for small RNA sequencing. Bioinformatic analyses revealed 374 known miRNAs and 19 novel miRNAs. Expression of most identified miRNAs was not dramatically changed at 3 days post infection (dpi) and 7 dpi by RSV infection. However, many numbers of miRNAs were up-regulated in mock and RSV-infected samples at 15 dpi by RSV infection. Moreover, expression profiles of identified miRNAs revealed that only few numbers of miRNAs were strongly regulated by RSV infection. In addition, 15 resistance genes were targets of six miRNAs suggesting that those identified miRNAs and 15 NBS-LRR resistance genes might be involved in RSV infection. Taken together, our results provide novel insight into the dynamic expression profiles of rice miRNAs upon RSV infection and clues for the understanding of the regulatory roles of miRNAs via time-course.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0162319PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5023111PMC
August 2017

Integrated analyses using RNA-Seq data reveal viral genomes, single nucleotide variations, the phylogenetic relationship, and recombination for Apple stem grooving virus.

BMC Genomics 2016 08 9;17:579. Epub 2016 Aug 9.

Department of Agricultural Biotechnology, College of Agriculture and Life Sciences, Seoul National University, Seoul, 151-921, Republic of Korea.

Background: Next-generation sequencing (NGS) provides many possibilities for plant virology research. In this study, we performed integrated analyses using plant transcriptome data for plant virus identification using Apple stem grooving virus (ASGV) as an exemplar virus. We used 15 publicly available transcriptome libraries from three different studies, two mRNA-Seq studies and a small RNA-Seq study.

Results: We de novo assembled nearly complete genomes of ASGV isolates Fuji and Cuiguan from apple and pear transcriptomes, respectively, and identified single nucleotide variations (SNVs) of ASGV within the transcriptomes. We demonstrated the application of NGS raw data to confirm viral infections in the plant transcriptomes. In addition, we compared the usability of two de novo assemblers, Trinity and Velvet, for virus identification and genome assembly. A phylogenetic tree revealed that ASGV and Citrus tatter leaf virus (CTLV) are the same virus, which was divided into two clades. Recombination analyses identified six recombination events from 21 viral genomes.

Conclusions: Taken together, our in silico analyses using NGS data provide a successful application of plant transcriptomes to reveal extensive information associated with viral genome assembly, SNVs, phylogenetic relationships, and genetic recombination.
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http://dx.doi.org/10.1186/s12864-016-2994-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4977635PMC
August 2016

Development of Virus-Induced Gene Expression and Silencing Vector Derived from Grapevine Algerian Latent Virus.

Plant Pathol J 2016 Aug 1;32(4):371-6. Epub 2016 Aug 1.

Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Sciences, Seoul National University, Seoul 08826, Korea; Plant Genomics and Breeding Institute, Seoul National University, Seoul 08826, Korea.

Grapevine Algerian latent virus (GALV) is a member of the genus Tombusvirus in the Tombusviridae and infects not only woody perennial grapevine plant but also herbaceous Nicotiana benthamiana plant. In this study, we developed GALV-based gene expression and virus-induced gene silencing (VIGS) vectors in N. benthamiana. The GALV coat protein deletion vector, pGMG, was applied to express the reporter gene, green fluorescence protein (GFP), but the expression of GFP was not detected due to the necrotic cell death on the infiltrated leaves. The p19 silencing suppressor of GALV was engineered to inactivate its expression and GFP was successfully expressed with unrelated silencing suppressor, HC-Pro, from soybean mosaic virus. The pGMG vector was used to knock down magnesium chelatase (ChlH) gene in N. benthamaina and the silencing phenotype was clearly observed on systemic leaves. Altogether, the GALV-derived vector is expected to be an attractive tool for useful gene expression and VIGS vectors in grapevine as well as N. benthamiana.
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http://dx.doi.org/10.5423/PPJ.NT.11.2015.0237DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4968648PMC
August 2016

Two homologous host proteins interact with potato virus X RNAs and CPs and affect viral replication and movement.

Sci Rep 2016 06 29;6:28743. Epub 2016 Jun 29.

Department of Agricultural Biotechnology, Seoul National University, Seoul, Korea.

Because viruses encode only a small number of proteins, all steps of virus infection rely on specific interactions between viruses and hosts. We previously screened several Nicotiana benthamiana (Nb) proteins that interact with the stem-loop 1 (SL1) RNA structure located at the 5' end of the potato virus X (PVX) genome. In this study, we characterized two of these proteins (NbCPIP2a and NbCPIP2b), which are homologous and are induced upon PVX infection. Electrophoretic mobility shift assay confirmed that both proteins bind to either SL1(+) or SL1(-) RNAs of PVX. The two proteins also interact with the PVX capsid protein (CP) in planta. Overexpression of NbCPIP2a positively regulated systemic movement of PVX in N. benthamiana, whereas NbCPIP2b overexpression did not affect systemic movement of PVX. Transient overexpression and silencing experiments demonstrated that NbCPIP2a and NbCPIP2b are positive regulators of PVX replication and that the effect on replication was greater for NbCPIP2a than for NbCPIP2b. Although these two host proteins are associated with plasma membranes, PVX infection did not affect their subcellular localization. Taken together, these results indicate that NbCPIP2a and NbCPIP2b specifically bind to PVX SL1 RNAs as well as to CP and enhance PVX replication and movement.
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http://dx.doi.org/10.1038/srep28743DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4926161PMC
June 2016

De novo transcriptome assembly of Setatria italica variety Taejin.

Genom Data 2016 Jun 5;8:121-2. Epub 2016 May 5.

Department of Agricultural Biotechnology, College of Agriculture and Life Sciences, Seoul National University, Seoul 151-921, Republic of Korea; The Taejin Genome Institute, Gadam-gil 61, Hoeongseong 25239, Republic of Korea.

Foxtail millet (Setaria italica) belonging to the family Poaceae is an important millet that is widely cultivated in East Asia. Of the cultivated millets, the foxtail millet has the longest history and is one of the main food crops in South India and China. Moreover, foxtail millet is a model plant system for biofuel generation utilizing the C4 photosynthetic pathway. In this study, we carried out de novo transcriptome assembly for the foxtail millet variety Taejin collected from Korea using next-generation sequencing. We obtained a total of 8.676 GB raw data by paired-end sequencing. The raw data in this study can be available in NCBI SRA database with accession number of SRR3406552. The Trinity program was used to de novo assemble 145,332 transcripts. Using the TransDecoder program, we predicted 82,925 putative proteins. BLASTP was performed against the Swiss-Prot protein sequence database to annotate the functions of identified proteins, resulting in 20,555 potentially novel proteins. Taken together, this study provides transcriptome data for the foxtail millet variety Taejin by RNA-Seq.
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http://dx.doi.org/10.1016/j.gdata.2016.05.001DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4878839PMC
June 2016