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{"title"=>"Predicting the Impact of Alternative Splicing on Plant MADS Domain Protein Function", "type"=>"journal", "authors"=>[{"first_name"=>"Edouard I.", "last_name"=>"Severing"}, {"first_name"=>"Aalt D. J.", "last_name"=>"van Dijk"}, {"first_name"=>"Giuseppa", "last_name"=>"Morabito"}, {"first_name"=>"Jacqueline", "last_name"=>"Busscher-Lange"}, {"first_name"=>"Richard G. H.", "last_name"=>"Immink"}, {"first_name"=>"Roeland C. H. J.", "last_name"=>"van Ham"}], "year"=>2012, "source"=>"PLoS ONE", "identifiers"=>{"doi"=>"10.1371/journal.pone.0030524", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pmid"=>"22295091", "issn"=>"1932-6203"}, "id"=>"7126b802-57cb-3412-b0df-5b00b707afc1", "abstract"=>"Several genome-wide studies demonstrated that alternative splicing (AS) significantly increases the transcriptome complexity in plants. However, the impact of AS on the functional diversity of proteins is difficult to assess using genome-wide approaches. The availability of detailed sequence annotations for specific genes and gene families allows for a more detailed assessment of the potential effect of AS on their function. One example is the plant MADS-domain transcription factor family, members of which interact to form protein complexes that function in transcription regulation. Here, we perform an in silico analysis of the potential impact of AS on the protein-protein interaction capabilities of MIKC-type MADS-domain proteins. We first confirmed the expression of transcript isoforms resulting from predicted AS events. Expressed transcript isoforms were considered functional if they were likely to be translated and if their corresponding AS events either had an effect on predicted dimerisation motifs or occurred in regions known to be involved in multimeric complex formation, or otherwise, if their effect was conserved in different species. Nine out of twelve MIKC MADS-box genes predicted to produce multiple protein isoforms harbored putative functional AS events according to those criteria. AS events with conserved effects were only found at the borders of or within the K-box domain. We illustrate how AS can contribute to the evolution of interaction networks through an example of selective inclusion of a recently evolved interaction motif in the MADS AFFECTING FLOWERING1-3 (MAF1-3) subclade. Furthermore, we demonstrate the potential effect of an AS event in SHORT VEGETATIVE PHASE (SVP), resulting in the deletion of a short sequence stretch including a predicted interaction motif, by overexpression of the fully spliced and the alternatively spliced SVP transcripts. For most of the AS events we were able to formulate hypotheses about the potential impact on the interaction capabilities of the encoded MIKC proteins.", "link"=>"http://www.mendeley.com/research/predicting-impact-alternative-splicing-plant-mads-domain-protein-function", "reader_count"=>62, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>3, "Researcher"=>14, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>20, "Student > Postgraduate"=>3, "Student > Master"=>8, "Student > Bachelor"=>3, "Lecturer"=>2, "Lecturer > Senior Lecturer"=>1, "Professor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>3, "Researcher"=>14, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>20, "Student > Postgraduate"=>3, "Student > Master"=>8, "Student > Bachelor"=>3, "Lecturer"=>2, "Lecturer > Senior Lecturer"=>1, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Biochemistry, Genetics and Molecular Biology"=>7, "Agricultural and Biological Sciences"=>47, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Chemistry"=>3, "Computer Science"=>1}, "reader_count_by_subdiscipline"=>{"Chemistry"=>{"Chemistry"=>3}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>47}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>7}, "Unspecified"=>{"Unspecified"=>3}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"United States"=>1, "Mexico"=>1, "France"=>1, "Germany"=>2, "India"=>1}, "group_count"=>4}

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• http://doi.org/10.1038/nature12633
• http://doi.org/10.1002/pld3.60
• http://doi.org/10.1093/nar/gkt1362
• http://doi.org/10.1186/1471-2164-14-689
• http://doi.org/10.1038/nplants.2016.55
• http://doi.org/10.1016/j.tplants.2015.11.015
• http://doi.org/10.1016/j.tplants.2012.06.001
• http://doi.org/10.1038/srep44948
• http://doi.org/10.1007/s00299-017-2140-1
• http://doi.org/10.3390/genes10020091
• http://doi.org/10.1038/nplants.2017.53
• http://doi.org/10.1016/j.csbj.2019.06.014
• http://doi.org/10.1109/TCBB.2012.165
• http://doi.org/10.3390/biology2041311
• http://doi.org/10.1016/j.jplph.2014.08.017
• http://doi.org/10.1371/journal.pone.0078944
• http://doi.org/10.1093/dnares/dss041
• http://doi.org/10.1007/s00425-013-1882-4
• http://doi.org/10.3389/fpls.2018.01625
• http://doi.org/10.1016/j.tplants.2014.03.009
• http://doi.org/10.1007/s11103-012-9982-2
• http://doi.org/10.3389/fpls.2019.00707
• http://doi.org/10.1007/s00344-019-10008-z
• http://doi.org/10.1371/journal.pone.0091896
• http://doi.org/10.1016/j.envexpbot.2014.01.003
• http://doi.org/10.1093/pcp/pcz124
• http://doi.org/10.1371/journal.pbio.1001835
• http://doi.org/10.1093/nar/gky095
• http://doi.org/10.3389/fpls.2019.00740

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Figshare

• {"files"=>["https://ndownloader.figshare.com/files/350747", "https://ndownloader.figshare.com/files/350782", "https://ndownloader.figshare.com/files/350810", "https://ndownloader.figshare.com/files/350844", "https://ndownloader.figshare.com/files/350869", "https://ndownloader.figshare.com/files/350917", "https://ndownloader.figshare.com/files/350974", "https://ndownloader.figshare.com/files/351024", "https://ndownloader.figshare.com/files/351062", "https://ndownloader.figshare.com/files/351163", "https://ndownloader.figshare.com/files/351221"], "description"=>"<div><p>Several genome-wide studies demonstrated that alternative splicing (AS) significantly increases the transcriptome complexity in plants. However, the impact of AS on the functional diversity of proteins is difficult to assess using genome-wide approaches. The availability of detailed sequence annotations for specific genes and gene families allows for a more detailed assessment of the potential effect of AS on their function. One example is the plant MADS-domain transcription factor family, members of which interact to form protein complexes that function in transcription regulation. Here, we perform an <em>in silico</em> analysis of the potential impact of AS on the protein-protein interaction capabilities of MIKC-type MADS-domain proteins. We first confirmed the expression of transcript isoforms resulting from predicted AS events. Expressed transcript isoforms were considered functional if they were likely to be translated and if their corresponding AS events either had an effect on predicted dimerisation motifs or occurred in regions known to be involved in multimeric complex formation, or otherwise, if their effect was conserved in different species. Nine out of twelve MIKC MADS-box genes predicted to produce multiple protein isoforms harbored putative functional AS events according to those criteria. AS events with conserved effects were only found at the borders of or within the K-box domain. We illustrate how AS can contribute to the evolution of interaction networks through an example of selective inclusion of a recently evolved interaction motif in the MADS AFFECTING FLOWERING1-3 (MAF1–3) subclade. Furthermore, we demonstrate the potential effect of an AS event in SHORT VEGETATIVE PHASE (SVP), resulting in the deletion of a short sequence stretch including a predicted interaction motif, by overexpression of the fully spliced and the alternatively spliced <em>SVP</em> transcripts. For most of the AS events we were able to formulate hypotheses about the potential impact on the interaction capabilities of the encoded MIKC proteins.</p> </div>", "links"=>[], "tags"=>["predicting", "splicing", "mads"], "article_id"=>129337, "categories"=>["Biochemistry", "Biological Sciences", "Physics", "Biophysics", "Cell Biology"], "users"=>["Edouard I. Severing", "Aalt D. J. van Dijk", "Giuseppa Morabito", "Jacqueline Busscher-Lange", "Richard G. H. Immink", "Roeland C. H. J. van Ham"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0030524.s001", "https://dx.doi.org/10.1371/journal.pone.0030524.s002", "https://dx.doi.org/10.1371/journal.pone.0030524.s003", "https://dx.doi.org/10.1371/journal.pone.0030524.s004", "https://dx.doi.org/10.1371/journal.pone.0030524.s005", "https://dx.doi.org/10.1371/journal.pone.0030524.s006", "https://dx.doi.org/10.1371/journal.pone.0030524.s007", "https://dx.doi.org/10.1371/journal.pone.0030524.s008", "https://dx.doi.org/10.1371/journal.pone.0030524.s009", "https://dx.doi.org/10.1371/journal.pone.0030524.s010", "https://dx.doi.org/10.1371/journal.pone.0030524.s011"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Predicting_the_Impact_of_Alternative_Splicing_on_Plant_MADS_Domain_Protein_Function/129337", "title"=>"Predicting the Impact of Alternative Splicing on Plant MADS Domain Protein Function", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-01-25 02:35:37"}
• {"files"=>["https://ndownloader.figshare.com/files/688500"], "description"=>"<p>Triangles indicate the position of AS events in relation to the protein-domain architecture of MIKC proteins. Bars on top of the triangles indicate that the event overlapped with at least one computationally predicted interaction motif. Asterisks indicate that the transcripts associated with the AS events are not annotated in TAIR 10. The color of a triangle indicates whether the AS induced polymorphism corresponding to the event was only identified in <i>Arabidopsis</i> (white), was conserved between different species but was not observed in <i>Arabidopsis</i> (grey) or, was conserved between <i>Arabidopsis</i> and other species (black).</p>", "links"=>[], "tags"=>["splicing", "events", "mikc-type", "mads-box"], "article_id"=>358983, "categories"=>["Biochemistry", "Biological Sciences", "Physics", "Biophysics", "Plant Biology"], "users"=>["Edouard I. Severing", "Aalt D. J. van Dijk", "Giuseppa Morabito", "Jacqueline Busscher-Lange", "Richard G. H. Immink", "Roeland C. H. J. van Ham"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0030524.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Putatively_functional_Alternative_Splicing_AS_events_in_the_Arabidopsis_MIKC_type_MADS_box_family_/358983", "title"=>"Putatively functional Alternative Splicing (AS) events in the <i>Arabidopsis</i> MIKC-type MADS-box family.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-01-25 02:29:43"}
• {"files"=>["https://ndownloader.figshare.com/files/688579"], "description"=>"<p><b>A</b>) Graphical representation of protein-protein interaction capacity of the SVP1 (black) and SVP3 (grey) splicing variants as determined by matrix-based yeast two-hybrid studies (Van Dijk et al, 2010). <b>B</b>) and <b>C</b>) Effect of ectopic expression of <i>SVP1</i> (CZN094) and <i>SVP3</i> (CZN756) on flowering-time under short day conditions. Flowering-time was assessed using days until bolting (<b>B</b>) as well as the number of rosette leaves (<b>C</b>). For both constructs, flowering-time of three segregating lines was analyzed and compared to flowering-time of wild type control plants. * denotes statistical significance with p<0.01 (<i>t</i>-test). <b>D</b>) Floral phenotypes upon ectopic expression of <i>SVP1</i>. First and second whorl organs are greenish and leaf-like and flowers are partially sterile due to reduced anther filament elongation.</p>", "links"=>[], "tags"=>["vegetative"], "article_id"=>359065, "categories"=>["Biochemistry", "Biological Sciences", "Physics", "Biophysics", "Plant Biology"], "users"=>["Edouard I. Severing", "Aalt D. J. van Dijk", "Giuseppa Morabito", "Jacqueline Busscher-Lange", "Richard G. H. Immink", "Roeland C. H. J. van Ham"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0030524.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Functional_analysis_of_two_SHORT_VEGETATIVE_PHASE_SVP_isoforms_/359065", "title"=>"Functional analysis of two <i>SHORT VEGETATIVE PHASE (SVP)</i> isoforms.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-01-25 02:31:05"}
• {"files"=>["https://ndownloader.figshare.com/files/688681"], "description"=>"<p>A neighbor-joining tree illustrates the phylogenetic relationship between homologs of the <i>Arabidopsis AG</i> protein. Nodes with less than 70% bootstrap support are indicated with grey triangles. Except for <i>Zea mays</i>, which was included as outgroup species, the taxa within the tree are either members of the <i>Brassicaceae</i> subfamily or the <i>Asteridae</i> class. Residues behind taxon names correspond to the AIP sequence segment and an asterisk indicates that only the inserted residue(s) were found. No insertions were found in <i>Arabidopsis</i> and in <i>P. hybrida</i>. The distinct insertions found in <i>R. raphanistrum</i> might be the result of different allelic variants or sequencing errors. Note that the sequences from the taxa within the <i>Asteridae</i> are homologs of the <i>FARINELLI (FAR)</i> gene in <i>Antirrhinum majus.</i> The full names of the species used in this tree are provided in the <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0030524#s4\" target=\"_blank\">Material and Methods</a> section. The alignment corresponding to this tree is provided in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0030524#pone.0030524.s005\" target=\"_blank\">Figure S5</a>.</p>", "links"=>[], "tags"=>["induced", "polymorphisms", "homologs", "agamous"], "article_id"=>359171, "categories"=>["Biochemistry", "Biological Sciences", "Physics", "Biophysics", "Plant Biology"], "users"=>["Edouard I. Severing", "Aalt D. J. van Dijk", "Giuseppa Morabito", "Jacqueline Busscher-Lange", "Richard G. H. Immink", "Roeland C. H. J. van Ham"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0030524.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Conservation_of_AS_induced_polymorphisms_AIPs_between_homologs_of_the_Arabidopsis_AGAMOUS_AG_protein_/359171", "title"=>"Conservation of AS induced polymorphisms (AIPs) between homologs of the <i>Arabidopsis AGAMOUS (AG)</i> protein.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-01-25 02:32:51"}
• {"files"=>["https://ndownloader.figshare.com/files/688739"], "description"=>"<p>Conserved intron positions of the <i>Arabidopsis ABS</i>, <i>STK</i>, <i>AG</i> and <i>SHP2</i> genes are represented by horizontal lines and their flanking exons by rectangles. Grey colored regions correspond to predicted interaction motifs that overlap with AIPs. The light grey motif only overlaps the AIP in <i>STK</i>. <b>M1</b>: Homologous interaction motifs that overlap with AIPs in <i>ABS</i> and <i>STK</i>. <b>M2</b>: Homologous interaction motifs that overlap with AIPs in <i>STK</i>, <i>AG</i>, and <i>SHP-2</i>.</p>", "links"=>[], "tags"=>["motifs", "overlapping"], "article_id"=>359234, "categories"=>["Biochemistry", "Biological Sciences", "Physics", "Biophysics", "Plant Biology"], "users"=>["Edouard I. Severing", "Aalt D. J. van Dijk", "Giuseppa Morabito", "Jacqueline Busscher-Lange", "Richard G. H. Immink", "Roeland C. H. J. van Ham"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0030524.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Homologous_interaction_motifs_overlapping_with_AIPs_/359234", "title"=>"Homologous interaction motifs overlapping with AIPs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-01-25 02:33:54"}
• {"files"=>["https://ndownloader.figshare.com/files/688798"], "description"=>"<p>Two <i>MADS AFFECTING FLOWERING1</i> (<i>MAF1</i>) isoforms differ as the result of the selective inclusion of either one of the two mutually exclusive exons (named 5′- and 3′-exon). Only the 5′-exon of the mutually exclusive pair that is included in isoform 1 contains motif <b>A</b>. Both the 5′- and 3′-exons of the mutually exclusive pair have residues at their 3′-boundary that can form interaction motifs (<b>BD</b> or <b>CD</b>) together with the first residues of the downstream constitutively spliced exon. Introns are indicated by horizontal lines.</p>", "links"=>[], "tags"=>["motif", "affecting", "flowering1"], "article_id"=>359285, "categories"=>["Biochemistry", "Biological Sciences", "Physics", "Biophysics", "Plant Biology"], "users"=>["Edouard I. Severing", "Aalt D. J. van Dijk", "Giuseppa Morabito", "Jacqueline Busscher-Lange", "Richard G. H. Immink", "Roeland C. H. J. van Ham"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0030524.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Interaction_motif_architecture_of_MADS_AFFECTING_FLOWERING1_MAF1_isoforms_/359285", "title"=>"Interaction motif architecture of <i>MADS AFFECTING FLOWERING1 (MAF1)</i> isoforms.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-01-25 02:34:45"}
• {"files"=>["https://ndownloader.figshare.com/files/688847"], "description"=>"<p>The type of event and effect on the protein domain architecture is provided for each AS event that results in a translatable mRNA. For each event the TAIR 10 identifiers of the corresponding variants are given when possible. The EST-based annotation corresponds to variants that were not present in the TAIR 10 annotation.</p>", "links"=>[], "tags"=>["spliced", "loci", "producing"], "article_id"=>359337, "categories"=>["Biochemistry", "Biological Sciences", "Physics", "Biophysics", "Plant Biology"], "users"=>["Edouard I. Severing", "Aalt D. J. van Dijk", "Giuseppa Morabito", "Jacqueline Busscher-Lange", "Richard G. H. Immink", "Roeland C. H. J. van Ham"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0030524.t001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Alternative_spliced_loci_producing_multiple_protein_isoforms_/359337", "title"=>"Alternative spliced loci producing multiple protein isoforms.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-01-25 02:35:37"}
• {"files"=>["https://ndownloader.figshare.com/files/688880"], "description"=>"a<p>The difference in cycle threshold (CT) value between the gene- or isoform-specific reaction and the non-template control reaction with the same oligonucleotides is given. Most of the “non-template” control reactions did not give any amplification after 40 cycles and in these cases a CT of 40 was taken for the calculation. Hence, the higher the number, the higher the expression level.</p>b<p>No oligonucleotides could be designed that are specific for the <i>SVP1</i> splicing variant only. The indicated primers detect both <i>SVP1</i> and <i>SVP3.</i></p><p>The tissue for which the expression analysis was performed is indicated. The selection of tissue is based on a relative high expression of the fully spliced transcripts in the respective tissues. Isoform specific oligonucleotide sets were used (see <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0030524#pone.0030524.s011\" target=\"_blank\">Table S3</a>).</p>", "links"=>[], "tags"=>["plant biology", "Computational biology", "biophysics", "physics", "Biochemistry"], "article_id"=>359363, "categories"=>["Biochemistry", "Biological Sciences", "Physics", "Biophysics", "Plant Biology"], "users"=>["Edouard I. Severing", "Aalt D. J. van Dijk", "Giuseppa Morabito", "Jacqueline Busscher-Lange", "Richard G. H. Immink", "Roeland C. H. J. van Ham"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0030524.t002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Additional_expression_evidence_for_the_predicted_functional_AS_event_/359363", "title"=>"Additional expression evidence for the predicted functional AS event.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-01-25 02:36:03"}
• {"files"=>["https://ndownloader.figshare.com/files/688908"], "description"=>"<p>The total numbers of reads supporting each of the alternatives are given for the translatome data as determined using MISO. “X” is used to denote that an AS event could not be confirmed in this analysis.</p>", "links"=>[], "tags"=>["translatome"], "article_id"=>359400, "categories"=>["Biochemistry", "Biological Sciences", "Physics", "Biophysics", "Plant Biology"], "users"=>["Edouard I. Severing", "Aalt D. J. van Dijk", "Giuseppa Morabito", "Jacqueline Busscher-Lange", "Richard G. H. Immink", "Roeland C. H. J. van Ham"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0030524.t003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Additional_translatome_evidence_for_the_predicted_functional_AS_events_/359400", "title"=>"Additional translatome evidence for the predicted functional AS events.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-01-25 02:36:40"}

PMC Usage Stats | Further Information

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Relative Metric

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F1000Prime