Publications by authors named "Kook-Hyung Kim"

96 Publications

Using RNA-Sequencing Data to Examine Tissue-Specific Garlic Microbiomes.

Int J Mol Sci 2021 Jun 24;22(13). Epub 2021 Jun 24.

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

Garlic () is a perennial bulbous plant. Due to its clonal propagation, various diseases threaten the yield and quality of garlic. In this study, we conducted in silico analysis to identify microorganisms, bacteria, fungi, and viruses in six different tissues using garlic RNA-sequencing data. The number of identified microbial species was the highest in inflorescences, followed by flowers and bulb cloves. With the Kraken2 tool, 57% of identified microbial reads were assigned to bacteria and 41% were assigned to viruses. Fungi only made up 1% of microbial reads. At the species level, was the most dominant bacteria while was the most abundant fungi. Several allexiviruses were identified. Of them, the most abundant virus was garlic virus C followed by shallot virus X. We obtained a total of 14 viral genome sequences for four allexiviruses. As we expected, the microbial community varied depending on the tissue types, although there was a dominant microorganism in each tissue. In addition, we found that Kraken2 was a very powerful and efficient tool for the bacteria using RNA-sequencing data with some limitations for virome study.
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http://dx.doi.org/10.3390/ijms22136791DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8268838PMC
June 2021

Comparative Study of Metagenomics and Metatranscriptomics to Reveal Microbiomes in Overwintering Pepper Fruits.

Int J Mol Sci 2021 Jun 8;22(12). Epub 2021 Jun 8.

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

Red pepper (, L.), is one of the most important spice plants in Korea. Overwintering pepper fruits are a reservoir of various microbial pepper diseases. Here, we conducted metagenomics (DNA sequencing) and metatranscriptomics (RNA sequencing) using samples collected from three different fields. We compared two different library types and three different analytical methods for the identification of microbiomes in overwintering pepper fruits. Our results demonstrated that DNA sequencing might be useful for the identification of bacteria and DNA viruses such as bacteriophages, while mRNA sequencing might be beneficial for the identification of fungi and RNA viruses. Among three analytical methods, KRAKEN2 with raw data reads (KRAKEN2_R) might be superior for the identification of microbial species to other analytical methods. However, some microbial species with a low number of reads were wrongly assigned at the species level by KRAKEN2_R. Moreover, we found that the databases for bacteria and viruses were better established as compared to the fungal database with limited genome data. In summary, we carefully suggest that different library types and analytical methods with proper databases should be applied for the purpose of microbiome study.
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http://dx.doi.org/10.3390/ijms22126202DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8227054PMC
June 2021

A Phenome-Wide Association Study of the Effects of Transcription Factors on Fusarium Graminearum Virus 1 Infection.

Front Microbiol 2021 11;12:622261. Epub 2021 Feb 11.

Plant Genomics and Breeding Institute, Seoul National University, Seoul, South Korea.

The Fusarium graminearum virus 1 (FgV1) causes noticeable phenotypic changes such as reduced mycelial growth, increase pigmentation, and reduced pathogenicity in its host fungi, . Previous study showed that the numerous genes including regulatory factors were differentially expressed upon FgV1 infection, however, we have limited knowledge on the effect(s) of specific transcription factor (TF) during FgV1 infection in host fungus. Using gene-deletion mutant library of 657 putative TFs in , we transferred FgV1 by hyphal anastomosis to screen transcription factors that might be associated with viral replication or symptom induction. FgV1-infected TF deletion mutants were divided into three groups according to the mycelial growth phenotype compare to the FgV1-infected wild-type strain (WT-VI). The FgV1-infected TF deletion mutants in Group 1 exhibited slow or weak mycelial growth compare to that of WT-VI on complete medium at 5 dpi. In contrast, Group 3 consists of virus-infected TF deletion mutants showing faster mycelial growth and mild symptom compared to that of WT-VI. The hyphal growth of FgV1-infected TF deletion mutants in Group 2 was not significantly different from that of WT-VI. We speculated that differences of mycelial growth among the FgV1-infected TF deletion mutant groups might be related with the level of FgV1 RNA accumulations in infected host fungi. By conducting real-time quantitative reverse transcription polymerase chain reaction, we observed close association between FgV1 RNA accumulation and phenotypic differences of FgV1-infected TF deletion mutants in each group, i.e., increased and decreased dsRNA accumulation in Group 1 and Group 3, respectively. Taken together, our analysis provides an opportunity to identify host's regulator(s) of FgV1-triggered signaling and antiviral responses and helps to understand complex regulatory networks between FgV1 and interaction.
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http://dx.doi.org/10.3389/fmicb.2021.622261DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7904688PMC
February 2021

The Signatures of Natural Selection and Molecular Evolution in Fusarium graminearum Virus 1.

Front Microbiol 2020 12;11:600775. Epub 2020 Nov 12.

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

Fusarium graminearum virus 1 (FgV1) is a positive-sense ssRNA virus that confers hypovirulence in its fungal host, . Like most mycoviruses, FgV1 exists in fungal cells, lacks an extracellular life cycle, and is therefore transmitted during sporulation or hyphal anastomosis. To understand FgV1 evolution and/or adaptation, we conducted mutation accumulation (MA) experiments by serial passage of FgV1 alone or with FgV2, 3, or 4 in . We expected that the effects of positive selection would be highly limited because of repeated bottleneck events. To determine whether selection on the virus was positive, negative, or neutral, we assessed both the phenotypic traits of the host fungus and the RNA sequences of FgV1. We inferred that there was positive selection on beneficial mutations in FgV1 based on the ratio of non-synonymous to synonymous substitutions ( ), on the ratio of radical to conservation amino acid replacements ( ), and by changes in the predicted protein structures. In support of this inference, we found evidence of positive selection only in the open reading frame 4 (ORF4) protein of DK21/FgV1 (MA line 1); mutations at amino acids 163A and 289H in the ORF4 of MA line 1 affected the entire structure of the protein predicted to be under positive selection. We also found, however, that deleterious mutations were a major driving force in viral evolution during serial passages. Linear relationships between changes in viral fitness and the number of mutations in each MA line demonstrated that some deleterious mutations resulted in fitness decline. Several mutations in MA line 1 were not shared with any of the other four MA lines (PH-1/FgV1, PH-1/FgV1 + 2, PH-1/FgV1 + 3, and PH-1/FgV1 + 4). This suggests that evolutionary pathways of the virus could differ with respect to hosts and also with respect to co-infecting viruses. The data also suggested that the differences among MA lines might also be explained by mutational robustness and other unidentified factors. Additional research is needed to clarify the effects of virus co-infection on the adaptation or evolution of FgV1 to its environments.
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http://dx.doi.org/10.3389/fmicb.2020.600775DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7688778PMC
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

Exploration of the interactions between mycoviruses and Fusarium graminearum.

Adv Virus Res 2020 5;106:123-144. Epub 2020 Feb 5.

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

In this review, we discuss recent studies of the interaction between Fusarium graminearum viruses (FgVs) and the fungal host, Fusarium graminearum. Comprehensive transcriptome and proteome analyses have shown changes in the expression of host genes in response to infection by diverse FgVs. Using omics data and reverse genetics, researchers have determined the effects of some fungal host proteins (including FgHex1, FgHal2, FgSwi6, and vr1) on virus accumulation, virus transmission, and host symptom development. Recent reports have revealed the functions of the RNAi component in F. graminearum and the functional redundancy of FgDICERs and FgAGOs in the antiviral defense response against different FgV infections. Studies have also documented a unique mechanism used by FgV1 to overcome the antiviral response of the fungal host.
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http://dx.doi.org/10.1016/bs.aivir.2020.01.004DOI Listing
October 2020

Soybean Resistance to Soybean Mosaic Virus.

Plants (Basel) 2020 Feb 8;9(2). Epub 2020 Feb 8.

Department of Agricultural Biotechnology, College of Agriculture and Life Sciences, Seoul National University, Seoul 08826, Korea.

Soybean mosaic virus (SMV) occurs in all soybean-growing areas in the world and causes huge losses in soybean yields and seed quality. During early viral infection, molecular interactions between SMV effector proteins and the soybean resistance (R) protein, if present, determine the development of resistance/disease in soybean plants. Depending on the interacting strain and cultivar, R-protein in resistant soybean perceives a specific SMV effector, which triggers either the extreme silent resistance or the typical resistance manifested by hypersensitive responses and induction of salicylic acid and reactive oxygen species. In this review, we consider the major advances that have been made in understanding the soybean-SMV arms race. We also focus on dissecting mechanisms SMV employs to establish infection and how soybean perceives and then responds to SMV attack. In addition, progress on soybean -genes studies, as well as those addressing independent resistance genes, are also addressed.
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http://dx.doi.org/10.3390/plants9020219DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7076706PMC
February 2020

The ORF2 protein of Fusarium graminearum virus 1 suppresses the transcription of FgDICER2 and FgAGO1 to limit host antiviral defences.

Mol Plant Pathol 2020 02 9;21(2):230-243. Epub 2019 Dec 9.

Plant Genomics and Breeding Institute, Seoul National University, Seoul, Korea.

The filamentous fungus Fusarium graminearum possesses an RNA-interference (RNAi) pathway that acts as a defence response against virus infections and exogenous double-stranded (ds) RNA. Fusarium graminearum virus 1 (FgV1), which infects F. graminearum, confers hypovirulence-associated traits such as reduced mycelial growth, increased pigmentation and reduced pathogenicity. In this study, we found that FgV1 can suppress RNA silencing by interfering with the induction of FgDICER2 and FgAGO1, which are involved in RNAi antiviral defence and the hairpin RNA/RNAi pathway in F. graminearum. In an FgAGO1- or FgDICER2-promoter/GFP-reporter expression assay the green fluorescent protein (GFP) transcript levels were reduced in FgV1-infected transformed mutant strains. By comparing transcription levels of FgDICER2 and FgAGO1 in fungal transformed mutants expressing each open reading frame (ORF) of FgV1 with or without a hairpin RNA construct, we determined that reduction of FgDICER2 and FgAGO1 transcript levels requires only the FgV1 ORF2-encoded protein (pORF2). Moreover, we confirmed that the pORF2 binds to the upstream region of FgDICERs and FgAGOs in vitro. These combined results indicate that the pORF2 of FgV1 counteracts the RNAi defence response of F. graminearum by interfering with the induction of FgDICER2 and FgAGO1 in a promoter-dependent manner.
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http://dx.doi.org/10.1111/mpp.12895DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6988435PMC
February 2020

An Avirulent Strain of Soybean Mosaic Virus Reverses the Defensive Effect of Abscisic Acid in a Susceptible Soybean Cultivar.

Viruses 2019 09 19;11(9). Epub 2019 Sep 19.

Department of Agricultural Biotechnology, College of Agriculture and Life Sciences, Seoul National University, Seoul 08826, Korea.

In soybean cultivar L29, the gene is responsible for extreme resistance (ER) against the soybean mosaic virus avirulent strain G5H, but is ineffective against the virulent strain G7H. Part of this ER is attributed to the rapid increase in abscisic acid (ABA) and callose, and to the rapid induction of several genes in the RNA-silencing pathway. Whether these two defense mechanisms are correlated or separated in the ER is unknown. Here, we found that ABA treatment of L29 plants increased the expression of several antiviral RNA-silencing genes as well as the gene, which was previously shown to increase callose accumulation; as a consequence, ABA increased the resistance of L29 plants to G7H. The effect of ABA treatment on these genes was weaker in the rsv3-null cultivar (Somyungkong) than in L29. Besides, G5H-infection of Somyungkong plants subverted the effect of ABA leading to reduced callose accumulation and decreased expression of several RNA-silencing genes, which resulted in increased susceptibility to G5H infection. ABA treatment, however, still induced some resistance to G7H in Somyungkong, but only was significantly induced. Our data suggest that modulates the effect of ABA on these two resistance mechanisms, i.e., callose accumulation and the antiviral RNA-silencing pathway, and that in the absence of , some strains can reverse the effect of ABA and thereby facilitate their replication and spread.
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http://dx.doi.org/10.3390/v11090879DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6783863PMC
September 2019

Effects of Abscisic Acid and Salicylic Acid on Gene Expression in the Antiviral RNA Silencing Pathway in Arabidopsis.

Int J Mol Sci 2019 May 23;20(10). Epub 2019 May 23.

Institute of Plant and Microbial Biology, Academia Sinica, Taipei 11529, Taiwan.

The RNA silencing pathways modulate responses to certain stresses, and can be partially tuned by several hormones such as salicylic acid (SA) and abscisic acid (ABA). Although SA and ABA are often antagonistic and often modulate different stress responses, they have similar effects on virus resistance, which are partially achieved through the antiviral RNA silencing pathway. Whether they play similar roles in regulating the RNA silencing pathway is unclear. By employing coexpression and promoter analyses, we found that some ABA- and SA-related transcription factors (TFs) are coexpressed with several , , and genes, and have multiple binding sites for the identified TFs in the queried promoters. ABA and SA are antagonistic with respect to the expression of and because ABA was able to induce these genes only in the SA mutant. Nevertheless, both hormones showed similarities in the regulation of other genes, for example, the induction of by ABA was SA-dependent, indicating that ABA acts upstream of SA in this regulation. We inferred that the similar effects of ABA and SA on some genes resulted in the redundancy of their roles in resistance to bamboo mosaic virus, but that the two hormones are antagonistic with respect to other genes unrelated to their biosynthesis pathways.
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http://dx.doi.org/10.3390/ijms20102538DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6566719PMC
May 2019

A plant intron enhances the performance of an infectious clone in planta.

J Virol Methods 2019 03 19;265:26-34. Epub 2018 Dec 19.

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

Although infectious clones are fundamental tools in virology and plant pathology, their efficacy is often reduced by the instability of viral sequences in Escherichia coli. In this study, we constructed an infectious clone of PepMoV (pPepMoV) in a bacterial binary vector (pSNU1); the clone induces symptoms of PepMoV in agroinfiltrated plants. During its modification and maintenance in E. coli, however, the pPepMoV infectious clone was instable in the bacteria. Manipulation of this unstable clone in the bacterial strain DH10B led to the spontaneous formation of a recombined clone with high stability in the bacteria but with reduced infectivity due to an unwanted insertion of an E. coli sequence in the NIa-protease coding region. Replacement of this sequence with a plant intron restored infectivity and maintained plasmid stability. In addition to restoring plasmid growth in both E. coli and Agrobacterium, the presence of the intron in the PepMoV sequence enhanced the accumulation of PepMoV in agroinfiltrated leaves and resulted in symptom induction in upper systemic leaves that was nearly as strong as with PepMoV sap-inoculation. Plant introns have been previously used to stabilize plasmids in E. coli without any effect or with an unexpected lag in symptom development. In contrast, the current results demonstrated the in vivo enhancement of an infectious clone by a plant intron.
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http://dx.doi.org/10.1016/j.jviromet.2018.12.012DOI Listing
March 2019

Elements Involved in the Rsv3-Mediated Extreme Resistance against an Avirulent Strain of Soybean Mosaic Virus.

Viruses 2018 10 24;10(11). Epub 2018 Oct 24.

Department of Agricultural Biotechnology, College of Agriculture and Life Sciences, Seoul National University, Seoul 08826, Korea.

Extreme resistance (ER) is a type of -gene-mediated resistance that rapidly induces a symptomless resistance phenotype, which is different from the phenotypical -resistance manifested by the programmed cell death, accumulation of reactive oxygen species, and hypersensitive response. The gene in soybean cultivar L29 is responsible for ER against the avirulent strain G5H of soybean mosaic virus (SMV), but is ineffective against the virulent strain G7H. Rsv3-mediated ER is achieved through the rapid accumulation of callose, which arrests SMV-G5H at the point of infection. Callose accumulation, however, may not be the lone mechanism of this ER. Analyses of RNA-seq data obtained from infected soybean plants revealed a rapid induction of the abscisic acid pathway at 8 h post infection (hpi) in response to G5H but not to G7H, which resulted in the down-regulation of transcripts encoding β-1,3 glucanases that degrade callose in G5H-infected but not G7H-infected plants. In addition, parts of the autophagy and the small interfering (si) RNA pathways were temporally up-regulated at 24 hpi in response to G5H but not in response to G7H. The jasmonic acid (JA) pathway and many WRKY factors were clearly up-regulated only in G7H-infected plants. These results suggest that ER against SMV-G5H is achieved through the quick and temporary induction of ABA, autophagy, and the siRNA pathways, which rapidly eliminate G5H. The results also suggest that suppression of the JA pathway in the case of G5H is important for the Rsv3-mediated ER.
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http://dx.doi.org/10.3390/v10110581DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6267276PMC
October 2018

ICTV Virus Taxonomy Profile: Hypoviridae.

J Gen Virol 2018 05 28;99(5):615-616. Epub 2018 Mar 28.

Department of Plant Biology and Pathology, Rutgers University, New Brunswick, NJ 08901, USA.

The Hypoviridae, comprising one genus, Hypovirus, is a family of capsidless viruses with positive-sense, ssRNA genomes of 9.1-12.7 kb that possess either a single large ORF or two ORFs. The ORFs appear to be translated from genomic RNA by non-canonical mechanisms, i.e. internal ribosome entry site-mediated and stop/restart translation. Hypoviruses have been detected in ascomycetous or basidiomycetous filamentous fungi, and are considered to be replicated in host Golgi-derived, lipid vesicles that contain their dsRNA as a replicative form. Some hypoviruses induce hypovirulence to host fungi, while others do not. This is a summary of the current ICTV report on the taxonomy of the Hypoviridae, which is available at www.ictv.global/report/hypoviridae.
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http://dx.doi.org/10.1099/jgv.0.001055DOI Listing
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

Isolation and validation of a candidate Rsv3 gene from a soybean genotype that confers strain-specific resistance to soybean mosaic virus.

Virology 2018 01 5;513:153-159. Epub 2017 Nov 5.

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

Soybean mosaic virus (SMV), a member of the genus Potyvirus, significantly reduces soybean production worldwide. Rsv3, which confers strain-specific resistance to SMV, was previously mapped between the markers A519F/R and M3Satt in chromosome 14 of the soybean [Glycine max (L.) Merr.] genotype L29. Analysis of the soybean genome database revealed that five different NBS-LRR sequences exist between the flanking markers. Among these candidate Rsv3 genes, the full-length cDNA of the Glyma.14g204700 was successfully cloned from L29. Over-expression of Glyma.14g204700 in leaves inoculated with SMV inhibited viral infection in a soybean genotype lacking Rsv3. In addition, the transient silencing of the candidate gene caused a high accumulation of an avirulent strain in L29 carrying Rsv3. Our results therefore provide additional line of evidence to support that Glyma.14g204700 is likely Rsv3 gene that confers strain-specific resistance to SMV.
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http://dx.doi.org/10.1016/j.virol.2017.10.014DOI Listing
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

Engineering an auto-activated R protein that is in vivo activated by a viral protease.

Virology 2017 10 25;510:242-247. Epub 2017 Jul 25.

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

Autonomous hypersensitive responses (self-HRs) are caused by constitutively active R proteins. In this study, we identified an auto-activated form of the R gene Pvr9 (autoPvr9); the auto-activation results from an amino acid substitution between its NBS and LRR domains. Self-HR was strongly reduced or completely inhibited by fusion of an extra peptide to the autoPvr9 N-terminal or C-terminal, respectively. When an NIa recognition site was placed between autoPvr9 and the extra peptide, the fusion construct could trigger an NIa-dependent HR. Several C-terminal fusions were tested, but only those that maintained detectable protein expression were capable of an NIa-dependent HR. Our results suggest the potential for transforming malfunctioning and auto-activated R proteins into a new construct targeting potyviral NIa proteases.
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http://dx.doi.org/10.1016/j.virol.2017.07.020DOI Listing
October 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

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

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

The Transcription Cofactor Swi6 of the Fusarium graminearum Is Involved in Fusarium Graminearum Virus 1 Infection-Induced Phenotypic Alterations.

Plant Pathol J 2016 Aug 1;32(4):281-9. Epub 2016 Aug 1.

Department of Agricultural Biotechnology and Center for Fungal Pathogenesis, College of Agriculture and Life Sciences, Seoul National University, Seoul 08826, Korea; Research Institute of Agriculture and Life Sciences, College of Agriculture and Life Sciences, Seoul National University, Seoul 08826, Korea; Department of Applied Biology and Chemistry, College of Agriculture and Life Sciences, Seoul National University, Seoul 08826, Korea.

The transcription cofactor Swi6 plays important roles in regulating vegetative growth and meiosis in Saccharomyces cerevisiae. Functions of Swi6 ortholog were also characterized in Fusarium graminearum which is one of the devastating plant pathogenic fungi. Here, we report possible role of FgSwi6 in the interaction between F. graminearum and Fusarium graminearum virus 1 (FgV1) strain DK21. FgV1 perturbs biological characteristics of host fungi such as vegetative growth, sporulation, pigmentation, and reduction of the virulence (hypovirulence) of its fungal host. To characterize function(s) of FgSWI6 gene during FgV1 infection, targeted deletion, over-expression, and complementation mutants were generated and further infected successfully with FgV1. Deletion of FgSwi6 led to severe reduction of vegetative growth even aerial mycelia while over-expression did not affect any remarkable alteration of phenotype in virus-free isolates. Virus-infected (VI) FgSWI6 deletion isolate exhibited completely delayed vegetative growth. However, VI FgSWI6 over-expression mutant grew faster than any other VI isolates. To verify whether these different growth patterns in VI isolates, viral RNA quantification was carried out using qRT-PCR. Surprisingly, viral RNA accumulations in VI isolates were similar regardless of introduced mutations. These results provide evidence that FgSWI6 might play important role(s) in FgV1 induced phenotype alteration such as delayed vegetative growth.
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http://dx.doi.org/10.5423/PPJ.OA.12.2015.0267DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4968638PMC
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

Virus-induced gene silencing reveals signal transduction components required for the Pvr9-mediated hypersensitive response in Nicotiana benthamiana.

Virology 2016 08 26;495:167-72. Epub 2016 May 26.

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

Resistance to pathogens mediated by plant resistance (R) proteins requires different signaling transduction components and pathways. Our previous studies revealed that a potyvirus resistance gene in pepper, Pvr9, confers a hypersensitive response (HR) to pepper mottle virus in Nicotiana benthamiana. Our results show that the Pvr9-mediated HR against pepper mottle virus infection requires HSP90, SGT1, NDR1, but not EDS1. These results suggest that the Pvr9-mediated HR is possibly related to the SA pathway but not the ET, JA, ROS or NO pathways.
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http://dx.doi.org/10.1016/j.virol.2016.05.011DOI Listing
August 2016

Engineering of soybean mosaic virus as a versatile tool for studying protein-protein interactions in soybean.

Sci Rep 2016 Feb 29;6:22436. Epub 2016 Feb 29.

Department of Agricultural Biotechnology and Plant Genomics and Breeding Institute, Seoul National University, Seoul 151-921, Republic of Korea.

Transient gene expression approaches are valuable tools for rapid introduction of genes of interest and characterization of their functions in plants. Although agroinfiltration is the most effectively and routinely used method for transient expression of multiple genes in various plant species, this approach has been largely unsuccessful in soybean. In this study, we engineered soybean mosaic virus (SMV) as a dual-gene delivery vector to simultaneously deliver and express two genes in soybean cells. We further show the application of the SMV-based dual vector for a bimolecular fluorescence complementation assay to visualize in vivo protein-protein interactions in soybean and for a co-immunoprecipitation assay to identify cellular proteins interacting with SMV helper component protease. This approach provides a rapid and cost-effective tool for transient introduction of multiple traits into soybean and for in vivo characterization of the soybean cellular protein interaction network.
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http://dx.doi.org/10.1038/srep22436DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4772626PMC
February 2016

Establishment of a Simple and Rapid Gene Delivery System for Cucurbits by Using Engineered of Zucchini yellow mosaic virus.

Plant Pathol J 2016 Feb 1;32(1):70-6. Epub 2016 Feb 1.

Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Sciences, Seoul National University, Seoul 151-921, Korea; Plant Genomics and Breeding Institute, Seoul National University, Seoul 151-921, Korea.

The infectious full-length cDNA clone of zucchini yellow mosaic virus (ZYMV) isolate PA (pZYMV-PA), which was isolated from pumpkin, was constructed by utilizing viral transcription and processing signals to produce infectious in vivo transcripts. Simple rub-inoculation of plasmid DNAs of pZYMV-PA was successful to cause infection of zucchini plants (Cucurbita pepo L.). We further engineered this infectious cDNA clone of ZYMV as a viral vector for systemic expression of heterologous proteins in cucurbits. We successfully expressed two reporter genes including gfp and bar in zucchini plants by simple rub-inoculation of plasmid DNAs of the ZYMV-based expression constructs. Our method of the ZYMV-based viral vector in association with the simple rub-inoculation provides an easy and rapid approach for introduction and evaluation of heterologous genes in cucurbits.
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http://dx.doi.org/10.5423/PPJ.NT.08.2015.0173DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4755678PMC
February 2016

Specific binding of Fusarium graminearum Hex1 protein to untranslated regions of the genomic RNA of Fusarium graminearum virus 1 correlates with increased accumulation of both strands of viral RNA.

Virology 2016 Feb 9;489:202-11. Epub 2016 Jan 9.

Department of Agricultural Biotechnology, Seoul National University, Seoul, Korea; Center for Fungal Pathogenesis, Seoul National University, Seoul, Korea; Research Institute of Agriculture and Life Sciences, Seoul National University, Seoul, Korea; Plant Genomics and Breeding Institute, Seoul National University, Seoul, Korea. Electronic address:

The HEX1 gene of Fusarium graminearum was previously reported to be required for the efficient accumulation of Fusarium graminearum virus 1 (FgV1) RNA in its host. To investigate the molecular mechanism underlying the production of FgHEX1 and the replication of FgV1 viral RNA, we conducted electrophoretic mobility shift assays (EMSA) with recombinant FgHex1 protein and RNA sequences derived from various regions of FgV1 genomic RNA. These analyses demonstrated that FgHex1 and both the 5'- and 3'-untranslated regions of plus-strand FgV1 RNA formed complexes. To determine whether FgHex1 protein affects FgV1 replication, we quantified accumulation viral RNAs in protoplasts and showed that both (+)- and (-)-strands of FgV1 RNAs were increased in the over-expression mutant and decreased in the deletion mutant. These results indicate that the FgHex1 functions in the synthesis of both strands of FgV1 RNA and therefore in FgV1 replication probably by specifically binding to the FgV1 genomic RNA.
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http://dx.doi.org/10.1016/j.virol.2015.12.013DOI Listing
February 2016

Establishment of an Agrobacterium-mediated Inoculation System for Cucumber Green Mottle Mosaic Virus.

Plant Pathol J 2015 Dec 30;31(4):433-7. Epub 2015 Dec 30.

Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Sciences, Seoul National University, Seoul 151-921, Korea ; Plant Genomics and Breeding Institute, Seoul National University, Seoul 151-921, Korea.

The infectious full-length cDNA clones of Cucumber green mottle mosaic virus (CGMMV) isolates KW and KOM, which were isolated from watermelon and oriental melon, respectively, were constructed under the control of the cauliflower mosaic virus 35S promoter. We successfully inoculated Nicotiana benthamiana with the cloned CGMMV isolates KW and KOM by Agrobacterium-mediated infiltration. Virulence and symptomatic characteristics of the cloned CGMMV isolates KW and KOM were tested on several indicator plants. No obvious differences between two cloned isolates in disease development were observed on the tested indicator plants. We also determined full genome sequences of the cloned CGMMV isolates KW and KOM. Sequence comparison revealed that only four amino acids (at positions 228, 699, 1212, and 1238 of the replicase protein region) differ between the cloned isolates KW and KOM. A previous study reported that the isolate KOM could not infect Chenopodium amaranticolor, but the cloned KOM induced chlorotic spots on the inoculated leaves. When compared with the previously reported sequence of the original KOM isolate, the cloned KOM contained one amino acid mutation (Ala to Thr) at position 228 of the replicase protein, suggesting that this mutation might be responsible for induction of chlorotic spots on the inoculated leaves of C. amaranticolor.
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http://dx.doi.org/10.5423/PPJ.NT.06.2015.0123DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4677753PMC
December 2015

Five Questions about Mycoviruses.

PLoS Pathog 2015 5;11(11):e1005172. Epub 2015 Nov 5.

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

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http://dx.doi.org/10.1371/journal.ppat.1005172DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4635019PMC
April 2016

Time-Course RNA-Seq Analysis Reveals Transcriptional Changes in Rice Plants Triggered by Rice stripe virus Infection.

PLoS One 2015 25;10(8):e0136736. Epub 2015 Aug 25.

Department of Agricultural Biotechnology and Plant Genomics and Breeding Institute, College of Agriculture and Life Sciences, Seoul National University, Seoul, 151-921, Republic of Korea; Research Institute of Agriculture and Life Sciences, Seoul National University, Seoul, 151-921, Republic of Korea.

Rice stripe virus (RSV) has become a major pathogen of rice. To determine how the rice transcriptome is modified in response to RSV infection, we used RNA-Seq to perform a genome-wide gene expression analysis of a susceptible rice cultivar. The transcriptomes of RSV-infected samples were compared to those of mock-treated samples at 3, 7, and 15 days post-infection (dpi). From 8 to 11% of the genes were differentially expressed (>2-fold difference in expression) in RSV-infected vs. noninfected rice. Among them, 532 genes were differentially expressed at all three time points. Surprisingly, 37.6% of the 532 genes are related to transposons. Gene ontology enrichment analysis revealed that many chloroplast genes were down-regulated in infected plants at 3 and 15 dpi. Expression of genes associated with cell differentiation and flowering was significantly down-regulated in infected plants at 15 dpi. In contrast, most of the up-regulated genes in infected plants concern the cell wall, plasma membrane, and vacuole and are known to function in various metabolic pathways and stress responses. In addition, transcripts of diverse transcription factors gradually accumulated in infected plants with increasing infection time. We also confirmed that the expression of gene subsets (including NBS-LRR domain-containing genes, receptor-like kinase genes, and genes involving RNA silencing) was changed by RSV infection. Taken together, we demonstrated that down-regulation of genes related to photosynthesis and flowering was strongly associated with disease symptoms caused by RSV and that up-regulation of genes involved in metabolic pathways, stress responses, and transcription was related to host defense mechanisms.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0136736PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4549299PMC
May 2016

Comparative analysis of chrysanthemum transcriptome in response to three RNA viruses: Cucumber mosaic virus, Tomato spotted wilt virus and Potato virus X.

Plant Mol Biol 2015 Jun 23;88(3):233-48. Epub 2015 Apr 23.

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

The chrysanthemum is one of popular flowers in the world and a host for several viruses. So far, molecular interaction studies between the chrysanthemum and viruses are limited. In this study, we carried out a transcriptome analysis of chrysanthemum in response to three different viruses including Cucumber mosaic virus (CMV), Tomato spotted wilt virus (TSWV) and Potato virus X (PVX). A chrysanthemum 135K microarray derived from expressed sequence tags was successfully applied for the expression profiles of the chrysanthemum at early stage of virus infection. Finally, we identified a total of 125, 70 and 124 differentially expressed genes (DEGs) for CMV, TSWV and PVX, respectively. Many DEGs were virus specific; however, 33 DEGs were commonly regulated by three viruses. Gene ontology (GO) enrichment analysis identified a total of 132 GO terms, and of them, six GO terms related stress response and MCM complex were commonly identified for three viruses. Several genes functioning in stress response such as chitin response and ethylene mediated signaling pathway were up-regulated indicating their involvement in establishment of host immune system. In particular, TSWV infection significantly down-regulated genes related to DNA metabolic process including DNA replication, chromatin organization, histone modification and cytokinesis, and they are mostly targeted to nucleosome and MCM complex. Taken together, our comparative transcriptome analysis revealed several genes related to hormone mediated viral stress response and DNA modification. The identified chrysanthemums genes could be good candidates for further functional study associated with resistant to various plant viruses.
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http://dx.doi.org/10.1007/s11103-015-0317-yDOI Listing
June 2015
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