Aphid Thermal Tolerance Is Governed by a Point Mutation in Bacterial Symbionts
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{"title"=>"Aphid thermal tolerance is governed by a point mutation in bacterial symbionts", "type"=>"journal", "authors"=>[{"first_name"=>"Helen E.", "last_name"=>"Dunbar", "scopus_author_id"=>"6603564441"}, {"first_name"=>"Alex C.C.", "last_name"=>"Wilson", "scopus_author_id"=>"55458730500"}, {"first_name"=>"Nicole R.", "last_name"=>"Ferguson", "scopus_author_id"=>"8950663000"}, {"first_name"=>"Nancy A.", "last_name"=>"Moran", "scopus_author_id"=>"7103226925"}], "year"=>2007, "source"=>"PLoS Biology", "identifiers"=>{"scopus"=>"2-s2.0-34249106083", "doi"=>"10.1371/journal.pbio.0050096", "sgr"=>"34249106083", "isbn"=>"1545-7885 (Electronic)", "pmid"=>"17425405", "issn"=>"15449173", "pui"=>"46790391"}, "id"=>"7983403e-2fe1-315a-9cf6-ddd249863ad5", "abstract"=>"Symbiosis is a ubiquitous phenomenon generating biological complexity, affecting adaptation, and expanding ecological capabilities. However, symbionts, which can be subject to genetic limitations such as clonality and genomic degradation, also impose constraints on hosts. A model of obligate symbiosis is that between aphids and the bacterium Buchnera aphidicola, which supplies essential nutrients. We report a mutation in Buchnera of the aphid Acyrthosiphon pisum that recurs in laboratory lines and occurs in field populations. This single nucleotide deletion affects a homopolymeric run within the heat-shock transcriptional promoter for ibpA, encoding a small heat-shock protein. This Buchnera mutation virtually eliminates the transcriptional response of ibpA to heat stress and lowers its expression even at cool or moderate temperatures. Furthermore, this symbiont mutation dramatically affects host fitness in a manner dependent on thermal environment. Following a short heat exposure as juveniles, aphids bearing short-allele symbionts produced few or no progeny and contained almost no Buchnera, in contrast to aphids bearing symbionts without the deletion. Conversely, under constant cool conditions, aphids containing symbionts with the short allele reproduced earlier and maintained higher reproductive rates. The short allele has appreciable frequencies in field populations (up to 20%), further supporting the view that lowering of ibpA expression improves host fitness under some conditions. This recurring Buchnera mutation governs thermal tolerance of aphid hosts. Other cases in which symbiont microevolution has a major effect on host ecological tolerance are likely to be widespread because of the high mutation rates of symbiotic bacteria and their crucial roles in host metabolism and development.", "link"=>"http://www.mendeley.com/research/aphid-thermal-tolerance-governed-point-mutation-bacterial-symbionts", "reader_count"=>231, "reader_count_by_academic_status"=>{"Unspecified"=>10, "Professor > Associate Professor"=>18, "Researcher"=>52, "Student > Doctoral Student"=>11, "Student > Ph. D. Student"=>62, "Student > Postgraduate"=>9, "Student > Master"=>26, "Other"=>3, "Student > Bachelor"=>20, "Lecturer"=>2, "Lecturer > Senior Lecturer"=>2, "Professor"=>16}, "reader_count_by_user_role"=>{"Unspecified"=>10, "Professor > Associate Professor"=>18, "Researcher"=>52, "Student > Doctoral Student"=>11, "Student > Ph. D. Student"=>62, "Student > Postgraduate"=>9, "Student > Master"=>26, "Other"=>3, "Student > Bachelor"=>20, "Lecturer"=>2, "Lecturer > Senior Lecturer"=>2, "Professor"=>16}, "reader_count_by_subject_area"=>{"Unspecified"=>19, "Environmental Science"=>14, "Biochemistry, Genetics and Molecular Biology"=>15, "Mathematics"=>1, "Agricultural and Biological Sciences"=>177, "Medicine and Dentistry"=>1, "Philosophy"=>1, "Physics and Astronomy"=>2, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>2}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>177}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>15}, "Mathematics"=>{"Mathematics"=>1}, "Unspecified"=>{"Unspecified"=>19}, "Environmental Science"=>{"Environmental Science"=>14}, "Philosophy"=>{"Philosophy"=>1}}, "reader_count_by_country"=>{"United States"=>5, "United Kingdom"=>1, "Portugal"=>1, "India"=>1, "Spain"=>2, "New Zealand"=>1, "Canada"=>3, "Czech Republic"=>1, "Belgium"=>1, "Poland"=>2, "Brazil"=>1, "Mexico"=>1, "South Africa"=>2, "France"=>3, "Germany"=>1}, "group_count"=>10}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/950704"], "description"=>"<div><p>(A) Gene expression changes in response to heat treatment (35 °C) as measured from a microarray experiment, including two control genes <i>(argG</i> and <i>cysG)</i> that did not show significant responses to heat treatment. Each bar represents the mean of technical and biological replicates of each line (four arrays/aphid line) ± standard error.</p>\n <p>(B) Gene expression changes in response to heat (35 °C) as measured with RT-qPCR using several A. pisum lines containing <i>Buchnera</i> with either short or long <i>ibpA</i> promoter alleles. For the long allele, <i>n</i> = 4 (three lines), and for the short allele, <i>n</i> = 2 (two lines). Error bars indicate means ± standard errors.</p>\n <p>(C) Effects of exposure to different temperatures on <i>ibpA</i> expression for three aphid lines bearing <i>Buchnera</i> with different <i>ibpA</i> promoter alleles. The two 5A lines differ only in the single-base deletion affecting the length of the <i>ibpA</i> spacer; whereas TUC matches 5A-long for the <i>ibpA</i> promoter sequence, but shows other differences from 5A lines throughout the <i>Buchnera</i> genome. Pairwise differences between the two 5A-derived lines are significant at every temperature, with the long allele always showing higher expression relative to a control gene <i>(cysG)</i>. TUC has other sequence differences, and these appear to have minor effects on <i>ibpA</i> expression.</p></div>", "links"=>[], "tags"=>["genes", "up-regulated"], "article_id"=>621026, "categories"=>["Ecology", "Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Helen E Dunbar", "Alex C. C Wilson", "Nicole R Ferguson", "Nancy A Moran"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.0050096.g002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Response_to_Heat_Treatment_in_Buchnera_Ap_lines_for_Genes_Typically_Up_Regulated_in_Response_to_Heat_/621026", "title"=>"Response to Heat Treatment in <i>Buchnera</i>-Ap lines, for Genes Typically Up-Regulated in Response to Heat", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2007-04-10 00:17:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/468562"], "description"=>"<div><p>Symbiosis is a ubiquitous phenomenon generating biological complexity, affecting adaptation, and expanding ecological capabilities. However, symbionts, which can be subject to genetic limitations such as clonality and genomic degradation, also impose constraints on hosts. A model of obligate symbiosis is that between aphids and the bacterium <em>Buchnera aphidicola,</em> which supplies essential nutrients. We report a mutation in <em>Buchnera</em> of the aphid Acyrthosiphon pisum that recurs in laboratory lines and occurs in field populations. This single nucleotide deletion affects a homopolymeric run within the heat-shock transcriptional promoter for <em>ibpA,</em> encoding a small heat-shock protein. This <em>Buchnera</em> mutation virtually eliminates the transcriptional response of <em>ibpA</em> to heat stress and lowers its expression even at cool or moderate temperatures. Furthermore, this symbiont mutation dramatically affects host fitness in a manner dependent on thermal environment. Following a short heat exposure as juveniles, aphids bearing short-allele symbionts produced few or no progeny and contained almost no <em>Buchnera,</em> in contrast to aphids bearing symbionts without the deletion. Conversely, under constant cool conditions, aphids containing symbionts with the short allele reproduced earlier and maintained higher reproductive rates. The short allele has appreciable frequencies in field populations (up to 20%), further supporting the view that lowering of <em>ibpA</em> expression improves host fitness under some conditions. This recurring <em>Buchnera</em> mutation governs thermal tolerance of aphid hosts. Other cases in which symbiont microevolution has a major effect on host ecological tolerance are likely to be widespread because of the high mutation rates of symbiotic bacteria and their crucial roles in host metabolism and development.</p> </div>", "links"=>[], "tags"=>["aphid", "thermal", "governed", "mutation", "bacterial", "symbionts"], "article_id"=>152388, "categories"=>["Ecology", "Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Helen E Dunbar", "Alex C. C Wilson", "Nicole R Ferguson", "Nancy A Moran"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.0050096", "stats"=>{"downloads"=>4, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Aphid_Thermal_Tolerance_Is_Governed_by_a_Point_Mutation_in_Bacterial_Symbionts_/152388", "title"=>"Aphid Thermal Tolerance Is Governed by a Point Mutation in Bacterial Symbionts", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2007-04-10 00:39:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/950940"], "description"=>"<p>Number of nymphs per day for the first 6 d of reproduction for 5A females with <i>Buchnera</i> bearing the long and short alleles (5A<sup>−</sup>R<sup>LONG</sup>and 5A<sup>SHORT</sup>). Bars show means ± standard errors. Temperature conditions were constant 15 °C, constant 20 °C, and 20 °C with 4 h at 35 °C on day 2 following birth.</p>", "links"=>[], "tags"=>["rates", "aphid", "lines", "promoter"], "article_id"=>621258, "categories"=>["Ecology", "Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Helen E Dunbar", "Alex C. C Wilson", "Nicole R Ferguson", "Nancy A Moran"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.0050096.g005", "stats"=>{"downloads"=>1, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Reproductive_Rates_under_Different_Temperature_Conditions_of_Aphid_Lines_with_Buchnera_with_Different_ibpA_Promoter_Alleles_/621258", "title"=>"Reproductive Rates under Different Temperature Conditions of Aphid Lines with <i>Buchnera</i> with Different <i>ibpA</i> Promoter Alleles", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2007-04-10 00:20:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/950619"], "description"=>"<div><p>(A) Schematic of regulation of <i>ibpA</i> expression showing position of heat-shock promoter.</p>\n <p>(B) Sequence of E. coli consensus heat-shock promoter and of all heat-shock promoters of <i>Buchnera</i> of S. graminum and of A. pisum. Sequences from published complete genome data were confirmed for both species. The only variant is the <i>ibpA</i> promoter allele, which has a shorter spacer length, resulting in almost complete loss of the heat-shock response of <i>ibpA</i>.</p></div>", "links"=>[], "tags"=>["promoter", "governing", "heat-shock"], "article_id"=>620939, "categories"=>["Ecology", "Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Helen E Dunbar", "Alex C. C Wilson", "Nicole R Ferguson", "Nancy A Moran"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.0050096.g001", "stats"=>{"downloads"=>1, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Heat_Shock_Promoter_Governing_Expression_of_the_Heat_Shock_Gene_ibpA_in_Buchnera_/620939", "title"=>"Heat-Shock Promoter Governing Expression of the Heat-Shock Gene <i>ibpA</i> in <i>Buchnera</i>", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2007-04-10 00:15:39"}
  • {"files"=>["https://ndownloader.figshare.com/files/951019"], "description"=>"<p>Estimates of <i>Buchnera</i> and aphid genome numbers are based on qPCR assays of genomic DNA determining numbers of copies of single-copy <i>Buchnera</i> genes relative to a single-copy aphid gene. Heat treatment was 4 h at 35 °C on day 2 following birth, and measures were taken within 24 h of attaining adulthood. Bars show means ± standard errors.</p>", "links"=>[], "tags"=>["densities", "aphids", "bearing", "promoter"], "article_id"=>621340, "categories"=>["Ecology", "Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Helen E Dunbar", "Alex C. C Wilson", "Nicole R Ferguson", "Nancy A Moran"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.0050096.g006", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effect_of_Heat_Stress_on_Buchnera_Densities_in_Aphids_Bearing_Buchnera_with_Different_ibpA_Promoter_Alleles_/621340", "title"=>"Effect of Heat Stress on <i>Buchnera</i> Densities in Aphids Bearing <i>Buchnera</i> with Different <i>ibpA</i> Promoter Alleles", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2007-04-10 00:22:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/950858"], "description"=>"<p>Bars show means ± standard errors.</p>", "links"=>[], "tags"=>["treatments", "fecundity", "aphid", "lines", "promoter"], "article_id"=>621182, "categories"=>["Ecology", "Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Helen E Dunbar", "Alex C. C Wilson", "Nicole R Ferguson", "Nancy A Moran"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.0050096.g004", "stats"=>{"downloads"=>2, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effect_of_Different_Temperature_Treatments_on_Day_2_on_Fecundity_as_Adults_for_Aphid_Lines_with_Buchnera_with_Different_ibpA_Promoter_Alleles_/621182", "title"=>"Effect of Different Temperature Treatments on Day 2 on Fecundity as Adults, for Aphid Lines with <i>Buchnera</i> with Different <i>ibpA</i> Promoter Alleles", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2007-04-10 00:19:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/950768"], "description"=>"<p>Line 5A was initiated from a single female in June 1999. In September 2000, it was transfected with a secondary symbiont to generate 5A<sup>+</sup>R<sup>LONG</sup>. Subsequently the 5A line acquired the first mutation to the short promoter allele, which became fixed. An identical mutation rose to near fixation in the 5A<sup>+</sup>R<sup>LONG</sup> culture in October 2005; both alleles were isolated from that colony to yield 5A<sup>+</sup>R<sup>SHORT</sup> and 5A<sup>+</sup>R<sup>LONG</sup>. Line 5A<sup>+</sup>R<sup>SHORT</sup> lost its <i>Candidatus</i> Serratia symbiotica to generate line 5A<sup>−</sup>R<sup>SHORT</sup>, and then in November 2005, 5A<sup>+</sup>R<sup>LONG</sup> was cured of <i>Candidatus</i> Serratia symbiotica to generate line 5A<sup>−</sup>R<sup>LONG</sup>. Thus the mutation occurred and rose to fixation or near fixation twice in sublines of the 5A laboratory line (<a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.0050096#pbio-0050096-g001\" target=\"_blank\">Figure 1</a>B).</p>", "links"=>[], "tags"=>["heat-shock", "promoter", "sublines", "5a"], "article_id"=>621087, "categories"=>["Ecology", "Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Helen E Dunbar", "Alex C. C Wilson", "Nicole R Ferguson", "Nancy A Moran"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.0050096.g003", "stats"=>{"downloads"=>1, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Chronology_of_ibpA_Heat_Shock_Promoter_Evolution_in_Sublines_of_the_5A_Line_/621087", "title"=>"Chronology of <i>ibpA</i> Heat-Shock Promoter Evolution in Sublines of the 5A Line", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2007-04-10 00:18:07"}

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Relative Metric

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