Long-Distance Translocation of Protein during Morphogenesis of the Fruiting Body in the Filamentous Fungus, Agaricus bisporus
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{"title"=>"Long-distance translocation of protein during morphogenesis of the fruiting body in the filamentous fungus, agaricus bisporus", "type"=>"journal", "authors"=>[{"first_name"=>"Benjamin M.", "last_name"=>"Woolston", "scopus_author_id"=>"54418136500"}, {"first_name"=>"Carl", "last_name"=>"Schlagnhaufer", "scopus_author_id"=>"6602666073"}, {"first_name"=>"Jack", "last_name"=>"Wilkinson", "scopus_author_id"=>"57197464707"}, {"first_name"=>"Jeffrey", "last_name"=>"Larsen", "scopus_author_id"=>"8139191600"}, {"first_name"=>"Zhixin", "last_name"=>"Shi", "scopus_author_id"=>"55468489200"}, {"first_name"=>"Kimberly M.", "last_name"=>"Mayer", "scopus_author_id"=>"55186193900"}, {"first_name"=>"Donald S.", "last_name"=>"Walters", "scopus_author_id"=>"54792363000"}, {"first_name"=>"Wayne R.", "last_name"=>"Curtis", "scopus_author_id"=>"7005160339"}, {"first_name"=>"C. Peter", "last_name"=>"Romaine", "scopus_author_id"=>"55954498300"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "scopus"=>"2-s2.0-82755186961", "sgr"=>"82755186961", "pui"=>"363035579", "pmid"=>"22163014", "doi"=>"10.1371/journal.pone.0028412"}, "id"=>"bbd659bc-2f08-3db6-bc59-e1e71932640e", "abstract"=>"Commercial cultivation of the mushroom fungus, Agaricus bisporus, utilizes a substrate consisting of a lower layer of compost and upper layer of peat. Typically, the two layers are seeded with individual mycelial inoculants representing a single genotype of A. bisporus. Studies aimed at examining the potential of this fungal species as a heterologous protein expression system have revealed unexpected contributions of the mycelial inoculants in the morphogenesis of the fruiting body. These contributions were elucidated using a dual-inoculant method whereby the two layers were differientially inoculated with transgenic β-glucuronidase (GUS) and wild-type (WT) lines. Surprisingly, use of a transgenic GUS line in the lower substrate and a WT line in the upper substrate yielded fruiting bodies expressing GUS activity while lacking the GUS transgene. Results of PCR and RT-PCR analyses for the GUS transgene and RNA transcript, respectively, suggested translocation of the GUS protein from the transgenic mycelium colonizing the lower layer into the fruiting body that developed exclusively from WT mycelium colonizing the upper layer. Effective translocation of the GUS protein depended on the use of a transgenic line in the lower layer in which the GUS gene was controlled by a vegetative mycelium-active promoter (laccase 2 and β-actin), rather than a fruiting body-active promoter (hydrophobin A). GUS-expressing fruiting bodies lacking the GUS gene had a bonafide WT genotype, confirmed by the absence of stably inherited GUS and hygromycin phosphotransferase selectable marker activities in their derived basidiospores and mycelial tissue cultures. Differientially inoculating the two substrate layers with individual lines carrying the GUS gene controlled by different tissue-preferred promoters resulted in up to a ∼3.5-fold increase in GUS activity over that obtained with a single inoculant. Our findings support the existence of a previously undescribed phenomenon of long-distance protein translocation in A. bisporus that has potential application in recombinant protein expression and biotechnological approaches for crop improvement.", "link"=>"http://www.mendeley.com/research/longdistance-translocation-protein-during-morphogenesis-fruiting-body-filamentous-fungus-agaricus-bi", "reader_count"=>25, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Researcher"=>9, "Student > Ph. D. Student"=>7, "Student > Master"=>1, "Other"=>1, "Student > Bachelor"=>3, "Professor"=>3}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Researcher"=>9, "Student > Ph. D. Student"=>7, "Student > Master"=>1, "Other"=>1, "Student > Bachelor"=>3, "Professor"=>3}, "reader_count_by_subject_area"=>{"Engineering"=>2, "Unspecified"=>3, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>2, "Agricultural and Biological Sciences"=>13, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Chemical Engineering"=>2, "Computer Science"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>13}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}, "Unspecified"=>{"Unspecified"=>3}, "Environmental Science"=>{"Environmental Science"=>1}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}, "Chemical Engineering"=>{"Chemical Engineering"=>2}}, "reader_count_by_country"=>{"Netherlands"=>2, "United States"=>3}, "group_count"=>2}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/705325"], "description"=>"<p>Indicated is the upper layer inoculant/lower layer inoculant for the bi-layered cultivation substrate. WT: wild-type line; GUS lines carrying the hydrophobin A promoter (HGS), laccase 2 promoter (LGS) and β-actin promoter (AGS). (A–D) Line HGS. (E–H) Line LGS. (I–L) Line AGS. (A, E, I) Histological GUS assay. (B, F, J) Quantitative GUS assay. Enzyme activity is expressed as nmol MUG hydrolyzed/minute/100 µg total soluble protein, and represents the mean value of two independent experiments. (C, G, K) PCR analysis of the <i>GUS</i> gene. The predicted 163-bp <i>GUS</i> amplicon (<i>GUS</i>) and 403-bp amplicon for the endogenous polyphenol oxidase 1 (<i>PPO</i>) gene, included as a PCR control, are indicated. (D, H, L) RT-PCR analysis of the <i>GUS</i> transcript. Indicated are the predicted 163-bp and 403-bp amplicons for the <i>GUS</i> transcript and endogenous <i>PPO</i> transcript control, respectively.</p>", "links"=>[], "tags"=>["assay", "molecular", "analyses", "fruiting", "bodies", "grown", "wild-type", "transgenic"], "article_id"=>375670, "categories"=>["Biotechnology", "Microbiology"], "users"=>["Benjamin M. Woolston", "Carl Schlagnhaufer", "Jack Wilkinson", "Jeffrey Larsen", "Zhixin Shi", "Kimberly M. Mayer", "Donald S. Walters", "Wayne R. Curtis", "C. Peter Romaine"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0028412.g002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_GUS_activity_assay_and_molecular_analyses_of_fruiting_bodies_grown_using_wild_type_and_transgenic_inoculants_/375670", "title"=>"GUS activity assay and molecular analyses of fruiting bodies grown using wild-type and transgenic inoculants.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-12-06 01:34:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/705665"], "description"=>"a<p>WT: wild-type line; GUS lines carrying the hydrophobin A promoter (HGS) and laccase 2 promoter (LGS); 3 and 412 denote independent transformants.</p>b<p>nmol MUG hydrolyzed/minute/100 µg total soluble protein.</p>c<p>Both upper and lower layers were inoculated with the indicated line.</p>d<p>Upper layer was inoculated with the indicated line and lower layer with a WT line.</p>e<p>Value represents the mean, where n = 2; (range).</p>", "links"=>[], "tags"=>["gus", "assay", "fruiting", "bodies", "grown", "wild-type", "transgenic"], "article_id"=>376011, "categories"=>["Biotechnology", "Microbiology"], "users"=>["Benjamin M. Woolston", "Carl Schlagnhaufer", "Jack Wilkinson", "Jeffrey Larsen", "Zhixin Shi", "Kimberly M. Mayer", "Donald S. Walters", "Wayne R. Curtis", "C. Peter Romaine"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0028412.t002", "stats"=>{"downloads"=>1, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Quantitative_GUS_activity_assay_of_fruiting_bodies_grown_using_wild_type_and_transgenic_inoculants_/376011", "title"=>"Quantitative GUS activity assay of fruiting bodies grown using wild-type and transgenic inoculants.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-12-06 01:40:11"}
  • {"files"=>["https://ndownloader.figshare.com/files/705566"], "description"=>"a<p>Promoter used to drive expression of the <i>GUS</i> gene.</p>b<p>Transcriptomic data represent the expression of each gene relative to the other 10,413 genes in the <i>A. bisporus</i> genome.</p>c<p>The ratio is calculated from the raw expression data and not from the rank.</p>", "links"=>[], "tags"=>["gus", "lines"], "article_id"=>375923, "categories"=>["Biotechnology", "Microbiology"], "users"=>["Benjamin M. Woolston", "Carl Schlagnhaufer", "Jack Wilkinson", "Jeffrey Larsen", "Zhixin Shi", "Kimberly M. Mayer", "Donald S. Walters", "Wayne R. Curtis", "C. Peter Romaine"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0028412.t001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Summary_of_the_GUS_lines_used_in_the_present_study_/375923", "title"=>"Summary of the GUS lines used in the present study.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-12-06 01:38:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/705187"], "description"=>"<p>(A) Cross-section of the bi-layered cultivation substrate for <i>Agaricus bisporus</i> showing the lower bed of compost (Lower Layer) and peat overlay (Upper Layer). Cellular fusion of the mycelia growing in the peat and compost occurs at the interface of the two layers (dashed line), forming a singular network throughout the cultivation substrate. (B) Notation system for dual-inoculant treatments shown in Fig. 1C. (C) GUS activity in fruiting bodies grown using wild-type and transgenic inoculants. WT: wild-type line; GUS lines carrying the hydrophobin A promoter (HGS) and laccase 2 promoter (LGS); 3 and 412 denote independent transformants.</p>", "links"=>[], "tags"=>["microbiology", "biotechnology"], "article_id"=>375541, "categories"=>["Biotechnology", "Microbiology"], "users"=>["Benjamin M. Woolston", "Carl Schlagnhaufer", "Jack Wilkinson", "Jeffrey Larsen", "Zhixin Shi", "Kimberly M. Mayer", "Donald S. Walters", "Wayne R. Curtis", "C. Peter Romaine"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0028412.g001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Dual_inoculant_method_/375541", "title"=>"Dual-inoculant method.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-12-06 01:32:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/358410", "https://ndownloader.figshare.com/files/358435", "https://ndownloader.figshare.com/files/358465", "https://ndownloader.figshare.com/files/358503"], "description"=>"<div><p>Commercial cultivation of the mushroom fungus, <em>Agaricus bisporus</em>, utilizes a substrate consisting of a lower layer of compost and upper layer of peat. Typically, the two layers are seeded with individual mycelial inoculants representing a single genotype of <em>A. bisporus</em>. Studies aimed at examining the potential of this fungal species as a heterologous protein expression system have revealed unexpected contributions of the mycelial inoculants in the morphogenesis of the fruiting body. These contributions were elucidated using a dual-inoculant method whereby the two layers were differientially inoculated with transgenic β-glucuronidase (GUS) and wild-type (WT) lines. Surprisingly, use of a transgenic GUS line in the lower substrate and a WT line in the upper substrate yielded fruiting bodies expressing GUS activity while lacking the <em>GUS</em> transgene. Results of PCR and RT-PCR analyses for the <em>GUS</em> transgene and RNA transcript, respectively, suggested translocation of the GUS protein from the transgenic mycelium colonizing the lower layer into the fruiting body that developed exclusively from WT mycelium colonizing the upper layer. Effective translocation of the GUS protein depended on the use of a transgenic line in the lower layer in which the <em>GUS</em> gene was controlled by a vegetative mycelium-active promoter (laccase 2 and β-actin), rather than a fruiting body-active promoter (hydrophobin A). GUS-expressing fruiting bodies lacking the <em>GUS</em> gene had a bonafide WT genotype, confirmed by the absence of stably inherited GUS and hygromycin phosphotransferase selectable marker activities in their derived basidiospores and mycelial tissue cultures. Differientially inoculating the two substrate layers with individual lines carrying the <em>GUS</em> gene controlled by different tissue-preferred promoters resulted in up to a ∼3.5-fold increase in GUS activity over that obtained with a single inoculant. Our findings support the existence of a previously undescribed phenomenon of long-distance protein translocation in <em>A. bisporus</em> that has potential application in recombinant protein expression and biotechnological approaches for crop improvement.</p> </div>", "links"=>[], "tags"=>["long-distance", "translocation", "morphogenesis", "fruiting", "filamentous"], "article_id"=>130838, "categories"=>["Biotechnology", "Microbiology"], "users"=>["Benjamin M. Woolston", "Carl Schlagnhaufer", "Jack Wilkinson", "Jeffrey Larsen", "Zhixin Shi", "Kimberly M. Mayer", "Donald S. Walters", "Wayne R. Curtis", "C. Peter Romaine"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0028412.s001", "https://dx.doi.org/10.1371/journal.pone.0028412.s002", "https://dx.doi.org/10.1371/journal.pone.0028412.s003", "https://dx.doi.org/10.1371/journal.pone.0028412.s004"], "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Long_Distance_Translocation_of_Protein_during_Morphogenesis_of_the_Fruiting_Body_in_the_Filamentous_Fungus_Agaricus_bisporus_/130838", "title"=>"Long-Distance Translocation of Protein during Morphogenesis of the Fruiting Body in the Filamentous Fungus, <em>Agaricus bisporus</em>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-12-06 00:13:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/705417"], "description"=>"<p>Indicated is the upper layer inoculant/lower layer inoculant for the bi-layered cultivation substrate. WT: wild-type line; LGS: GUS line carrying the laccase 2 promoter. (A) Histological GUS assay and (B) <i>GUS</i>-PCR analysis of fruiting bodies. The presence (+) or absence (-) of the <i>GUS</i> gene is indicated. Mycelial tissue cultures derived from the indicated fruiting bodies were analyzed for: (C) GUS activity by histological assay and (D) Hyrgromycin phosphotransferase (HPT) activity. Hygromycin B resistance was assessed by growth on malt extract agar (MEA) without (- Hyg) and with (+ Hyg) 50 mg l<sup>−1</sup> hygromycin B. Inserts 1 and 2: higher magnification of the fruiting body tissue discs indicated by the arrows.</p>", "links"=>[], "tags"=>["hpt", "assay", "mycelial", "cultures", "derived", "fruiting"], "article_id"=>375767, "categories"=>["Biotechnology", "Microbiology"], "users"=>["Benjamin M. Woolston", "Carl Schlagnhaufer", "Jack Wilkinson", "Jeffrey Larsen", "Zhixin Shi", "Kimberly M. Mayer", "Donald S. Walters", "Wayne R. Curtis", "C. Peter Romaine"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0028412.g003", "stats"=>{"downloads"=>1, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_GUS_and_HPT_activity_assay_of_mycelial_cultures_derived_from_fruiting_body_tissue_/375767", "title"=>"GUS and HPT activity assay of mycelial cultures derived from fruiting body tissue.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-12-06 01:36:07"}
  • {"files"=>["https://ndownloader.figshare.com/files/705609"], "description"=>"a<p>WT: wild-type line; GUS lines carrying the hydrophobin A promoter (HGS) and laccase 2 promoter (LGS); 3 and 412 denote independent transformants.</p>b<p>Value represents the mean normalized to the endogenous β-actin gene, where n = 3; (s.d.).</p>", "links"=>[], "tags"=>["fruiting", "bodies", "grown", "wild-type", "transgenic"], "article_id"=>375962, "categories"=>["Biotechnology", "Microbiology"], "users"=>["Benjamin M. Woolston", "Carl Schlagnhaufer", "Jack Wilkinson", "Jeffrey Larsen", "Zhixin Shi", "Kimberly M. Mayer", "Donald S. Walters", "Wayne R. Curtis", "C. Peter Romaine"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0028412.t003", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_qPCR_analysis_of_the_GUS_gene_in_fruiting_bodies_grown_using_wild_type_and_transgenic_inoculants_/375962", "title"=>"qPCR analysis of the <i>GUS</i> gene in fruiting bodies grown using wild-type and transgenic inoculants.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-12-06 01:39:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/705506"], "description"=>"<p>Shown is the GUS activity in fruiting bodies grown using single-transgenic inoculant and dual-transgenic inoculant strategies. Indicated is the upper layer inoculant/lower layer inoculant for the bi-layered cultivation substrate. The single-inoculant treatment employed a line carrying a fruiting body-active promoter, either HGS (hydrophobin A promoter), LnGS (lectin promoter), or DGS (fruiting body-specific D promoter), as the inoculant for both layers. For the dual-inoculant treatment, the aforementioned lines were used as the upper-layer inoculants and individually paired with line LGS carrying the strong vegetative mycelium promoter, laccase 2, as the inoculant for the lower layer. GUS activity is expressed as nmol MUG hydrolyzed/minute/100 µg total soluble protein, and represents the mean value of two independent experiments. GUS activity for inoculant treatment WT/LGS = 3.77.</p>", "links"=>[], "tags"=>["translocation", "recombinant"], "article_id"=>375862, "categories"=>["Biotechnology", "Microbiology"], "users"=>["Benjamin M. Woolston", "Carl Schlagnhaufer", "Jack Wilkinson", "Jeffrey Larsen", "Zhixin Shi", "Kimberly M. Mayer", "Donald S. Walters", "Wayne R. Curtis", "C. Peter Romaine"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0028412.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Use_of_protein_translocation_for_increased_recombinant_protein_production_/375862", "title"=>"Use of protein translocation for increased recombinant protein production.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-12-06 01:37:42"}

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Relative Metric

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