Environmental Heat and Salt Stress Induce Transgenerational Phenotypic Changes in Arabidopsis thaliana
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{"title"=>"Environmental Heat and Salt Stress Induce Transgenerational Phenotypic Changes in Arabidopsis thaliana", "type"=>"journal", "authors"=>[{"first_name"=>"Léonie", "last_name"=>"Suter", "scopus_author_id"=>"36194345500"}, {"first_name"=>"Alex", "last_name"=>"Widmer", "scopus_author_id"=>"7005334885"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-84876047512", "sgr"=>"84876047512", "issn"=>"19326203", "doi"=>"10.1371/journal.pone.0060364", "pmid"=>"23585834", "isbn"=>"1932-6203", "pui"=>"368705041"}, "id"=>"cc6ae8b5-c629-38b0-927e-75d9395e3020", "abstract"=>"Plants that can adapt their phenotype may be more likely to survive changing environmental conditions. Heritable epigenetic variation could provide a way to rapidly adapt to such changes. Here we tested whether environmental stress induces heritable, potentially adaptive phenotypic changes independent of genetic variation over few generations in Arabidopsis thaliana. We grew two accessions (Col-0, Sha-0) of A. thaliana for three generations under salt, heat and control conditions and tested for induced heritable phenotypic changes in the fourth generation (G4) and in reciprocal F1 hybrids generated in generation three. Using these crosses we further tested whether phenotypic changes were maternally or paternally transmitted. In generation five (G5), we assessed whether phenotypic effects persisted over two generations in the absence of stress. We found that exposure to heat stress in previous generations accelerated flowering under G4 control conditions in Sha-0, but heritable effects disappeared in G5 after two generations without stress exposure. Previous exposure to salt stress increased salt tolerance in one of two reciprocal F1 hybrids. Transgenerational effects were maternally and paternally inherited. Lacking genetic variability, maternal and paternal inheritance and reversibility of transgenerational effects together indicate that stress can induce heritable, potentially adaptive phenotypic changes, probably through epigenetic mechanisms. These effects were strongly dependent on plant genotype and may not be a general response to stress in A. thaliana.", "link"=>"http://www.mendeley.com/research/environmental-heat-salt-stress-induce-transgenerational-phenotypic-changes-arabidopsis-thaliana", "reader_count"=>97, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>3, "Researcher"=>25, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>32, "Student > Postgraduate"=>2, "Other"=>4, "Student > Master"=>11, "Student > Bachelor"=>9, "Lecturer"=>3, "Lecturer > Senior Lecturer"=>1, "Professor"=>4}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>3, "Researcher"=>25, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>32, "Student > Postgraduate"=>2, "Other"=>4, "Student > Master"=>11, "Student > Bachelor"=>9, "Lecturer"=>3, "Lecturer > Senior Lecturer"=>1, "Professor"=>4}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Environmental Science"=>4, "Biochemistry, Genetics and Molecular Biology"=>6, "Agricultural and Biological Sciences"=>80, "Medicine and Dentistry"=>1, "Neuroscience"=>1, "Chemistry"=>1, "Computer Science"=>1, "Earth and Planetary Sciences"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Neuroscience"=>{"Neuroscience"=>1}, "Chemistry"=>{"Chemistry"=>1}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>80}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>6}, "Unspecified"=>{"Unspecified"=>2}, "Environmental Science"=>{"Environmental Science"=>4}}, "reader_count_by_country"=>{"Canada"=>1, "Argentina"=>1, "Belgium"=>2, "United States"=>2, "Brazil"=>1, "Mexico"=>2, "France"=>1, "Switzerland"=>1, "Germany"=>1}, "group_count"=>5}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1019662"], "description"=>"<p>Transgenerational effects of plants grown in generation four (G4) were tested with linear mixed models separately for G4 salt and control treatments with past treatment as fixed factor and tray as random factor. A Tukey test was applied to determine which of the four groups (both parental lines, only maternal or paternal line or no parental line previously exposed to stress) significantly differed from one another. Grey background indicates G4 salt treatment, while white background indicates G4 control treatment. Plants where both parents belonged to salt stressed lines are shown in dark columns, hatched columns indicate that one parent belonged to heat stressed lines and one to control lines, while white columns indicate offspring of control lines. Error bars indicate standard errors of the mean. A: Rosette diameter at day 14. B: Number of rosette leaves at day 14. ***<i>P</i>-value <0.001; **<i>P</i>-value <0.01; *<i>P</i>-value <0.05;<sup>. </sup><i>P</i>-value <0. 1, ns: <i>P</i>-value >0.1.</p>", "links"=>[], "tags"=>["paternal", "inheritance", "transgenerational"], "article_id"=>678733, "categories"=>["Developmental Biology", "Genetics", "Plant Biology", "Evolutionary Biology"], "users"=>["Léonie Suter", "Alex Widmer"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0060364.g005", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Maternal_and_paternal_inheritance_of_transgenerational_effects_of_salt_stress_in_Sha_215_Col_/678733", "title"=>"Maternal and paternal inheritance of transgenerational effects of salt stress in Sha×Col.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-04-09 02:25:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/1019659"], "description"=>"<p>After three generations of heat stress Sha-0 was grown in generation four (G4) under heat or control conditions (also compare to <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0060364#pone-0060364-t001\" target=\"_blank\">Table 1</a>). Grey background indicates G4 heat treatment and white background indicates G4 control treatment. Dark columns represent descendants of heat stressed lines, while white columns denote descendants of control lines. Above columns significances of differences within G4 treatments are indicated, while letters within columns represent comparisons between descendants of control lines grown under G4 control conditions with the other treatments. Error bars indicate standard errors of the mean. A: Rosette diameter at first flowering day (FFD); B: Number of rosette leaves at FFD; c: Biomass. **<i>P</i>-value <0.01; ns: <i>P</i>-value >0.1.</p>", "links"=>[], "tags"=>["generations", "genotype"], "article_id"=>678729, "categories"=>["Developmental Biology", "Genetics", "Plant Biology", "Evolutionary Biology"], "users"=>["Léonie Suter", "Alex Widmer"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0060364.g002", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Transgenerational_effects_of_three_generations_of_heat_stress_in_genotype_Sha_0_/678729", "title"=>"Transgenerational effects of three generations of heat stress in genotype Sha-0.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-04-09 02:25:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/1019658"], "description"=>"<p>Plants were grown either in stress or control conditions. In G3, plants were reciprocally crossed between stress and control lines and self-fertilized. Genetically identical offspring with either both parents (dark rosette), only the pollen recipient (horizontally striped rosette), only the pollen donor (vertically striped rosette), or none of the parental lines (white rosettes) having experienced stress treatment was grown under stress and control conditions in generation 4 (G4). Additionally, reciprocal crosses between accessions were performed in G3 to receive F1 hybrids (Sha×Col and Col×Sha) with maternal and/or paternal lines belonging to stressed lines or control lines. Offspring of G4 plants grown under control conditions with heat stress history were propagated for another generation (G5) under control conditions to identify long-term epigenetic effects.</p>", "links"=>[], "tags"=>["accession", "grown", "subsequently", "propagated", "descent", "generations", "replications"], "article_id"=>678728, "categories"=>["Developmental Biology", "Genetics", "Plant Biology", "Evolutionary Biology"], "users"=>["Léonie Suter", "Alex Widmer"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0060364.g001", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Experimental_design_in_generation_0_G0_one_plant_per_accession_Col_0_and_Sha_0_was_grown_under_standard_conditions_and_subsequently_propagated_with_single_seed_descent_for_three_generations_G1_8211_G3_using_five_independent_replications_across_generation/678728", "title"=>"Experimental design: in generation 0 (G0) one plant per accession (Col-0 and Sha-0) was grown under standard conditions and subsequently propagated with single seed descent for three generations (G1– G3), using five independent replications across generations.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-04-09 02:25:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/1019667"], "description"=>"b<p><i>P</i>-values were corrected for multiple testing according to Benjamini and Hochberg (1995), which leads to identical P-values for some non-significant traits. ***<i>P</i>-value <0.001; **<i>P</i>-value <0.01; *<i>P</i>-value <0.05;.: <i>P</i>-value <0.1.</p>", "links"=>[], "tags"=>["g1", "g3", "separately", "g4", "treatments", "linear"], "article_id"=>678737, "categories"=>["Developmental Biology", "Genetics", "Plant Biology", "Evolutionary Biology"], "users"=>["Léonie Suter", "Alex Widmer"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0060364.t002", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Transgenerational_effects_of_salt_treatment_in_G1_to_G3_analyzed_separately_both_for_G4_salt_and_G4_control_treatments_in_Sha_215_Col_and_Col_215_Sha_using_linear_mixed_models_with_past_treatment_as_fixed_shown_below_and_tray_as_random_factors_/678737", "title"=>"Transgenerational effects of salt treatment in G1 to G3 analyzed separately both for G4 salt and G4 control treatments in Sha×Col and Col×Sha using linear mixed models with past treatment as fixed (shown below) and tray as random factors.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-04-09 02:25:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/1019665"], "description"=>"b<p><i>P</i>-values were corrected for multiple testing according to Benjamini and Hochberg (1995), which leads to identical P-values for some non-significant traits. ***<i>P</i>-value <0.001; **<i>P</i>-value <0.01; *<i>P</i>-value <0.05;. : <i>P</i>-value <0.1.</p>", "links"=>[], "tags"=>["g1", "g3", "separately", "g4", "treatments", "sha-0", "col-0", "linear"], "article_id"=>678735, "categories"=>["Developmental Biology", "Genetics", "Plant Biology", "Evolutionary Biology"], "users"=>["Léonie Suter", "Alex Widmer"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0060364.t001", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Transgenerational_effects_of_heat_treatment_in_G1_to_G3_analyzed_separately_both_for_G4_heat_and_G4_control_treatments_in_Sha_0_and_Col_0_using_linear_mixed_models_with_past_treatment_as_fixed_shown_below_and_tray_as_random_factors_/678735", "title"=>"Transgenerational effects of heat treatment in G1 to G3 analyzed separately both for G4 heat and G4 control treatments in Sha-0 and Col-0 using linear mixed models with past treatment as fixed (shown below) and tray as random factors.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-04-09 02:25:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/1019666"], "description"=>"<p>Analysis was based on a linear mixed model with manually defined contrasts. <i>P</i>-values were corrected for multiple testing according to Benjamini and Hochberg (1995).</p>a<p>♀S: maternal line salt stressed; ♂S: paternal line salt stressed; ♀C: maternal line control; ♂C: paternal line control.</p>***<p><i>P</i>-value <0.001; **<i>P</i>-value <0.01; *<i>P</i>-value <0.05; <i>P</i>-value <0.1.</p>", "links"=>[], "tags"=>["g1", "g3", "phenotypic", "differences", "reciprocal", "hybrids", "g4"], "article_id"=>678736, "categories"=>["Developmental Biology", "Genetics", "Plant Biology", "Evolutionary Biology"], "users"=>["Léonie Suter", "Alex Widmer"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0060364.t003", "stats"=>{"downloads"=>1, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Analysis_of_the_effects_of_salt_treatment_in_G1_to_G3_in_no_one_or_both_parental_lines_on_phenotypic_differences_between_reciprocal_hybrids_Sha_215_Col_vs_Col_215_Sha_in_G4_salt_and_control_treatments_/678736", "title"=>"Analysis of the effects of salt treatment in G1 to G3 (in no, one or both parental lines) on phenotypic differences between reciprocal hybrids (Sha×Col vs. Col×Sha) in G4 salt and control treatments.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-04-09 02:25:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1019664"], "description"=>"<p>Rosette diameter at day 14 is compared between Sha×Col (dark grey) and Col×Sha (light gray) with four different histories (both parental lines salt treated, maternal or paternal line salt treated, both parental lines control treated) grown in G4 salt treatment. ***<i>P</i>-value <0.001; ns: <i>P</i>-value >0.1.</p>", "links"=>[], "tags"=>["reciprocal", "f1"], "article_id"=>678734, "categories"=>["Developmental Biology", "Genetics", "Plant Biology", "Evolutionary Biology"], "users"=>["Léonie Suter", "Alex Widmer"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0060364.g006", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Transgenerational_effects_of_salt_treatment_on_reciprocal_F1_hybrids_/678734", "title"=>"Transgenerational effects of salt treatment on reciprocal F1 hybrids.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-04-09 02:25:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/1019661"], "description"=>"<p>Grey background indicates G4 salt treatment, while white background indicates G4 control treatment. Dark columns represent descendants of salt stressed lines, while white columns denote descendants of control lines. Error bars indicate standard errors of the mean. A: Rosette diameter at day 14. B: Number of rosette leaves at day 14. ***<i>P</i>-value <0.001; ns: <i>P</i>-value >0.1.</p>", "links"=>[], "tags"=>["generations", "grown"], "article_id"=>678731, "categories"=>["Developmental Biology", "Genetics", "Plant Biology", "Evolutionary Biology"], "users"=>["Léonie Suter", "Alex Widmer"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0060364.g004", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Transgenerational_effects_of_three_generations_of_salt_stress_in_Sha_215_Col_grown_in_generation_four_G4_/678731", "title"=>"Transgenerational effects of three generations of salt stress in Sha×Col grown in generation four (G4).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-04-09 02:25:31"}
  • {"files"=>["https://ndownloader.figshare.com/files/1019660"], "description"=>"<p>After three generations of heat stress or control conditions, reciprocal crosses were grown in generation four (G4) under heat and control conditions and effects tested with linear mixed models separately for G4 heat and control treatments with past treatment as fixed factor and tray as random factor. A Tukey test was applied to determine which of the four groups (both parental lines, only maternal or paternal line or no parental line previously exposed to stress) significantly differed from one another. Grey background indicates G4 heat treatment, while white background indicates G4 control treatment. Plants where both parents belonged to heat stressed lines are shown in dark columns, hatched columns indicate that one parent belonged to heat stressed lines and one to control lines, while white columns indicate offspring of control lines. Error bars indicate standard errors of the mean. A: Rosette diameter at first flowering day (FFD); B: Number of rosette leaves at FFD; ***<i>P</i>- value <0.001; **<i>P</i>-value <0.01; ns: <i>P</i>-value >0.05.</p>", "links"=>[], "tags"=>["paternal", "inheritance", "transgenerational"], "article_id"=>678730, "categories"=>["Developmental Biology", "Genetics", "Plant Biology", "Evolutionary Biology"], "users"=>["Léonie Suter", "Alex Widmer"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0060364.g003", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Maternal_and_paternal_inheritance_of_transgenerational_effects_of_heat_stress_in_Sha_0_/678730", "title"=>"Maternal and paternal inheritance of transgenerational effects of heat stress in Sha-0.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-04-09 02:25:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/1019669", "https://ndownloader.figshare.com/files/1019670", "https://ndownloader.figshare.com/files/1019671", "https://ndownloader.figshare.com/files/1019672", "https://ndownloader.figshare.com/files/1019674", "https://ndownloader.figshare.com/files/1019675"], "description"=>"<div><p>Plants that can adapt their phenotype may be more likely to survive changing environmental conditions. Heritable epigenetic variation could provide a way to rapidly adapt to such changes. Here we tested whether environmental stress induces heritable, potentially adaptive phenotypic changes independent of genetic variation over few generations in <i>Arabidopsis thaliana</i>. We grew two accessions (Col-0, Sha-0) of <i>A. thaliana</i> for three generations under salt, heat and control conditions and tested for induced heritable phenotypic changes in the fourth generation (G4) and in reciprocal F1 hybrids generated in generation three. Using these crosses we further tested whether phenotypic changes were maternally or paternally transmitted. In generation five (G5), we assessed whether phenotypic effects persisted over two generations in the absence of stress. We found that exposure to heat stress in previous generations accelerated flowering under G4 control conditions in Sha-0, but heritable effects disappeared in G5 after two generations without stress exposure. Previous exposure to salt stress increased salt tolerance in one of two reciprocal F1 hybrids. Transgenerational effects were maternally and paternally inherited. Lacking genetic variability, maternal and paternal inheritance and reversibility of transgenerational effects together indicate that stress can induce heritable, potentially adaptive phenotypic changes, probably through epigenetic mechanisms. These effects were strongly dependent on plant genotype and may not be a general response to stress in <i>A. thaliana</i>.</p> </div>", "links"=>[], "tags"=>["induce", "transgenerational", "phenotypic"], "article_id"=>678739, "categories"=>["Developmental Biology", "Genetics", "Plant Biology", "Evolutionary Biology"], "users"=>["Léonie Suter", "Alex Widmer"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0060364.s001", "https://dx.doi.org/10.1371/journal.pone.0060364.s002", "https://dx.doi.org/10.1371/journal.pone.0060364.s003", "https://dx.doi.org/10.1371/journal.pone.0060364.s004", "https://dx.doi.org/10.1371/journal.pone.0060364.s005", "https://dx.doi.org/10.1371/journal.pone.0060364.s006"], "stats"=>{"downloads"=>10, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Environmental_Heat_and_Salt_Stress_Induce_Transgenerational_Phenotypic_Changes_in_Arabidopsis_thaliana_/678739", "title"=>"Environmental Heat and Salt Stress Induce Transgenerational Phenotypic Changes in <i>Arabidopsis thaliana</i>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-04-09 02:25:39"}

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Relative Metric

{"start_date"=>"2013-01-01T00:00:00Z", "end_date"=>"2013-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences/Organisms", "average_usage"=>[281, 484, 611, 728, 835, 934, 1030, 1123, 1214, 1299, 1383, 1464]}, {"subject_area"=>"/Engineering and technology", "average_usage"=>[254, 440, 558, 675, 785, 883, 972, 1061, 1154, 1248, 1336, 1414, 1489]}]}
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