Efficient Gene Silencing Mediated by Tobacco Rattle Virus in an Emerging Model Plant Physalis
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{"title"=>"Efficient gene silencing mediated by tobacco rattle virus in an emerging model plant Physalis", "type"=>"journal", "authors"=>[{"first_name"=>"Ji Si", "last_name"=>"Zhang", "scopus_author_id"=>"36106529600"}, {"first_name"=>"Jing", "last_name"=>"Zhao", "scopus_author_id"=>"57191637360"}, {"first_name"=>"Shaohua", "last_name"=>"Zhang", "scopus_author_id"=>"56108882900"}, {"first_name"=>"Chaoying", "last_name"=>"He", "scopus_author_id"=>"7402283577"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-84893459867", "sgr"=>"84893459867", "issn"=>"19326203", "doi"=>"10.1371/journal.pone.0085534", "pmid"=>"24454885", "isbn"=>"1932-6203", "pui"=>"372801785"}, "id"=>"aacc9215-a0cb-3e06-8a99-925bd9967137", "abstract"=>"The fruit of Physalis has a berry and a novelty called inflated calyx syndrome (ICS, also named the 'Chinese lantern'). Elucidation of the underlying developmental mechanisms of fruit diversity demands an efficient gene functional inference platform. Here, we tested the application of the tobacco rattle virus (TRV)-mediated gene-silencing system in Physalis floridana. First, we characterized the putative gene of a phytoene desaturase in P. floridana (PfPDS). Infecting the leaves of the Physalis seedlings with the PfPDS-TRV vector resulted in a bleached plant, including the developing leaves, floral organs, ICS, berry, and seed. These results indicated that a local VIGS treatment can efficiently induce a systemic mutated phenotype. qRT-PCR analyses revealed that the bleaching extent correlated to the mRNA reduction of the endogenous PfPDS. Detailed comparisons of multiple infiltration and growth protocols allowed us to determine the optimal methodologies for VIGS manipulation in Physalis. We subsequently utilized this optimized VIGS methodology to downregulate the expression of two MADS-box genes, MPF2 and MPF3, and compared the resulting effects with gene-downregulation mediated by RNA interference (RNAi) methods. The VIGS-mediated gene knockdown plants were found to resemble the mutated phenotypes of floral calyx, fruiting calyx and pollen maturation of the RNAi transgenic plants for both MPF2 and MPF3. Moreover, the two MADS-box genes were appeared to have a novel role in the pedicel development in P. floridana. The major advantage of VIGS-based gene knockdown lies in practical aspects of saving time and easy manipulation as compared to the RNAi. Despite the lack of heritability and mosaic mutation phenotypes observed in some organs, the TRV-mediated gene silencing system provides an alternative efficient way to infer gene function in various developmental processes in Physalis, thus facilitating understanding of the genetic basis of the evolution and development of the morphological diversities within the Solanaceae.", "link"=>"http://www.mendeley.com/research/efficient-gene-silencing-mediated-tobacco-rattle-virus-emerging-model-plant-physalis", "reader_count"=>24, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>1, "Researcher"=>8, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>8, "Other"=>1, "Student > Master"=>2, "Professor"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>1, "Researcher"=>8, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>8, "Other"=>1, "Student > Master"=>2, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>2, "Agricultural and Biological Sciences"=>20, "Medicine and Dentistry"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>20}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"Netherlands"=>1, "Philippines"=>1, "Mexico"=>1, "India"=>1}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1346988"], "description"=>"<p>(<b>A</b>) An intact WT flower. (<b>B</b>) An intact <i>MPF2</i>-VIGS flower. Bars = 1 mm. (<b>C</b>) I<sub>2</sub>-KI stained pollen from WT. (<b>D</b>) I<sub>2</sub>-KI stained pollen from <i>MPF2</i>-VIGS. Active pollen is blue and sterile pollen is tawny. Bars = 100 µm. (<b>E</b>) Floral calyx epidermal cells of WT. (<b>F</b>) Floral calyx epidermal cells of <i>MPF2</i>-VIGS. Bars = 20 µm. (<b>G</b>) Size of calyx surface (gray column) and epidermal cells (white column) of the floral calyx in WT and <i>MPF2</i>-VIGS (“VIGS”). 20 cells and 20 calyces were analyzed for both WT and <i>MPF2</i>-VIGS samples. Mean values and standard deviation are presented. (<b>H</b>) Gene expression analysis of <i>MPF2</i>-RNAi and -VIGS. Expression of <i>MPF2</i> was compared between <i>MPF2</i>-RNAi flowers (R1–R3), <i>MPF2</i>-VIGS flowers (V1–V3) and wild-type (WT) <i>Physalis</i> via qRT-PCR analysis. The severe <i>MPF2</i> residual in VIGS was only 6% of that in the wild-type (WT), while in the RNAi the <i>MPF2</i> residual was 14% of that in the wild-type (WT). <i>PFACTIN</i> was used as an internal control. (<b>I</b>) <i>MPF2</i> expression was evaluated in two floral organs of VIGS flowers. Expression of <i>MPF2</i> in <i>MPF2</i>-RNAi (gray column), <i>MPF2</i>-VIGS (white column) was compared with that in the wild-type (WT, black column). The gene expression in the calyx of the WT was set as 1, and <i>PFACTIN</i> was used as an internal control. The experiments were repeated with three independent biological samples. Mean expression values and standard deviation are presented.</p>", "links"=>[], "tags"=>["Agricultural biotechnology", "developmental biology", "Plant growth and development", "genetics", "gene expression", "RNA interference", "Gene function", "Plant genetics", "Molecular cell biology", "Signal transduction", "Signaling in selected disciplines", "Developmental signaling", "Plant science", "phenocopies"], "article_id"=>900753, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Ji-Si Zhang", "Jing Zhao", "Shaohua Zhang", "Chaoying He"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085534.g003", "stats"=>{"downloads"=>1, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_VIGS_mediated_MPF2_silencing_phenocopies_MPF2_RNAi_/900753", "title"=>"VIGS-mediated <i>MPF2</i> silencing phenocopies <i>MPF2</i>-RNAi.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-14 03:10:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/1346991"], "description"=>"<p>(<b>A</b>) An intact WT small flower bud. (<b>B</b>) An intact WT flower bud. (<b>C</b>) A WT flower. (<b>D</b>) A WT ICS. (<b>E</b>) An intact <i>MPF3</i>-VIGS small flower bud. (<b>F</b>) An intact <i>MPF3</i>-VIGS flower bud. (<b>G</b>) An <i>MPF3</i>-VIGS flower. (<b>H</b>) An <i>MPF3</i>-VIGS ICS. (<b>I</b>) An <i>MPF3</i>-RNAi flower. Bars = 1 mm in <b>A</b>, <b>B</b>, <b>C</b>, <b>E</b>, <b>F</b>, <b>G,</b> and <b>I</b>. Bars = 5 mm in <b>D</b> and <b>H</b>. (<b>J</b>) <i>MPF3</i> was silenced using a VIGS approach. <i>MPF3</i> expression was evaluated in five floral organs of VIGS flowers. (<b>K</b>) <i>MPF3</i> was silenced using an RNAi approach. <i>MPF3</i> expression was evaluated in five floral organs of RNAi flowers. Total RNA from the indicated mutated floral organs was subjected to qRT-PCR. Gene expression in pedicels of WT samples were set as 1, and <i>PFACTIN</i> was used as an internal control. The dark gray column stands for the gene expression in WT organs light gray column indicates the gene expression in the organs of the mutants, as indicated. The experiments were repeated with three independent biological samples. Mean expression values and standard deviation are presented.</p>", "links"=>[], "tags"=>["Agricultural biotechnology", "developmental biology", "Plant growth and development", "genetics", "gene expression", "RNA interference", "Gene function", "Plant genetics", "Molecular cell biology", "Signal transduction", "Signaling in selected disciplines", "Developmental signaling", "Plant science", "phenocopies"], "article_id"=>900756, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Ji-Si Zhang", "Jing Zhao", "Shaohua Zhang", "Chaoying He"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085534.g004", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_VIGS_mediated_MPF3_silencing_phenocopies_MPF3_RNAi_/900756", "title"=>"VIGS-mediated <i>MPF3</i> silencing phenocopies <i>MPF3</i>-RNAi.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-14 03:10:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/1346992"], "description"=>"<p>Pedicel cells from the WT (<b>A</b>), <i>MPF2</i>-RNAi (<b>B</b>), <i>MPF2</i>-VIGS (<b>C</b>), <i>MPF3</i>-RNAi (<b>D</b>), and <i>MPF3</i>-VIGS (<b>E</b>). Bars = 50 µm. (<b>F</b>) Quantification of the pedicel size (dark gray column) and the respective pedicel cells lengths (light gray column). The number of pedicels analyzed was 20 for each line above. The numbers of cells analyzed were 60 in WT, <i>MPF2</i>-RNAi and <i>MPF2</i>-VIGS, and 50 in <i>MPF3</i>-RNAi and <i>MPF3</i>-VIGS. Mean values and standard deviation are presented in both cases. Two-tailed <i>t</i>-test significance was given as follows: one star for <i>p</i><0.05, and two stars for <i>p</i><0.01.</p>", "links"=>[], "tags"=>["Agricultural biotechnology", "developmental biology", "Plant growth and development", "genetics", "gene expression", "RNA interference", "Gene function", "Plant genetics", "Molecular cell biology", "Signal transduction", "Signaling in selected disciplines", "Developmental signaling", "Plant science", "pedicel"], "article_id"=>900757, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Ji-Si Zhang", "Jing Zhao", "Shaohua Zhang", "Chaoying He"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085534.g005", "stats"=>{"downloads"=>0, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_MPF3_and_MPF2_regulate_pedicel_development_and_pedicel_cell_length_/900757", "title"=>"<i>MPF3</i> and <i>MPF2</i> regulate pedicel development and pedicel cell length.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-14 03:10:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/1346977"], "description"=>"<p><i>TRV</i> cDNA clones were placed in between duplicated CaMV 35S promoters (2×35 S) and the nopaline synthase terminator (NOSt) in a T-DNA vector <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0085534#pone.0085534-Liu1\" target=\"_blank\">[22]</a>. RdRp: RNA-dependant RNA polymerase; MP: movement protein; 16 K: cysteine rich protein; Rz: self-cleaving ribozyme; CP: coat protein. <i>PfPDS-</i>, <i>MPF2-,</i> and <i>MPF3</i>-specific fragments were inserted separately into <i>TRV</i>2 using <i>Nco</i> I and <i>BamH</i> I restriction sites.</p>", "links"=>[], "tags"=>["Agricultural biotechnology", "developmental biology", "Plant growth and development", "genetics", "gene expression", "RNA interference", "Gene function", "Plant genetics", "Molecular cell biology", "Signal transduction", "Signaling in selected disciplines", "Developmental signaling", "Plant science", "trv-vigs"], "article_id"=>900742, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Ji-Si Zhang", "Jing Zhao", "Shaohua Zhang", "Chaoying He"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085534.g001", "stats"=>{"downloads"=>15, "page_views"=>257, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Organization_of_TRV_VIGS_vectors_/900742", "title"=>"Organization of TRV-VIGS vectors.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-14 03:10:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/1346994"], "description"=>"<div><p>The fruit of <i>Physalis</i> has a berry and a novelty called inflated calyx syndrome (ICS, also named the ‘Chinese lantern’). Elucidation of the underlying developmental mechanisms of fruit diversity demands an efficient gene functional inference platform. Here, we tested the application of the tobacco rattle virus (TRV)-mediated gene-silencing system in <i>Physalis floridana</i>. First, we characterized the putative gene of a phytoene desaturase in <i>P. floridana</i> (<i>PfPDS</i>). Infecting the leaves of the <i>Physalis</i> seedlings with the <i>PfPDS</i>-<i>TRV</i> vector resulted in a bleached plant, including the developing leaves, floral organs, ICS, berry, and seed. These results indicated that a local VIGS treatment can efficiently induce a systemic mutated phenotype. qRT-PCR analyses revealed that the bleaching extent correlated to the mRNA reduction of the endogenous <i>PfPDS</i>. Detailed comparisons of multiple infiltration and growth protocols allowed us to determine the optimal methodologies for VIGS manipulation in <i>Physalis</i>. We subsequently utilized this optimized VIGS methodology to downregulate the expression of two MADS-box genes, <i>MPF2</i> and <i>MPF3</i>, and compared the resulting effects with gene-downregulation mediated by RNA interference (RNAi) methods. The VIGS-mediated gene knockdown plants were found to resemble the mutated phenotypes of floral calyx, fruiting calyx and pollen maturation of the RNAi transgenic plants for both <i>MPF2</i> and <i>MPF3</i>. Moreover, the two MADS-box genes were appeared to have a novel role in the pedicel development in <i>P. floridana</i>. The major advantage of VIGS-based gene knockdown lies in practical aspects of saving time and easy manipulation as compared to the RNAi. Despite the lack of heritability and mosaic mutation phenotypes observed in some organs, the TRV-mediated gene silencing system provides an alternative efficient way to infer gene function in various developmental processes in <i>Physalis</i>, thus facilitating understanding of the genetic basis of the evolution and development of the morphological diversities within the Solanaceae.</p></div>", "links"=>[], "tags"=>["Agricultural biotechnology", "developmental biology", "Plant growth and development", "genetics", "gene expression", "RNA interference", "Gene function", "Plant genetics", "Molecular cell biology", "Signal transduction", "Signaling in selected disciplines", "Developmental signaling", "Plant science", "mediated", "rattle"], "article_id"=>900759, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Ji-Si Zhang", "Jing Zhao", "Shaohua Zhang", "Chaoying He"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085534", "stats"=>{"downloads"=>16, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Efficient_Gene_Silencing_Mediated_by_Tobacco_Rattle_Virus_in_an_Emerging_Model_Plant_Physalis_/900759", "title"=>"Efficient Gene Silencing Mediated by Tobacco Rattle Virus in an Emerging Model Plant <i>Physalis</i>", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-01-14 03:10:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/1346982"], "description"=>"<p>(<b>A</b>) A wild-type seedling of <i>P. floridana</i>. (<b>B</b>) Phenotypic variation in a seedling after <i>PfPDS</i>-<i>TRV2</i> infection for one week. Bars = 5.0 cm. (<b>C</b>) A 3-month old plant infected with <i>PfPDS</i>-<i>TRV2</i>. Bars = 1.5 cm. (<b>D–G</b>) Floral phenotypic variations. In comparison with wild-type floral bud (<b>D</b>) and mature flower (<b>F</b>), the floral bud (<b>E</b>) and mature flower (<b>G</b>) from the <i>PfPDS</i>-<i>TRV2</i> infected plants are bleached. Bars = 10 mm in <b>D</b> and <b>E</b>, and 25 mm in <b>F</b> and <b>G</b>. (<b>H</b>) ICS from wild-type <i>Physalis</i>. (<b>I</b>) Berry from wild-type <i>Physalis</i>. (<b>J</b>) Mosaic bleached ICS. (<b>K</b>) Completely bleached ICS. (<b>L</b>) Bleached berries with different bleaching degrees from the <i>PfPDS</i>-<i>TRV2</i> infected plants. Bars = 50 mm in <b>H</b>, <b>J</b> and <b>K</b>, and 25 mm in <b>I</b> and <b>L</b>. (<b>M</b>) Wild-type seeds. (<b>N</b>) Bleached seeds. Bars = 5 mm. (<b>O</b>) Expressions of <i>PfPDS</i> in the <i>PfPDS</i>-<i>TRV2</i> infected plants. The black column is for the wild type and the other columns are for the <i>PfPDS</i>-<i>TRV2</i> infected plants with different degrees of bleaching. qRT-PCR was performed using total RNA from the organs indicated. <i>PFACTIN</i> was used as an internal control. The experiments were repeated three times using independent biological samples. Mean expression values and standard deviation are presented.</p>", "links"=>[], "tags"=>["Agricultural biotechnology", "developmental biology", "Plant growth and development", "genetics", "gene expression", "RNA interference", "Gene function", "Plant genetics", "Molecular cell biology", "Signal transduction", "Signaling in selected disciplines", "Developmental signaling", "Plant science", "treatments", "induce", "systemic"], "article_id"=>900747, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Ji-Si Zhang", "Jing Zhao", "Shaohua Zhang", "Chaoying He"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085534.g002", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Local_treatments_induce_a_systemic_syndrome_/900747", "title"=>"Local treatments induce a systemic syndrome.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-14 03:10:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/1346993"], "description"=>"<p>Seedling survival and infected efficiency in different treatments.</p>", "links"=>[], "tags"=>["Agricultural biotechnology", "developmental biology", "Plant growth and development", "genetics", "gene expression", "RNA interference", "Gene function", "Plant genetics", "Molecular cell biology", "Signal transduction", "Signaling in selected disciplines", "Developmental signaling", "Plant science", "infected"], "article_id"=>900758, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Ji-Si Zhang", "Jing Zhao", "Shaohua Zhang", "Chaoying He"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085534.t001", "stats"=>{"downloads"=>4, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Seedling_survival_and_infected_efficiency_in_different_treatments_/900758", "title"=>"Seedling survival and infected efficiency in different treatments.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-01-14 03:10:16"}

PMC Usage Stats | Further Information

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Relative Metric

{"start_date"=>"2014-01-01T00:00:00Z", "end_date"=>"2014-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences/Agriculture", "average_usage"=>[282]}, {"subject_area"=>"/Biology and life sciences/Genetics", "average_usage"=>[306, 482]}]}
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