A Type 2C Protein Phosphatase FgPtc3 Is Involved in Cell Wall Integrity, Lipid Metabolism, and Virulence in Fusarium graminearum
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{"title"=>"A type 2C protein phosphatase FgPtc3 is involved in cell wall integrity, lipid metabolism, and virulence in fusarium graminearum", "type"=>"journal", "authors"=>[{"first_name"=>"Jinhua", "last_name"=>"Jiang", "scopus_author_id"=>"55565607600"}, {"first_name"=>"Yingzi", "last_name"=>"Yun", "scopus_author_id"=>"37666430800"}, {"first_name"=>"Qianqian", "last_name"=>"Yang", "scopus_author_id"=>"37025899900"}, {"first_name"=>"Won Bo", "last_name"=>"Shim", "scopus_author_id"=>"56749517100"}, {"first_name"=>"Zhengyi", "last_name"=>"Wang", "scopus_author_id"=>"14020738400"}, {"first_name"=>"Zhonghua", "last_name"=>"Ma", "scopus_author_id"=>"7403600773"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"362648518", "sgr"=>"80053293901", "pmid"=>"21980420", "scopus"=>"2-s2.0-80053293901", "isbn"=>"1932-6203", "doi"=>"10.1371/journal.pone.0025311", "issn"=>"19326203"}, "id"=>"c1731496-b96a-38e6-af3b-2eedd4a10169", "abstract"=>"Type 2C protein phosphatases (PP2Cs) play important roles in regulating many biological processes in eukaryotes. Currently, little is known about functions of PP2Cs in filamentous fungi. The causal agent of wheat head blight, Fusarium graminearum, contains seven putative PP2C genes, FgPTC1, -3, -5, -5R, -6, -7 and -7R. In order to investigate roles of these PP2Cs, we constructed deletion mutants for all seven PP2C genes in this study. The FgPTC3 deletion mutant (ΔFgPtc3-8) exhibited reduced aerial hyphae formation and deoxynivalenol (DON) production, but increased production of conidia. The mutant showed increased resistance to osmotic stress and cell wall-damaging agents on potato dextrose agar plates. Pathogencity assays showed that ΔFgPtc3-8 is unable to infect flowering wheat head. All of the defects were restored when ΔFgPtc3-8 was complemented with the wild-type FgPTC3 gene. Additionally, the FgPTC3 partially rescued growth defect of a yeast PTC1 deletion mutant under various stress conditions. Ultrastructural and histochemical analyses showed that conidia of ΔFgPtc3-8 contained an unusually high number of large lipid droplets. Furthermore, the mutant accumulated a higher basal level of glycerol than the wild-type progenitor. Quantitative real-time PCR assays showed that basal expression of FgOS2, FgSLT2 and FgMKK1 in the mutant was significantly higher than that in the wild-type strain. Serial analysis of gene expression in ΔFgPtc3-8 revealed that FgPTC3 is associated with various metabolic pathways. In contrast to the FgPTC3 mutant, the deletion mutants of FgPTC1, FgPTC5, FgPTC5R, FgPTC6, FgPTC7 or FgPTC7R did not show aberrant phenotypic features when grown on PDA medium or inoculated on wheat head. These results indicate FgPtc3 is the key PP2C that plays a critical role in a variety of cellular and biological functions, including cell wall integrity, lipid and secondary metabolisms, and virulence in F. graminearum.", "link"=>"http://www.mendeley.com/research/type-2c-protein-phosphatase-fgptc3-involved-cell-wall-integrity-lipid-metabolism-virulence-fusarium", "reader_count"=>24, "reader_count_by_academic_status"=>{"Librarian"=>1, "Researcher"=>9, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>7, "Student > Postgraduate"=>1, "Student > Master"=>1, "Student > Bachelor"=>3, "Professor"=>1}, "reader_count_by_user_role"=>{"Librarian"=>1, "Researcher"=>9, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>7, "Student > Postgraduate"=>1, "Student > Master"=>1, "Student > Bachelor"=>3, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>3, "Agricultural and Biological Sciences"=>16, "Business, Management and Accounting"=>1, "Psychology"=>1, "Social Sciences"=>1}, "reader_count_by_subdiscipline"=>{"Social Sciences"=>{"Social Sciences"=>1}, "Psychology"=>{"Psychology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>16}, "Business, Management and Accounting"=>{"Business, Management and Accounting"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>2}}, "reader_count_by_country"=>{"Austria"=>1, "Italy"=>1}, "group_count"=>3}

Scopus | Further Information

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Figshare

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  • {"files"=>["https://ndownloader.figshare.com/files/730517"], "description"=>"<p>Wheat heads were point-inoculated with conidial suspension of each strain, and infected wheat heads were examined 15 days after inoculation.</p>", "links"=>[], "tags"=>["mutant"], "article_id"=>400877, "categories"=>["Genetics", "Microbiology", "Plant Biology"], "users"=>["Jinhua Jiang", "Yingzi Yun", "Qianqian Yang", "Won-Bo Shim", "Zhengyi Wang", "Zhonghua Ma"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025311.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Virulence_of_PH_1_the_mutant_916_FgPtc3_8_916_FgPtc13_6_and_916_FgPtc3_8C_on_wheat_heads_/400877", "title"=>"Virulence of PH-1, the mutant ΔFgPtc3-8, ΔFgPtc13-6 and ΔFgPtc3-8C on wheat heads.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-28 00:14:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/731578"], "description"=>"<p>The primary structures of PP2C genes from <i>F. graminearum</i>.</p>", "links"=>[], "tags"=>["structures", "pp2c", "genes"], "article_id"=>401932, "categories"=>["Genetics", "Microbiology", "Plant Biology"], "users"=>["Jinhua Jiang", "Yingzi Yun", "Qianqian Yang", "Won-Bo Shim", "Zhengyi Wang", "Zhonghua Ma"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025311.t001", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_primary_structures_of_PP2C_genes_from_F_graminearum_/401932", "title"=>"The primary structures of PP2C genes from <i>F. graminearum</i>.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-09-28 00:32:12"}
  • {"files"=>["https://ndownloader.figshare.com/files/731188"], "description"=>"<p>RNA samples were extracted from mycelia of each strain after grown in potato dextrose broth for 2 days. The relative expression of <i>FgSLT1</i> and <i>FgMKK1</i> in ΔFgPtc3-8 is the relative amount of mRNA of each gene in the wild-type strain. Line bars in each column denote standard errors of three experiments.</p>", "links"=>[], "tags"=>["levels", "ph-1", "mutant"], "article_id"=>401545, "categories"=>["Genetics", "Microbiology", "Plant Biology"], "users"=>["Jinhua Jiang", "Yingzi Yun", "Qianqian Yang", "Won-Bo Shim", "Zhengyi Wang", "Zhonghua Ma"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025311.g010", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Relative_expression_levels_of_FgSLT1_and_FgMKK1_in_PH_1_and_mutant_FgPtc3_8_/401545", "title"=>"Relative expression levels of <i>FgSLT1</i> and <i>FgMKK1</i> in PH-1 and mutant ΔFgPtc3-8.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-28 00:25:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/369360", "https://ndownloader.figshare.com/files/369392", "https://ndownloader.figshare.com/files/369444", "https://ndownloader.figshare.com/files/369471", "https://ndownloader.figshare.com/files/369499", "https://ndownloader.figshare.com/files/369529", "https://ndownloader.figshare.com/files/369611", "https://ndownloader.figshare.com/files/369705"], "description"=>"<div><p>Type 2C protein phosphatases (PP2Cs) play important roles in regulating many biological processes in eukaryotes. Currently, little is known about functions of PP2Cs in filamentous fungi. The causal agent of wheat head blight, <em>Fusarium graminearum</em>, contains seven putative PP2C genes, <em>FgPTC1</em>, -<em>3</em>, -<em>5</em>, -<em>5R</em>, -<em>6</em>, -<em>7</em> and -<em>7R</em>. In order to investigate roles of these PP2Cs, we constructed deletion mutants for all seven PP2C genes in this study. The <em>FgPTC3</em> deletion mutant (ΔFgPtc3-8) exhibited reduced aerial hyphae formation and deoxynivalenol (DON) production, but increased production of conidia. The mutant showed increased resistance to osmotic stress and cell wall-damaging agents on potato dextrose agar plates. Pathogencity assays showed that ΔFgPtc3-8 is unable to infect flowering wheat head. All of the defects were restored when ΔFgPtc3-8 was complemented with the wild-type <em>FgPTC3</em> gene. Additionally, the <em>FgPTC3</em> partially rescued growth defect of a yeast <em>PTC1</em> deletion mutant under various stress conditions. Ultrastructural and histochemical analyses showed that conidia of ΔFgPtc3-8 contained an unusually high number of large lipid droplets. Furthermore, the mutant accumulated a higher basal level of glycerol than the wild-type progenitor. Quantitative real-time PCR assays showed that basal expression of <em>FgOS2</em>, <em>FgSLT2</em> and <em>FgMKK1</em> in the mutant was significantly higher than that in the wild-type strain. Serial analysis of gene expression in ΔFgPtc3-8 revealed that <em>FgPTC3</em> is associated with various metabolic pathways. In contrast to the <em>FgPTC3</em> mutant, the deletion mutants of <em>FgPTC1</em>, <em>FgPTC5</em>, <em>FgPTC5R</em>, <em>FgPTC6</em>, <em>FgPTC7</em> or <em>FgPTC7R</em> did not show aberrant phenotypic features when grown on PDA medium or inoculated on wheat head. These results indicate FgPtc3 is the key PP2C that plays a critical role in a variety of cellular and biological functions, including cell wall integrity, lipid and secondary metabolisms, and virulence in <em>F. graminearum</em>.</p> </div>", "links"=>[], "tags"=>["2c", "phosphatase", "fgptc3", "lipid", "virulence"], "article_id"=>132986, "categories"=>["Genetics", "Microbiology", "Cell Biology"], "users"=>["Jinhua Jiang", "Yingzi Yun", "Qianqian Yang", "Won-Bo Shim", "Zhengyi Wang", "Zhonghua Ma"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0025311.s001", "https://dx.doi.org/10.1371/journal.pone.0025311.s002", "https://dx.doi.org/10.1371/journal.pone.0025311.s003", "https://dx.doi.org/10.1371/journal.pone.0025311.s004", "https://dx.doi.org/10.1371/journal.pone.0025311.s005", "https://dx.doi.org/10.1371/journal.pone.0025311.s006", "https://dx.doi.org/10.1371/journal.pone.0025311.s007", "https://dx.doi.org/10.1371/journal.pone.0025311.s008"], "stats"=>{"downloads"=>8, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/A_Type_2C_Protein_Phosphatase_FgPtc3_Is_Involved_in_Cell_Wall_Integrity_Lipid_Metabolism_and_Virulence_in_Fusarium_graminearum_/132986", "title"=>"A Type 2C Protein Phosphatase FgPtc3 Is Involved in Cell Wall Integrity, Lipid Metabolism, and Virulence in <em>Fusarium graminearum</em>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-09-28 00:49:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/731416"], "description"=>"<p>(<b>A</b>) 1369 genes up-regulated more than 5 folds in the mutant ΔFgPtc3-8 compared with wild-type PH-1. (<b>B</b>) 410 genes down-regulated more than 5 folds in the mutant ΔFgPtc3-8 compared with wild-type PH-1. The expressions of genes were detected by the serial analysis of gene expression method.</p>", "links"=>[], "tags"=>["grouping", "genes", "up-", "down-regulated", "compared"], "article_id"=>401767, "categories"=>["Genetics", "Microbiology", "Plant Biology"], "users"=>["Jinhua Jiang", "Yingzi Yun", "Qianqian Yang", "Won-Bo Shim", "Zhengyi Wang", "Zhonghua Ma"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025311.g012", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Pie_chart_grouping_the_genes_up_and_down_regulated_in_expression_in_916_FgPtc3_8_compared_with_PH_1_/401767", "title"=>"Pie chart grouping the genes up- and down-regulated in expression in ΔFgPtc3-8 compared with PH-1.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-28 00:29:27"}
  • {"files"=>["https://ndownloader.figshare.com/files/730643"], "description"=>"<p>Amount of DON (per mg fungal DNA) produced by the wild type PH-1, the mutants ΔFgPtc3-8, ΔFgPtc13-6, or ΔFgPtc3-8C were detected in infected wheat kernels after 20 days of incubation. Line bars in each column denote standard errors of three experiments.</p>", "links"=>[], "tags"=>["fgptc3", "biosynthesis"], "article_id"=>401000, "categories"=>["Genetics", "Microbiology", "Plant Biology"], "users"=>["Jinhua Jiang", "Yingzi Yun", "Qianqian Yang", "Won-Bo Shim", "Zhengyi Wang", "Zhonghua Ma"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025311.g005", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effects_of_FgPtc3_on_the_biosynthesis_of_DON_/401000", "title"=>"Effects of FgPtc3 on the biosynthesis of DON.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-28 00:16:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/730166"], "description"=>"<p>The wild-type strain PH-1, the mutant ΔFgPtc1-5, ΔFgPtc3-8, ΔFgPtc13-6, ΔFgPtc3-8C, ΔFgPtc5-5, ΔFgPtc5R-2, ΔFgPtc6-9, ΔFgPtc7-3 and ΔFgPtc7R-2 were grown on PDA for 4 days at 25°C.</p>", "links"=>[], "tags"=>["morphology", "pigment"], "article_id"=>400514, "categories"=>["Genetics", "Microbiology", "Plant Biology"], "users"=>["Jinhua Jiang", "Yingzi Yun", "Qianqian Yang", "Won-Bo Shim", "Zhengyi Wang", "Zhonghua Ma"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025311.g001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Impact_of_FgPTC3_on_colony_morphology_and_pigment_formation_/400514", "title"=>"Impact of <i>FgPTC3</i> on colony morphology and pigment formation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-28 00:08:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/730962"], "description"=>"<p>Intracellular glycerol concentration [nmol/mg dried mycelia] in mycelia of the wild-type strain PH-1, and the mutant ΔFgPtc3-8, ΔFgPtc13-6, ΔFgPtc3-8C and ΔFgOs2-4 were analyzed after 2 h of 1.2 M NaCl treatment. Bars denote standard errors from three repeated experiments.</p>", "links"=>[], "tags"=>["fgptc3", "fgos2", "glycerol"], "article_id"=>401315, "categories"=>["Genetics", "Microbiology", "Plant Biology"], "users"=>["Jinhua Jiang", "Yingzi Yun", "Qianqian Yang", "Won-Bo Shim", "Zhengyi Wang", "Zhonghua Ma"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025311.g008", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effects_of_FgPtc3_and_FgOs2_on_the_glycerol_biosynthesis_/401315", "title"=>"Effects of FgPtc3 and FgOs2 on the glycerol biosynthesis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-28 00:21:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/730368"], "description"=>"<p>(A) Lipid drops within conidia of the wild type PH-1 and the mutant <b>Δ</b>FgPtc3-8 examined with a transmission electronic microscope. (B) Lipid drops in conidium [top] and germinating conidium [middle] and hyphae [bottom] were stained with Nile Red and examined under a microscope with episcopic fluorescence.</p>", "links"=>[], "tags"=>["histochemical", "analyses", "lipid", "droplets", "conidia", "mutant"], "article_id"=>400721, "categories"=>["Genetics", "Microbiology", "Plant Biology"], "users"=>["Jinhua Jiang", "Yingzi Yun", "Qianqian Yang", "Won-Bo Shim", "Zhengyi Wang", "Zhonghua Ma"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025311.g003", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Ultrastructural_and_histochemical_analyses_of_lipid_droplets_within_conidia_of_mutant_916_FgPtc3_8_/400721", "title"=>"Ultrastructural and histochemical analyses of lipid droplets within conidia of mutant ΔFgPtc3-8.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-28 00:12:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/731313"], "description"=>"<p>The yeast <i>PTC1</i> mutant was complemented with <i>FgPTC3</i> to generate the strain BY4741ΔPTC1 + pYES2-FgPTC3. The wild type strain BY4741 and <i>PTC1</i> mutant BY4741ΔPTC1 transformed with empty pYES2 vector were used as controls. Different dilutions of cell suspension of each strain were spotted on SG plates under different stresses. After incubated at 30°C [or 37°C as indicated] for four days, growth of each strain on each plate was examined.</p>", "links"=>[], "tags"=>["fgptc3", "complements", "cerevisiae"], "article_id"=>401666, "categories"=>["Genetics", "Microbiology", "Plant Biology"], "users"=>["Jinhua Jiang", "Yingzi Yun", "Qianqian Yang", "Won-Bo Shim", "Zhengyi Wang", "Zhonghua Ma"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025311.g011", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_F_graminearum_FgPtc3_complements_the_S_cerevisiae_PTC1_mutant_/401666", "title"=>"<i>F. graminearum</i> FgPtc3 complements the <i>S. cerevisiae PTC1</i> mutant.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-28 00:27:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/730882"], "description"=>"<p>RNA samples were extracted from mycelia of each strain untreated or treated with 1.2 M NaCl or 0.2 M LiCl for 2 hours after grown in potato dextrose broth for 2 days. The relative expression of <i>FgOS2</i> in the wild-type strain or ΔFgPtc3-8 is the relative amount of mRNA of each gene in the wild-type strain without treatment. Line bars in each column denote standard errors of three experiments.</p>", "links"=>[], "tags"=>["levels", "wild-type", "ph-1", "mutant"], "article_id"=>401231, "categories"=>["Genetics", "Microbiology", "Plant Biology"], "users"=>["Jinhua Jiang", "Yingzi Yun", "Qianqian Yang", "Won-Bo Shim", "Zhengyi Wang", "Zhonghua Ma"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025311.g007", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Relative_expression_levels_of_FgOS2_in_the_wild_type_strain_PH_1_and_the_mutant_FgPtc3_8_/401231", "title"=>"Relative expression levels of <i>FgOS2</i> in the wild-type strain PH-1 and the mutant ΔFgPtc3-8.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-28 00:20:31"}
  • {"files"=>["https://ndownloader.figshare.com/files/730762"], "description"=>"<p>(A) Osmotic stresses were mediated by addition of NaCl or KCl in potato dextrose agar [PDA] medium. (B) Metal cations were added into minimal medium [MM]. Bars denote standard errors from three repeated experiments.</p>", "links"=>[], "tags"=>["osmotic", "stresses", "cations"], "article_id"=>401122, "categories"=>["Genetics", "Microbiology", "Plant Biology"], "users"=>["Jinhua Jiang", "Yingzi Yun", "Qianqian Yang", "Won-Bo Shim", "Zhengyi Wang", "Zhonghua Ma"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025311.g006", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sensitivity_to_osmotic_stresses_and_metal_cations_of_PH_1_916_FgPtc3_8_916_FgPtc13_6_916_FgPtc3_8C_and_916_FgOs2_4_/401122", "title"=>"Sensitivity to osmotic stresses and metal cations of PH-1, ΔFgPtc3-8, ΔFgPtc13-6, ΔFgPtc3-8C, and ΔFgOs2-4.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-28 00:18:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/730230"], "description"=>"<p>(A) Conidia were accounted after incubation of the wild-type strain PH-1, the mutant ΔFgPtc3-8, ΔFgPtc13-6, or ΔFgPtc3-8C in mung bean liquid medium for 4 days. Blank bars with the same letter are not significantly different at <i>P</i> = 0.05 (ANOVA of SAS). (B) Differential interference contrast [DIC] images of conidia were captured with an electronic microscope.</p>", "links"=>[], "tags"=>["conidiation"], "article_id"=>400586, "categories"=>["Genetics", "Microbiology", "Plant Biology"], "users"=>["Jinhua Jiang", "Yingzi Yun", "Qianqian Yang", "Won-Bo Shim", "Zhengyi Wang", "Zhonghua Ma"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025311.g002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Impact_of_FgPTC3_on_conidiation_of_F_graminearum_/400586", "title"=>"Impact of <i>FgPTC3</i> on conidiation of <i>F. graminearum</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-28 00:09:46"}

PMC Usage Stats | Further Information

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Relative Metric

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Net::HTTPTooManyRequests

Source
Scopus
Time
2019-08-27 20:08:34 UTC
Target URL
https://api.elsevier.com/content/search/index:SCOPUS?query=DOI(10.1371%2Fjournal.pone.0025311)
Trace

/app/models/concerns/networkable.rb:21:in `get_result'
/app/models/source.rb:165:in `get_data'
/app/models/retrieval_status.rb:47:in `perform_get_data'
/app/jobs/source_job.rb:52:in `block (2 levels) in perform'
/app/jobs/source_job.rb:51:in `block in perform'
/app/jobs/source_job.rb:35:in `each'
/app/jobs/source_job.rb:35:in `perform'