Compatibility in the Ustilago maydis–Maize Interaction Requires Inhibition of Host Cysteine Proteases by the Fungal Effector Pit2
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{"title"=>"Compatibility in the Ustilago maydis-Maize Interaction Requires Inhibition of Host Cysteine Proteases by the Fungal Effector Pit2", "type"=>"journal", "authors"=>[{"first_name"=>"André N.", "last_name"=>"Mueller", "scopus_author_id"=>"55453842100"}, {"first_name"=>"Sebastian", "last_name"=>"Ziemann", "scopus_author_id"=>"55618049100"}, {"first_name"=>"Steffi", "last_name"=>"Treitschke", "scopus_author_id"=>"37032193300"}, {"first_name"=>"Daniela", "last_name"=>"Aßmann", "scopus_author_id"=>"12806152500"}, {"first_name"=>"Gunther", "last_name"=>"Doehlemann", "scopus_author_id"=>"8574720000"}], "year"=>2013, "source"=>"PLoS Pathogens", "identifiers"=>{"isbn"=>"1553-7374 (Electronic)\\r1553-7366 (Linking)", "sgr"=>"84874787430", "scopus"=>"2-s2.0-84874787430", "issn"=>"15537366", "pui"=>"368489991", "doi"=>"10.1371/journal.ppat.1003177", "pmid"=>"23459172"}, "id"=>"c4fd318f-0332-3aa7-95ee-efc2e04c3ae4", "abstract"=>"The basidiomycete Ustilago maydis causes smut disease in maize, with large plant tumors being formed as the most prominent disease symptoms. During all steps of infection, U. maydis depends on a biotrophic interaction, which requires an efficient suppression of plant immunity. In a previous study, we identified the secreted effector protein Pit2, which is essential for maintenance of biotrophy and induction of tumors. Deletion mutants for pit2 successfully penetrate host cells but elicit various defense responses, which stops further fungal proliferation. We now show that Pit2 functions as an inhibitor of a set of apoplastic maize cysteine proteases, whose activity is directly linked with salicylic-acid-associated plant defenses. Consequently, protease inhibition by Pit2 is required for U. maydis virulence. Sequence comparisons with Pit2 orthologs from related smut fungi identified a conserved sequence motif. Mutation of this sequence caused loss of Pit2 function. Consequently, expression of the mutated protein in U. maydis could not restore virulence of the pit2 deletion mutant, indicating that the protease inhibition by Pit2 is essential for fungal virulence. Moreover, synthetic peptides of the conserved sequence motif showed full activity as protease inhibitor, which identifies this domain as a new, minimal protease inhibitor domain in plant-pathogenic fungi.", "link"=>"http://www.mendeley.com/research/compatibility-ustilago-maydismaize-interaction-requires-inhibition-host-cysteine-proteases-fungal-ef", "reader_count"=>111, "reader_count_by_academic_status"=>{"Unspecified"=>3, "Professor > Associate Professor"=>3, "Researcher"=>19, "Student > Doctoral Student"=>8, "Student > Ph. D. Student"=>32, "Student > Postgraduate"=>4, "Student > Master"=>11, "Other"=>2, "Student > Bachelor"=>19, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>8}, "reader_count_by_user_role"=>{"Unspecified"=>3, "Professor > Associate Professor"=>3, "Researcher"=>19, "Student > Doctoral Student"=>8, "Student > Ph. D. Student"=>32, "Student > Postgraduate"=>4, "Student > Master"=>11, "Other"=>2, "Student > Bachelor"=>19, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>8}, "reader_count_by_subject_area"=>{"Unspecified"=>6, "Biochemistry, Genetics and Molecular Biology"=>18, "Agricultural and Biological Sciences"=>81, "Medicine and Dentistry"=>1, "Physics and Astronomy"=>1, "Chemistry"=>3, "Computer Science"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Chemistry"=>{"Chemistry"=>3}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>81}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>18}, "Unspecified"=>{"Unspecified"=>6}}, "reader_count_by_country"=>{"United States"=>1, "Denmark"=>1, "Mexico"=>1, "United Kingdom"=>1, "Germany"=>3}, "group_count"=>3}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/486058", "https://ndownloader.figshare.com/files/486061", "https://ndownloader.figshare.com/files/486063", "https://ndownloader.figshare.com/files/486068", "https://ndownloader.figshare.com/files/486078", "https://ndownloader.figshare.com/files/486084", "https://ndownloader.figshare.com/files/486087"], "description"=>"<div><p>The basidiomycete <em>Ustilago maydis</em> causes smut disease in maize, with large plant tumors being formed as the most prominent disease symptoms. During all steps of infection, <em>U. maydis</em> depends on a biotrophic interaction, which requires an efficient suppression of plant immunity. In a previous study, we identified the secreted effector protein Pit2, which is essential for maintenance of biotrophy and induction of tumors. Deletion mutants for <em>pit2</em> successfully penetrate host cells but elicit various defense responses, which stops further fungal proliferation. We now show that Pit2 functions as an inhibitor of a set of apoplastic maize cysteine proteases, whose activity is directly linked with salicylic-acid-associated plant defenses. Consequently, protease inhibition by Pit2 is required for <em>U. maydis</em> virulence. Sequence comparisons with Pit2 orthologs from related smut fungi identified a conserved sequence motif. Mutation of this sequence caused loss of Pit2 function. Consequently, expression of the mutated protein in <em>U. maydis</em> could not restore virulence of the <em>pit2</em> deletion mutant, indicating that the protease inhibition by Pit2 is essential for fungal virulence. Moreover, synthetic peptides of the conserved sequence motif showed full activity as protease inhibitor, which identifies this domain as a new, minimal protease inhibitor domain in plant-pathogenic fungi.</p> </div>", "links"=>[], "tags"=>["compatibility", "requires", "inhibition", "cysteine", "proteases", "fungal", "effector", "pit2"], "article_id"=>157073, "categories"=>["Microbiology", "Plant Biology"], "users"=>["André N. Mueller", "Sebastian Ziemann", "Steffi Treitschke", "Daniela Aßmann", "Gunther Doehlemann"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1003177.s001", "https://dx.doi.org/10.1371/journal.ppat.1003177.s002", "https://dx.doi.org/10.1371/journal.ppat.1003177.s003", "https://dx.doi.org/10.1371/journal.ppat.1003177.s004", "https://dx.doi.org/10.1371/journal.ppat.1003177.s005", "https://dx.doi.org/10.1371/journal.ppat.1003177.s006", "https://dx.doi.org/10.1371/journal.ppat.1003177.s007"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Compatibility_in_the_Ustilago_maydis_Maize_Interaction_Requires_Inhibition_of_Host_Cysteine_Proteases_by_the_Fungal_Effector_Pit2__/157073", "title"=>"Compatibility in the <em>Ustilago maydis</em>–Maize Interaction Requires Inhibition of Host Cysteine Proteases by the Fungal Effector Pit2", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-02-14 01:57:53"}
  • {"files"=>["https://ndownloader.figshare.com/files/488979"], "description"=>"<p>(<b>A</b>) Domain structure of the maize cysteine protease CP2, which was identified as Pit2 interaction partner in a yeast-two-hybrid screen. SP: signal peptide, M: minichain, typical for aleurain-like proteases <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003177#ppat.1003177-vanderLinde2\" target=\"_blank\">[29]</a>. Cys167, His307, Asn327 form the catalytic triad. Numbers (1–3) indicate sequence start of CP2 constructs (1) used for heterologous CP2 expression in <i>E. coli</i>, (2) used for Y2H experiments, (3) the CP2 fragment identified in the initial Y2H library screen. (<b>B</b>) Y2H interaction tests of Pit2 with different versions of CP2. Pit2 does not interact with CP2<sub>full</sub> (Full-length protease including N-terminal prodomain, corresponding to (1) shown in (A)) but interacts with inactivated CP2<sub>i</sub> (Catalytic triad residues were replaced by Glycine). BD: Gal4 Binding Domain. AD: Gal4 Activation Domain. (<b>C</b>) Co-immunoprecipitation shows interaction of Pit2 and CP2 fusion-proteins isolated from yeast cells. (<b>D</b>) Co-immunoprecipitation of <i>E. coli</i> expressed GST-Pit2 and HA-tagged CP2 protein that was expressed in <i>N. benthamiana</i> (see <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003177#ppat-1003177-g003\" target=\"_blank\">Figure 3</a>). (<b>E</b>) Fluorescence based protease assay shows activity of recombinant CP2 that was purified from <i>E. coli</i> and its inhibition by Pit2 as well as the specific small-molecule cysteine protease inhibitor E-64. not activated: purified CP2 shows only very low activity. activated: activity of CP2 after activation by pH-shift and treatment with 10 mM pepsin (see <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003177#s4\" target=\"_blank\">material and methods</a> for further details). Pit2: Addition of 10 µM Pit2 resulted in significant reduction of CP2 activity. 2.5 µM E-64 inhibited CP2. The experiment was carried out in three independent replicates; error bars represent SEM; P values were calculated by an unpaired t test. *P<0.05.</p>", "links"=>[], "tags"=>["pit2", "maize", "protease"], "article_id"=>159503, "categories"=>["Microbiology", "Plant Biology"], "users"=>["André N. Mueller", "Sebastian Ziemann", "Steffi Treitschke", "Daniela Aßmann", "Gunther Doehlemann"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1003177.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Interaction_of_Pit2_and_the_maize_protease_CP2_/159503", "title"=>"Interaction of Pit2 and the maize protease CP2.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-14 02:38:23"}
  • {"files"=>["https://ndownloader.figshare.com/files/489054"], "description"=>"<p>(<b>A</b>) Y2H assay showing interaction of Pit2 with the maize cysteine proteases CP1A, CP1B, CP2 and XCP2 but not with CatB. BD: Gal4 Binding Domain. AD: Gal4 Activation Domain. (<b>B</b>) Protease activity in fractionated apoplastic fluid of maize leaves after treatment with SA. Highest activity was observed in fractions at elution volume 19.5 ml and 20.5 ml. Protease activity was inhibited by treatment with 10 µM recombinant Pit2 or 5 µM E-64, respectively. (<b>C</b>) Protease activity in apoplastic fluid fractions 19.5 ml (dark grey) and 20.5 ml (light grey). Application of 1–10 µM recombinant Pit2 resulted in a concentration-dependent inhibition of protease activity. <b>D</b>) Activity based protein profiling of cysteine proteases in apoplastic fractions 19.5 ml and 20.5 ml using the specific probe DCG-04 shows inhibition of the apoplastic proteases by Pit2 and E-64. LC: loading control; error bars represent SEM.</p>", "links"=>[], "tags"=>["interacts", "apoplastic", "maize", "cysteine", "proteases", "inhibits"], "article_id"=>159573, "categories"=>["Microbiology", "Plant Biology"], "users"=>["André N. Mueller", "Sebastian Ziemann", "Steffi Treitschke", "Daniela Aßmann", "Gunther Doehlemann"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1003177.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Pit2_interacts_with_different_apoplastic_maize_cysteine_proteases_and_inhibits_their_activity_/159573", "title"=>"Pit2 interacts with different apoplastic maize cysteine proteases and inhibits their activity.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-14 02:39:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/489140"], "description"=>"<p>Activity of CP2, CP1A, XCP2 and CatB that were transiently expressed in <i>N. benthamiana</i> using <i>A. tumefaciens</i> mediated transformation. Protease activity of CP2, CP1A and XCP2 was significantly inhibited by 10 µM of recombinant Pit2, while activity of CatB was not sensitive to Pit2. E-64 (5 µM) inhibited all four maize proteases. The experiment was carried out in three independent replicates; error bars represent SEM; P values were calculated by an unpaired t test. *P<0.05.</p>", "links"=>[], "tags"=>["maize", "cysteine", "proteases", "inhibition"], "article_id"=>159659, "categories"=>["Microbiology", "Plant Biology"], "users"=>["André N. Mueller", "Sebastian Ziemann", "Steffi Treitschke", "Daniela Aßmann", "Gunther Doehlemann"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1003177.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Activity_of_N_benthamiana_expressed_maize_cysteine_proteases_and_their_inhibition_by_Pit2_/159659", "title"=>"Activity of <i>N. benthamiana</i> expressed maize cysteine proteases and their inhibition by Pit2.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-14 02:40:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/489195"], "description"=>"<p>(<b>A</b>) Alignment of <i>U. maydis</i> Pit2 (Um01375) and orthologs from the barley covered smut fungus <i>Ustilago hordei</i> (Uh02064) and the maize anther smut <i>Sporisorium reilianum</i> (Sr10529). Red box marks predicted secretion signals. Magenta labels identical (dark) and similar (light) amino acid residues. Orange box shows a 14 amino acid, highly conserved sequence stretch (residues 44–57). Green box marks the four aromatic residues that were addressed by targeted mutagenesis (see <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003177#ppat-1003177-t001\" target=\"_blank\">Table 1</a>). (<b>B</b>) Y2H analysis of Pit2 mutants carrying deletions of the conserved domain shown in (A). (<b>C</b>) Y2H of Pit2 mutants carrying mutations of the conserved domain shown in (A) and <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003177#ppat-1003177-t001\" target=\"_blank\">Table 1</a>. BD: Gal4 Binding Domain. AD: Gal4 Activation Domain.</p>", "links"=>[], "tags"=>["pit2", "smut", "fungi", "conserved", "cysteine"], "article_id"=>159711, "categories"=>["Microbiology", "Plant Biology"], "users"=>["André N. Mueller", "Sebastian Ziemann", "Steffi Treitschke", "Daniela Aßmann", "Gunther Doehlemann"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1003177.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sequence_conservation_of_Pit2_in_related_smut_fungi_and_the_role_of_a_conserved_domain_for_interaction_with_cysteine_proteases_/159711", "title"=>"Sequence conservation of Pit2 in related smut fungi and the role of a conserved domain for interaction with cysteine proteases.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-14 02:41:51"}
  • {"files"=>["https://ndownloader.figshare.com/files/489332"], "description"=>"<p>(<b>A</b>) Disease rating of maize seedlings 12 days after infection with <i>U. maydis</i>. SG200: virulent <i>U. maydis</i> strain showing wild type disease symptoms. Δpit2: strain SG200Δpit2, a <i>pit2</i> deletion mutant derived from strain SG200 <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003177#ppat.1003177-Doehlemann2\" target=\"_blank\">[27]</a>. Δpit2_pit2<sup>mut49–53</sup>: Strain SG200Δpit2 complemented with pit2<sup>mut49–53</sup> (see <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003177#ppat-1003177-g004\" target=\"_blank\">Figure 4A</a>, <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003177#ppat-1003177-t001\" target=\"_blank\">Table 1</a>). Δpit2_pit2<sup>Δ49–53</sup>: Strain SG200Δpit2 complemented with pit2<sup>Δ49–53</sup> (see <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003177#ppat-1003177-g004\" target=\"_blank\">Figure 4A</a>, <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003177#ppat-1003177-t001\" target=\"_blank\">Table 1</a>). Δpit2_pit2: Δpit2 mutant complemented with wild-type <i>pit2 </i><a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003177#ppat.1003177-Doehlemann2\" target=\"_blank\">[27]</a>. (<b>B</b>) Disease symptoms on maize leaves 12 days after infection with the <i>U. maydis</i> strains shown in (A). (<b>C</b>) Confocal images of intracellular <i>U. maydis</i> hyphae showing secretion of mCherry-tagged wild type Pit2 (lower panel) as well as the mutated Pit2 versions Pit2<sup>Δ44–57</sup> (upper panel) and Pit2<sup>mut49–53</sup> (middle panel). Red: mCherry fluorescence. Grey: UV-laser induced autofluorescence of maize cell walls. Bars: 10 µm.</p>", "links"=>[], "tags"=>["conserved", "pit2", "virulence"], "article_id"=>159854, "categories"=>["Microbiology", "Plant Biology"], "users"=>["André N. Mueller", "Sebastian Ziemann", "Steffi Treitschke", "Daniela Aßmann", "Gunther Doehlemann"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1003177.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_conserved_domain_is_required_for_function_of_Pit2_and_virulence_of_U_maydis_/159854", "title"=>"The conserved domain is required for function of Pit2 and virulence of <i>U. maydis</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-14 02:44:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/489459"], "description"=>"<p>(<b>A</b>) Protease activity in fractionated apoplastic fluid of maize leaves is inhibited by 10 µM Pit2 but not by the same concentration of Pit2<sup>mut49–53</sup>. (<b>B</b>) Protease activity of the apoplastic fluid fractions shown in (A) is efficiently inhibited by 10 µM of the PID14 peptide, while the same concentration of peptide PID14<sup>mut</sup> did not significantly influence protease activity. (<b>C</b>) Activity of <i>N. benthamiana</i> expressed maize proteases CP2, CP1A and XCP2 is inhibited by 10 µM recombinant Pit2 (as shown in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003177#ppat-1003177-g003\" target=\"_blank\">Figure 3</a>) but not by the same concentration of recombinant Pit2<sup>mut49–53</sup>. (<b>D</b>) Activity of <i>N. benthamiana</i> expressed maize proteases CP2, CP1A, XCP2 and CatB is inhibited by 10 µM of the PID14 peptide but not by the same concentration of recombinant PID14<sup>mut</sup>. The experiment was carried out in three independent replicates; error bars represent SEM; P values were calculated by an unpaired t test. *P<0.05.</p>", "links"=>[], "tags"=>["inhibition", "apoplastic", "maize", "proteases", "pit2", "protease", "inhibitor"], "article_id"=>159973, "categories"=>["Microbiology", "Plant Biology"], "users"=>["André N. Mueller", "Sebastian Ziemann", "Steffi Treitschke", "Daniela Aßmann", "Gunther Doehlemann"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1003177.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Specific_inhibition_of_apoplastic_maize_proteases_by_Pit2_and_the_protease_inhibitor_domain_PID14_/159973", "title"=>"Specific inhibition of apoplastic maize proteases by Pit2 and the protease inhibitor domain PID14.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-14 02:46:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/489542"], "description"=>"<p>Apoplastic fluid was isolated from maize leaves two days after infection with <i>U. maydis</i> strain SG200 or SG200Δpit2, respectively. Buffer: Apoplastic fluid extracts showing increased protease activity in SG200Δpit2 infected maize plants compared to SG200 wild type infections. E-64: Activity after treatment with 5 µM E-64. Pit2: Treatment with 10 µM recombinant Pit2 reduced protease activity in both samples below wild-type infected level. The same concentration of Pit2<sup>mut49–53</sup> did not cause reduction of protease activity. PID14: Treatment with 10 µM of the PID14 peptide completely inhibited protease activity; PID14<sup>mut</sup> did not inhibit proteases. The experiment was carried out in three independent replicates; error bars represent SEM.</p>", "links"=>[], "tags"=>["apoplastic", "fluids", "maize", "plants", "infected"], "article_id"=>160061, "categories"=>["Microbiology", "Plant Biology"], "users"=>["André N. Mueller", "Sebastian Ziemann", "Steffi Treitschke", "Daniela Aßmann", "Gunther Doehlemann"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1003177.g007"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Protease_activity_in_apoplastic_fluids_of_maize_plants_infected_with_U_maydis_/160061", "title"=>"Protease activity in apoplastic fluids of maize plants infected with <i>U. maydis</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-14 00:01:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/489599"], "description"=>"<p>The conserved Pit2 motif and different mutations tested in this study.</p>", "links"=>[], "tags"=>["conserved", "pit2", "motif", "mutations", "tested"], "article_id"=>160117, "categories"=>["Microbiology", "Plant Biology"], "users"=>["André N. Mueller", "Sebastian Ziemann", "Steffi Treitschke", "Daniela Aßmann", "Gunther Doehlemann"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1003177.t001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_conserved_Pit2_motif_and_different_mutations_tested_in_this_study_/160117", "title"=>"The conserved Pit2 motif and different mutations tested in this study.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-14 00:01:57"}

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Relative Metric

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