Mechano-Chemical Aspects of Organ Formation in Arabidopsis thaliana: The Relationship between Auxin and Pectin
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{"title"=>"Mechano-Chemical Aspects of Organ Formation in Arabidopsis thaliana: The Relationship between Auxin and Pectin", "type"=>"journal", "authors"=>[{"first_name"=>"Siobhan A.", "last_name"=>"Braybrook", "scopus_author_id"=>"12767061700"}, {"first_name"=>"Alexis", "last_name"=>"Peaucelle", "scopus_author_id"=>"8115771700"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"368517989", "sgr"=>"84874884307", "issn"=>"19326203", "arxiv"=>"NIHMS150003", "pmid"=>"23554870", "scopus"=>"2-s2.0-84874884307", "doi"=>"10.1371/journal.pone.0057813", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)"}, "id"=>"247cbbbd-c91f-3ddb-9d60-30db6fa73226", "abstract"=>"How instructive signals are translated into robust and predictable changes in growth is a central question in developmental biology. Recently, much interest has centered on the feedback between chemical instructions and mechanical changes for pattern formation in development. In plants, the patterned arrangement of aerial organs, or phyllotaxis, is instructed by the phytohormone auxin; however, it still remains to be seen how auxin is linked, at the apex, to the biochemical and mechanical changes of the cell wall required for organ outgrowth. Here, using Atomic Force Microscopy, we demonstrate that auxin reduces tissue rigidity prior to organ outgrowth in the shoot apex of Arabidopsis thaliana, and that the de-methyl-esterification of pectin is necessary for this reduction. We further show that development of functional organs produced by pectin-mediated ectopic wall softening requires auxin signaling. Lastly, we demonstrate that coordinated localization of the auxin transport protein, PIN1, is disrupted in a naked-apex produced by increasing cell wall rigidity. Our data indicates that a feedback loop between the instructive chemical auxin and cell wall mechanics may play a crucial role in phyllotactic patterning.", "link"=>"http://www.mendeley.com/research/mechanochemical-aspects-organ-formation-arabidopsis-thaliana-relationship-between-auxin-pectin", "reader_count"=>129, "reader_count_by_academic_status"=>{"Unspecified"=>4, "Professor > Associate Professor"=>11, "Researcher"=>30, "Student > Doctoral Student"=>8, "Student > Ph. D. Student"=>34, "Student > Postgraduate"=>7, "Student > Master"=>18, "Other"=>5, "Student > Bachelor"=>5, "Professor"=>6, "Lecturer"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>4, "Professor > Associate Professor"=>11, "Researcher"=>30, "Student > Doctoral Student"=>8, "Student > Ph. D. Student"=>34, "Student > Postgraduate"=>7, "Student > Master"=>18, "Other"=>5, "Student > Bachelor"=>5, "Professor"=>6, "Lecturer"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>7, "Engineering"=>1, "Environmental Science"=>2, "Biochemistry, Genetics and Molecular Biology"=>12, "Materials Science"=>2, "Agricultural and Biological Sciences"=>99, "Design"=>1, "Physics and Astronomy"=>3, "Computer Science"=>1, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Design"=>{"Design"=>1}, "Engineering"=>{"Engineering"=>1}, "Materials Science"=>{"Materials Science"=>2}, "Physics and Astronomy"=>{"Physics and Astronomy"=>3}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>99}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>12}, "Unspecified"=>{"Unspecified"=>7}, "Environmental Science"=>{"Environmental Science"=>2}}, "reader_count_by_country"=>{"Netherlands"=>1, "United States"=>1, "China"=>1, "Mexico"=>1, "Kazakhstan"=>1, "France"=>3, "Germany"=>2}, "group_count"=>4}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/985265"], "description"=>"<p>(A–D) SEM images of non-transgenic meristem (A), induced PMEI3oe meristem (B), or <i>PMEI3oe</i> meristems after 24 h induction and ∼72 h recovery (C,D). After recovery, organs present abnormal size (C) and phyllotactic positioning (D). Images representative of n = 100 meristems). (E–F) Immuno labeling of PIN1 protein in meristem epidermal cells of non-transgenic (E, as in A) or 24 h induced <i>PMEI3oe</i> (F, as in B) meristems. PIN1 displays local organization of polarity in non-transgenic meristems (E), but this organization is lost in <i>PMEI3oe</i> meristems (F). Red arrows indicate direction of PIN1 polarity within cells. Insets show larger section views for orientation (further details in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0057813#pone.0057813.s008\" target=\"_blank\">Figure S8</a>). (G) Quantification of PIN orientation within L1 cells as described by the ratio of cells showing unique wall polarity to those showing PIN1 on multiple walls (<i>NT</i> n = 482 cells, <i>PMEIi</i> n = 331 cells; sampled from 12 meristems per genotype). (H) Measurement of coordination of PIN1 polarity between adjacent cells as described by the fraction of neighbors exhibiting the same PIN1 orientation within 20° (<i>NT</i> n = 384 cells, <i>PMEIi</i> n = 286 cells; sampled from 12 meristems per genotype). T-test for significant difference was applied in both cases with n = above numbers, and a significance cut-off of p-value<0.001. (I) Model for the mechano-chemical regulatory loop underlying organ formation in plants: (1) Local auxin accumulation, driven by coordinated PIN1 polarity, leads to HG de-methyl-esterification. (2) HG de-methyl-esterification causes tissue softening (directly and indirectly) which then allows for tissue outgrowth; however, (3) local auxin accumulation is again required at the new organ to obtain a functional organ, (4) and this would be affected by PIN1 polarity - which is sensitive to tissue bulging and/or HG de-methyl-esterification. M: meristem, o: organ, Scale bars  = 100 µm (A–D) or 10 µm (E–F, including insets).</p>", "links"=>[], "tags"=>["inhibition", "pectin", "de-methyl-esterification", "leads", "altered", "causes", "disorganization", "pin1"], "article_id"=>650645, "categories"=>["Physics", "Biological Sciences", "Biophysics"], "users"=>["Siobhan A. Braybrook", "Alexis Peaucelle"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0057813.g004", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Recovery_from_inhibition_of_pectin_de_methyl_esterification_leads_to_altered_organ_size_and_phyllotaxis_and_complete_inhibition_causes_a_disorganization_in_local_PIN1_polarity_/650645", "title"=>"Recovery from inhibition of pectin de-methyl-esterification leads to altered organ size and phyllotaxis, and complete inhibition causes a disorganization in local PIN1 polarity.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-13 09:47:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/985214"], "description"=>"<p>(A) IAA induced organ formation in a <i>pin1</i> mutant inflorescence apex (t = 72 h post application). Apparent Young's modulus (E<sub>A</sub>, or 'rigidity') map of a representative <i>pin1</i> meristem ∼18 hours post IAA application as determined with a 1 µm (B) or 5 µm (C) spherical tip. Total number of meristems analyzed + IAA, n = 13. Each pixel in a rigidity map corresponds to the E<sub>A</sub> value obtained from one indentation point. (D) Graphical display of averaged E<sub>A</sub> data from all meristems with values for meristem (black bars) and just above application site (white bars). Significant difference indicated by asterisk at p-value<0.01 (T-test on averages from n meristems: ‘<i>pin1</i>–IAA’ 5 µm n = 6 and 1 µm n = 7 (p-values 0.71 and 0.57 respectively), ‘<i>pin1</i>+IAA’ n = 13 (p-values: 1 µm p = 0.02, 5 µm p = 2.2E-5). Error bars are propagated standard deviations). Non-averaged results for all meristems can be found in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0057813#pone.0057813.s001\" target=\"_blank\">Figure S1</a> (displaying reduced rigidity: 1 µm, +Inactive IAA n = 0/7, +IAA n = 1/13. 5 µm, +Inactive IAA n = 3/7, +IAA n = 13/13). (E,F) Topographical reconstruction of measured surfaces, as estimated by AFM point-of-contact, with the rigidity maps of (B,C) respectively used to color the surface. Note that meristem curvature does not correlate with areas of decreased E<sub>A</sub>, and that there is no bulging of the meristem accompanying decreased rigidity. (G) Serial transverse sections showing 2F4 labeling of HG de-methyl-esterification in a representative <i>pin1</i> meristem ∼18 hours after IAA application (n = 9). M: meristem, as: application site, Scale bars  = 100 µm (A,G) or 10 µm (B,C). Asterisk in (G) indicates 2F4 labeling in sub-epidermal tissues. Statistics in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0057813#pone.0057813.s002\" target=\"_blank\">Figure S2</a>, control data in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0057813#pone.0057813.s003\" target=\"_blank\">Figure S3</a>.</p>", "links"=>[], "tags"=>["meristem", "leads", "softening", "pectin", "de-methyl-esterification", "sub-epidermal"], "article_id"=>650614, "categories"=>["Physics", "Biological Sciences", "Biophysics"], "users"=>["Siobhan A. Braybrook", "Alexis Peaucelle"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0057813.g001", "stats"=>{"downloads"=>1, "page_views"=>21, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_IAA_application_on_pin1_meristem_leads_to_local_tissue_softening_and_pectin_de_methyl_esterification_in_sub_epidermal_tissues_/650614", "title"=>"IAA application on <i>pin1</i> meristem leads to local tissue softening and pectin de-methyl-esterification in sub-epidermal tissues.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-13 09:43:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/985301", "https://ndownloader.figshare.com/files/985306", "https://ndownloader.figshare.com/files/985330", "https://ndownloader.figshare.com/files/985342", "https://ndownloader.figshare.com/files/985346", "https://ndownloader.figshare.com/files/985350", "https://ndownloader.figshare.com/files/985351", "https://ndownloader.figshare.com/files/985359", "https://ndownloader.figshare.com/files/985363"], "description"=>"<div><p>How instructive signals are translated into robust and predictable changes in growth is a central question in developmental biology. Recently, much interest has centered on the feedback between chemical instructions and mechanical changes for pattern formation in development. In plants, the patterned arrangement of aerial organs, or phyllotaxis, is instructed by the phytohormone auxin; however, it still remains to be seen how auxin is linked, at the apex, to the biochemical and mechanical changes of the cell wall required for organ outgrowth. Here, using Atomic Force Microscopy, we demonstrate that auxin reduces tissue rigidity prior to organ outgrowth in the shoot apex of <i>Arabidopsis thaliana</i>, and that the de-methyl-esterification of pectin is necessary for this reduction. We further show that development of functional organs produced by pectin-mediated ectopic wall softening requires auxin signaling. Lastly, we demonstrate that coordinated localization of the auxin transport protein, PIN1, is disrupted in a naked-apex produced by increasing cell wall rigidity. Our data indicates that a feedback loop between the instructive chemical auxin and cell wall mechanics may play a crucial role in phyllotactic patterning.</p></div>", "links"=>[], "tags"=>["mechano-chemical", "aspects", "auxin", "pectin"], "article_id"=>650671, "categories"=>["Physics", "Biological Sciences", "Biophysics"], "users"=>["Siobhan A. Braybrook", "Alexis Peaucelle"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0057813.s001", "https://dx.doi.org/10.1371/journal.pone.0057813.s002", "https://dx.doi.org/10.1371/journal.pone.0057813.s003", "https://dx.doi.org/10.1371/journal.pone.0057813.s004", "https://dx.doi.org/10.1371/journal.pone.0057813.s005", "https://dx.doi.org/10.1371/journal.pone.0057813.s006", "https://dx.doi.org/10.1371/journal.pone.0057813.s007", "https://dx.doi.org/10.1371/journal.pone.0057813.s008", "https://dx.doi.org/10.1371/journal.pone.0057813.s009"], "stats"=>{"downloads"=>12, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Mechano_Chemical_Aspects_of_Organ_Formation_in_Arabidopsis_thaliana_The_Relationship_between_Auxin_and_Pectin_/650671", "title"=>"Mechano-Chemical Aspects of Organ Formation in <em>Arabidopsis thaliana</em>: The Relationship between Auxin and Pectin", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-03-13 09:49:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/985256"], "description"=>"<p>SEM images of representative untreated (A) or PME treated <i>pin1</i> (B,C) meristems ∼72 h after treatment. Close ups of untreated meristem flank (D) or treated flank (E). (F) Direct magnification of the treated meristem in (C). Lateral stem bulging at the application site was observed on all treated plants (shaded yellow, n = 22), and stick-like lateral organs were observed in some samples (shaded green, n = 6/22). The two phenomena could be observed on the same stem (E). Young's modulus (E<sub>A</sub>, or 'rigidity') map of a representative <i>pin1</i> meristem treated with inactive PME (G) or active PME (H) as observed with a 5 µm spherical tip, ∼18 h post application. (I) Graphical display of averaged E<sub>A</sub> data from PME treated (n = 6) or inactive PME treated (n = 3) meristems with values for meristem (black bars) and application site (white bars) (T-test on averages from n meristems: <i>pin1</i>-PME n = 3, p-value = 0.54; <i>pin1</i>+PME n = 6, p-value = 4.3E-3; significant difference at p-value<0.001, asterisk. Error bars are propagated standard deviations, statistics in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0057813#pone.0057813.s002\" target=\"_blank\">Fig. S2</a>). Non-averaged results for meristems displaying reduced rigidity can be found in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0057813#pone.0057813.s007\" target=\"_blank\">Figure S7</a> (+Inactive PME n = 0/3, +IAA n = 3/3, +PME n = 5/6). (J) <i>DR5:GFP</i> signal (green) in a representative <i>pin1</i> meristem with IAA application, and (K) with PME application. Cell walls stained with propidium iodide (yellow). Insets in J–K show <i>DR5:GFP</i> signal alone. M: meristem, as: application site, Scale bars  = 100 µm (A–C), 50 µm (D–F) or 10 µm (G,H,J,K). <i>DR5:GFP</i> data for all meristems in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0057813#pone.0057813.s008\" target=\"_blank\">Figure S8</a>.</p>", "links"=>[], "tags"=>["meristems", "leads", "bulging"], "article_id"=>650638, "categories"=>["Physics", "Biological Sciences", "Biophysics"], "users"=>["Siobhan A. Braybrook", "Alexis Peaucelle"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0057813.g003", "stats"=>{"downloads"=>1, "page_views"=>21, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_PME_application_on_pin1_meristems_leads_to_tissue_bulging_and_local_tissue_softening_but_not_functional_organ_development_/650638", "title"=>"PME application on <i>pin1</i> meristems leads to tissue bulging and local tissue softening, but not functional organ development.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-13 09:46:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/985234"], "description"=>"<p>(A)Representative <i>PMEI3oe</i> meristem ∼24 hours after PMEI induction. (B) Representative induced <i>PMEI3oe</i> meristem ∼72 hours post IAA application. (C,D) Apparent Young's modulus (E<sub>A</sub>, or 'rigidity') map of a representative control (C) or IAA applied (D) <i>PMEI3oe</i> meristem ∼18 hours after treatment as visualized with a 5 µm spherical tip. Analyzed meristems: control (n = 11), +IAA (n = 9). (E) Graphical display of averaged E<sub>A</sub> data from all meristems with values for meristem (black bars) and just above application site (white bars). No significant difference was found in either treatment or control (T-test on averages from n meristems: <i>PMEI3oe</i> -IAA n = 9, meristem vs. periphery p-value  = 0.037; <i>PMEI3oe</i> +IAA n = 11, meristem vs. periphery p-value = 0.098. Error bars are propagated standard deviations. Statistics in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0057813#pone.0057813.s002\" target=\"_blank\">Fig. S2</a>); both showed higher variability than non-transgenic meristems. Non-averaged results for all meristems can be found in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0057813#pone.0057813.s006\" target=\"_blank\">Figure S6</a> (displaying reduced rigidity: +Inactive IAA n = 1/11, +IAA n = 2/9). M: meristem, as: application site, Scale bars  = 100 µm (A,B) or 10 µm (C,D).</p>", "links"=>[], "tags"=>["pectin", "de-methyl-esterification", "inhibits", "iaa-induced"], "article_id"=>650631, "categories"=>["Physics", "Biological Sciences", "Biophysics"], "users"=>["Siobhan A. Braybrook", "Alexis Peaucelle"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0057813.g002", "stats"=>{"downloads"=>0, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Blocking_pectin_de_methyl_esterification_inhibits_IAA_induced_organ_formation_and_tissue_softening_/650631", "title"=>"Blocking pectin de-methyl-esterification inhibits IAA-induced organ formation and tissue softening.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-13 09:45:18"}

PMC Usage Stats | Further Information

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Relative Metric

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