Pollen Competition as a Reproductive Isolation Barrier Represses Transgene Flow between Compatible and Co-Flowering Citrus Genotypes
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{"title"=>"Pollen competition as a reproductive isolation barrier represses transgene flow between compatible and co-flowering citrus genotypes", "type"=>"journal", "authors"=>[{"first_name"=>"Elsa", "last_name"=>"Pons", "scopus_author_id"=>"6701849454"}, {"first_name"=>"Antonio", "last_name"=>"Navarro", "scopus_author_id"=>"7202496078"}, {"first_name"=>"Patrick", "last_name"=>"Ollitrault", "scopus_author_id"=>"6602788846"}, {"first_name"=>"Leandro", "last_name"=>"Peña", "scopus_author_id"=>"7005404671"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"21991359", "doi"=>"10.1371/journal.pone.0025810", "pui"=>"362683464", "issn"=>"19326203", "sgr"=>"80053462824", "scopus"=>"2-s2.0-80053462824"}, "id"=>"48d612c1-2bf8-34f8-af65-7b7ae64d9493", "abstract"=>"BACKGROUND/OBJECTIVE: Despite potential benefits granted by genetically modified (GM) fruit trees, their release and commercialization raises concerns about their potential environmental impact, and the transfer via pollen of transgenes to cross-compatible cultivars is deemed to be the greatest source for environmental exposure. Information compiled from field trials on GM trees is essential to propose measures to minimize the transgene dispersal. We have conducted a field trial of seven consecutive years to investigate the maximum frequency of pollen-mediated crop-to-crop transgene flow in a citrus orchard, and its relation to the genetic, phenological and environmental factors involved. METHODOLOGY/PRINCIPAL FINDINGS: Three different citrus genotypes carrying the uidA (GUS) tracer marker gene (pollen donors) and a non-GM self-incompatible contiguous citrus genotype (recipient) were used in conditions allowing natural entomophilous pollination to occur. The examination of 603 to 2990 seeds per year showed unexpectedly low frequencies (0.17-2.86%) of transgene flow. Paternity analyses of the progeny of subsets of recipient plants using 10 microsatellite (SSR) loci demonstrated a higher mating competence of trees from another non-GM pollen source population that greatly limited the mating chance of the contiguous cross-compatible and flowering-synchronized transgenic pollen source. This mating superiority could be explained by a much higher pollen competition capacity of the non-GM genotypes, as was confirmed through mixed-hand pollinations. CONCLUSIONS/SIGNIFICANCE: Pollen competition strongly contributed to transgene confinement. Based on this finding, suitable isolation measures are proposed for the first time to prevent transgene outflow between contiguous plantings of citrus types that may be extendible to other entomophilous transgenic fruit tree species.", "link"=>"http://www.mendeley.com/research/pollen-competition-reproductive-isolation-barrier-represses-transgene-flow-between-compatible-coflow", "reader_count"=>27, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Librarian"=>1, "Student > Doctoral Student"=>1, "Researcher"=>3, "Student > Ph. D. Student"=>6, "Student > Postgraduate"=>1, "Student > Master"=>3, "Other"=>1, "Student > Bachelor"=>5, "Lecturer"=>1, "Professor"=>2, "Unspecified"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Librarian"=>1, "Student > Doctoral Student"=>1, "Researcher"=>3, "Student > Ph. D. Student"=>6, "Student > Postgraduate"=>1, "Student > Master"=>3, "Other"=>1, "Student > Bachelor"=>5, "Lecturer"=>1, "Professor"=>2, "Unspecified"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>1, "Agricultural and Biological Sciences"=>19, "Psychology"=>1, "Social Sciences"=>1, "Earth and Planetary Sciences"=>1, "Economics, Econometrics and Finance"=>1}, "reader_count_by_subdiscipline"=>{"Social Sciences"=>{"Social Sciences"=>1}, "Psychology"=>{"Psychology"=>1}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>1}, "Economics, Econometrics and Finance"=>{"Economics, Econometrics and Finance"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>19}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>1}, "Unspecified"=>{"Unspecified"=>2}, "Environmental Science"=>{"Environmental Science"=>1}}, "reader_count_by_country"=>{"Netherlands"=>1, "United States"=>1, "United Kingdom"=>1, "Italy"=>1, "Spain"=>2}, "group_count"=>2}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/729563"], "description"=>"<p><b>A</b>) Map showing the relative location of recipients (dots) and pollen source populations (T, A and B plots). Recipient (mother) trees sampled in 2005 and/or 2006 whose progeny were analyzed for paternity assignment are represented by filled circles. <b>B</b>) Radial graphs represent the profiles of genotyped progeny from each mother tree. Numbers in the vertices indicate the recipient tree number followed by the total number of progeny seedlings analyzed from the mother tree (number in parentheses). The distribution of recipient trees in the vertices of the graph has been established according to their relative position in the field to accurately visualize the pollen dispersal patterns. The percentage of progeny from each corresponding recipient tree is represented on each radial axis by following categories: “B”, progeny unambiguously assigned to B; “A”, progeny unambiguously assigned to A; “T”, progeny unambiguously assigned to T; and “na”, progeny that could not be assigned to any PPD. Clementine plants producing an insufficient number of progeny seedlings were excluded from this study.</p>", "links"=>[], "tags"=>["pollen", "dispersal", "patterns"], "article_id"=>399920, "categories"=>["Biotechnology", "Ecology", "Genetics", "Plant Biology"], "users"=>["Elsa Pons", "Antonio Navarro", "Patrick Ollitrault", "Leandro Peña"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025810.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Schematic_representation_of_pollen_dispersal_patterns_at_the_study_site_/399920", "title"=>"Schematic representation of pollen dispersal patterns at the study site.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-10-03 02:45:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/729433"], "description"=>"<p>Based on the classification of the pollination events made in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0025810#pone-0025810-t004\" target=\"_blank\">Table 4</a>, maximum reproductive success was estimated for each plot, as the percentage of pollination events unambiguously assigned (black color) plus the partial contributions of the percentages corresponding to pollination events ambiguously assigned (grey color). n.a., not assigned.</p>", "links"=>[], "tags"=>["reproductive", "assessed", "pollen", "2005"], "article_id"=>399788, "categories"=>["Biotechnology", "Ecology", "Genetics", "Plant Biology"], "users"=>["Elsa Pons", "Antonio Navarro", "Patrick Ollitrault", "Leandro Peña"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025810.g003", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Maximum_reproductive_success_assessed_for_each_pollen_source_population_in_A_2005_and_B_2006_/399788", "title"=>"Maximum reproductive success assessed for each pollen source population in A) 2005 and B) 2006.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-10-03 02:43:08"}
  • {"files"=>["https://ndownloader.figshare.com/files/729932"], "description"=>"<p>Results of mixed-pollination treatments performed in 2006 and 2007 in comparison with single-pollination control treatments with PC and P1, including fruit set, seed set, and the percentage of GUS-positive (GUS+) seedlings in progeny as a parameter determining the siring success of P1.</p>", "links"=>[], "tags"=>["mixed-pollination", "treatments", "performed", "2006", "2007", "single-pollination", "pc", "gus-positive", "seedlings", "progeny", "parameter", "determining", "siring"], "article_id"=>400277, "categories"=>["Biotechnology", "Ecology", "Genetics", "Plant Biology"], "users"=>["Elsa Pons", "Antonio Navarro", "Patrick Ollitrault", "Leandro Peña"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025810.t005", "stats"=>{"downloads"=>1, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Results_of_mixed_pollination_treatments_performed_in_2006_and_2007_in_comparison_with_single_pollination_control_treatments_with_PC_and_P1_including_fruit_set_seed_set_and_the_percentage_of_GUS_positive_GUS_seedlings_in_progeny_as_a_parameter_determining/400277", "title"=>"Results of mixed-pollination treatments performed in 2006 and 2007 in comparison with single-pollination control treatments with PC and P1, including fruit set, seed set, and the percentage of GUS-positive (GUS+) seedlings in progeny as a parameter determining the siring success of P1.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-10-03 00:04:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/729249"], "description"=>"<p>It consisted of 130 trees, planted in rows along the transgenic (T) plot, including 16 transgenic plants of Pineapple sweet orange (black circles), 16 transgenic plants of Carrizo citrange (black squares) and 16 transgenic plants of Mexican lime (black triangles) (2 plants each from 8 independent transgenic lines numbered from 1 to 8, from left to right). In addition, there were 8 non-transgenic control plants from each genotype individually interspersed between the two plants from each transgenic line and represented by grey figures. Fifty-eight non-transgenic Clemenules clementine trees planted along an external edge (white circles; numbered in increasing order going clockwise) were used as the pollen recipients to estimate transgene flow frequencies.</p>", "links"=>[], "tags"=>["diagram"], "article_id"=>399605, "categories"=>["Biotechnology", "Ecology", "Genetics", "Plant Biology"], "users"=>["Elsa Pons", "Antonio Navarro", "Patrick Ollitrault", "Leandro Peña"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025810.g001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Schematic_diagram_of_the_experimental_field_trial_/399605", "title"=>"Schematic diagram of the experimental field trial.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-10-03 02:40:05"}
  • {"files"=>["https://ndownloader.figshare.com/files/729691"], "description"=>"<p>Progeny from all recipient trees analyzed in 2005 and/or 2006 unambiguously assigned to each plot was divided into classes based on the distance between the (mother) recipient tree and plot B, measured in rows. Black dots represent the mating frequencies in each distance class as a proportion of all pollination events unambiguously assigned to this plot. Lines represent the curves fitted to regression models that best describe the relationship between mating frequencies and distance to Plot B for each pollen source population (*<i>P</i><0.05; **<i>P</i><0.01).</p>", "links"=>[], "tags"=>["dispersal", "curves"], "article_id"=>400049, "categories"=>["Biotechnology", "Ecology", "Genetics", "Plant Biology"], "users"=>["Elsa Pons", "Antonio Navarro", "Patrick Ollitrault", "Leandro Peña"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025810.g005", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Pollen_dispersal_curves_of_each_plot_as_a_function_of_distance_to_plot_B_/400049", "title"=>"Pollen dispersal curves of each plot as a function of distance to plot B.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-10-03 00:00:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/729817"], "description"=>"<p>Relationship between the maximum mating success achieved in 2005 and 2006 by each Potential Pollen Donor (PPD) of plot B (H1, H2, H3, H4 and H5) and its relative abundance at the study site (reported in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0025810#pone-0025810-t001\" target=\"_blank\">Table 1</a>). Black dots represent the proportion of mating events (unambiguously plus ambiguously) assigned to each PPD from plot B calculated over the total progeny unambiguously assigned to this plot and averaged between years. Bars represent standard errors. n.s., P>0.1 (not significant).</p>", "links"=>[], "tags"=>["genetics and genomics", "plant biology", "biotechnology", "ecology"], "article_id"=>400175, "categories"=>["Biotechnology", "Ecology", "Genetics", "Plant Biology"], "users"=>["Elsa Pons", "Antonio Navarro", "Patrick Ollitrault", "Leandro Peña"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025810.g006", "stats"=>{"downloads"=>1, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Density_effect_/400175", "title"=>"Density effect.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-10-03 00:02:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/368638", "https://ndownloader.figshare.com/files/368732", "https://ndownloader.figshare.com/files/368806", "https://ndownloader.figshare.com/files/368897", "https://ndownloader.figshare.com/files/368987", "https://ndownloader.figshare.com/files/369058", "https://ndownloader.figshare.com/files/369115", "https://ndownloader.figshare.com/files/369214"], "description"=>"<div><h3>Background/Objective</h3><p>Despite potential benefits granted by genetically modified (GM) fruit trees, their release and commercialization raises concerns about their potential environmental impact, and the transfer via pollen of transgenes to cross-compatible cultivars is deemed to be the greatest source for environmental exposure. Information compiled from field trials on GM trees is essential to propose measures to minimize the transgene dispersal. We have conducted a field trial of seven consecutive years to investigate the maximum frequency of pollen-mediated crop-to-crop transgene flow in a citrus orchard, and its relation to the genetic, phenological and environmental factors involved.</p> <h3>Methodology/Principal Findings</h3><p>Three different citrus genotypes carrying the <em>uidA</em> (GUS) tracer marker gene (pollen donors) and a non-GM self-incompatible contiguous citrus genotype (recipient) were used in conditions allowing natural entomophilous pollination to occur. The examination of 603 to 2990 seeds per year showed unexpectedly low frequencies (0.17–2.86%) of transgene flow. Paternity analyses of the progeny of subsets of recipient plants using 10 microsatellite (SSR) loci demonstrated a higher mating competence of trees from another non-GM pollen source population that greatly limited the mating chance of the contiguous cross-compatible and flowering-synchronized transgenic pollen source. This mating superiority could be explained by a much higher pollen competition capacity of the non-GM genotypes, as was confirmed through mixed-hand pollinations.</p> <h3>Conclusions/Significance</h3><p>Pollen competition strongly contributed to transgene confinement. Based on this finding, suitable isolation measures are proposed for the first time to prevent transgene outflow between contiguous plantings of citrus types that may be extendible to other entomophilous transgenic fruit tree species.</p> </div>", "links"=>[], "tags"=>["pollen", "reproductive", "represses", "transgene", "compatible", "co-flowering", "citrus", "genotypes"], "article_id"=>132848, "categories"=>["Biotechnology", "Ecology", "Genetics", "Cell Biology"], "users"=>["Elsa Pons", "Antonio Navarro", "Patrick Ollitrault", "Leandro Peña"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0025810.s001", "https://dx.doi.org/10.1371/journal.pone.0025810.s002", "https://dx.doi.org/10.1371/journal.pone.0025810.s003", "https://dx.doi.org/10.1371/journal.pone.0025810.s004", "https://dx.doi.org/10.1371/journal.pone.0025810.s005", "https://dx.doi.org/10.1371/journal.pone.0025810.s006", "https://dx.doi.org/10.1371/journal.pone.0025810.s007", "https://dx.doi.org/10.1371/journal.pone.0025810.s008"], "stats"=>{"downloads"=>30, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Pollen_Competition_as_a_Reproductive_Isolation_Barrier_Represses_Transgene_Flow_between_Compatible_and_Co_Flowering_Citrus_Genotypes/132848", "title"=>"Pollen Competition as a Reproductive Isolation Barrier Represses Transgene Flow between Compatible and Co-Flowering Citrus Genotypes", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-10-03 00:47:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/729879"], "description"=>"<p>All pollination events were categorized by the origin of the pollen donor(s) assigned according to microsatellite (SSR) genotyping, GUS expression and leaf morphology (trifoliate character).</p>", "links"=>[], "tags"=>["paternity", "progeny", "open-pollinated", "recipients", "harvested", "2005"], "article_id"=>400234, "categories"=>["Biotechnology", "Ecology", "Genetics", "Plant Biology"], "users"=>["Elsa Pons", "Antonio Navarro", "Patrick Ollitrault", "Leandro Peña"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025810.t004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Results_of_paternity_assignment_in_progeny_from_open_pollinated_recipients_harvested_in_2005_and_2006_/400234", "title"=>"Results of paternity assignment in progeny from open-pollinated recipients harvested in 2005 and 2006.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-10-03 00:03:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/729319"], "description"=>"<p>Different phases of the bloom period for Pineapple sweet orange, Carrizo citrange and Clemenules clementine genotypes are represented by different colors. The overlap in the full-flowering phase (pink) determines the flowering synchrony between genotypes.</p>", "links"=>[], "tags"=>["calendars", "flowering", "genotypes"], "article_id"=>399671, "categories"=>["Biotechnology", "Ecology", "Genetics", "Plant Biology"], "users"=>["Elsa Pons", "Antonio Navarro", "Patrick Ollitrault", "Leandro Peña"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025810.g002", "stats"=>{"downloads"=>1, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phenological_calendars_of_flowering_for_genotypes_in_plot_T_/399671", "title"=>"Phenological calendars of flowering for genotypes in plot T.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-10-03 02:41:11"}
  • {"files"=>["https://ndownloader.figshare.com/files/730007"], "description"=>"1<p>Number of transgenic seedlings was determined by GUS expression in leaves and confirmed by PCR analysis of the <i>uidA</i> transgene. False GUS negative seedlings were not found in any case.</p>2<p>PMTF frequency was calculated as the percentage of transgenic seedlings from the total number of seedlings analyzed per year.</p>3<p>For each year, χ<sup>2</sup> tests were performed to compare the PMTF frequencies obtained by this method with the PMTF frequencies obtained by testing GUS expression in seeds (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0025810#pone-0025810-t002\" target=\"_blank\">Table 2</a>). The critical value for 1 <i>df</i> at a 95% confidence level is 3.84.</p>", "links"=>[], "tags"=>["validation", "pollen-mediated", "transgene", "seedlings", "subset", "open-pollinated", "trees", "years"], "article_id"=>400357, "categories"=>["Biotechnology", "Ecology", "Genetics", "Plant Biology"], "users"=>["Elsa Pons", "Antonio Navarro", "Patrick Ollitrault", "Leandro Peña"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025810.t003", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Molecular_validation_of_the_pollen_mediated_transgene_flow_PMTF_assessment_method_by_testing_seedlings_from_a_subset_of_open_pollinated_recipient_trees_during_two_years_2005_and_2006_/400357", "title"=>"Molecular validation of the pollen-mediated transgene flow (PMTF) assessment method by testing seedlings from a subset of open-pollinated recipient trees during two years (2005 and 2006).", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-10-03 00:05:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/730048"], "description"=>"<p>Potential pollen donor (PPD) genotypes present at the study site, including their abbreviation codes, population sizes (number of adult trees) and relative amounts.</p>", "links"=>[], "tags"=>["pollen", "genotypes", "abbreviation", "sizes"], "article_id"=>400403, "categories"=>["Biotechnology", "Ecology", "Genetics", "Plant Biology"], "users"=>["Elsa Pons", "Antonio Navarro", "Patrick Ollitrault", "Leandro Peña"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025810.t001", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Potential_pollen_donor_PPD_genotypes_present_at_the_study_site_including_their_abbreviation_codes_population_sizes_number_of_adult_trees_and_relative_amounts_/400403", "title"=>"Potential pollen donor (PPD) genotypes present at the study site, including their abbreviation codes, population sizes (number of adult trees) and relative amounts.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-10-03 00:06:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/729973"], "description"=>"<p>The pollen-mediated transgene flow (PMTF) frequencies for seven years as determined by testing seeds from open-pollinated recipient trees for GUS expression.</p>", "links"=>[], "tags"=>["pollen-mediated", "transgene", "frequencies", "years", "seeds", "open-pollinated", "trees", "gus"], "article_id"=>400321, "categories"=>["Biotechnology", "Ecology", "Genetics", "Plant Biology"], "users"=>["Elsa Pons", "Antonio Navarro", "Patrick Ollitrault", "Leandro Peña"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025810.t002", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_pollen_mediated_transgene_flow_PMTF_frequencies_for_seven_years_as_determined_by_testing_seeds_from_open_pollinated_recipient_trees_for_GUS_expression_/400321", "title"=>"The pollen-mediated transgene flow (PMTF) frequencies for seven years as determined by testing seeds from open-pollinated recipient trees for GUS expression.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-10-03 00:05:21"}

PMC Usage Stats | Further Information

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