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Depletion of Arabidopsis SC35 and SC35-like serine/arginine-rich proteins affects the transcription and splicing of a subset of genes

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PLoS Genetics

Public Library of Science

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      Abstract

      Serine/arginine-rich (SR) proteins are important splicing factors which play significant roles in spliceosome assembly and splicing regulation. However, little is known regarding their biological functions in plants. Here, we analyzed the phenotypes of mutants upon depleting different subfamilies of Arabidopsis SR proteins. We found that loss of the functions of SC35 and SC35-like (SCL) proteins cause pleiotropic changes in plant morphology and development, including serrated leaves, late flowering, shorter roots and abnormal silique phyllotaxy. Using RNA-seq, we found that SC35 and SCL proteins play roles in the pre-mRNA splicing. Motif analysis revealed that SC35 and SCL proteins preferentially bind to a specific RNA sequence containing the AGAAGA motif. In addition, the transcriptions of a subset of genes are affected by the deletion of SC35 and SCL proteins which interact with NRPB4, a specific subunit of RNA polymerase II. The splicing of FLOWERING LOCUS C ( FLC) intron1 and transcription of FLC were significantly regulated by SC35 and SCL proteins to control Arabidopsis flowering. Therefore, our findings provide mechanistic insight into the functions of plant SC35 and SCL proteins in the regulation of splicing and transcription in a direct or indirect manner to maintain the proper expression of genes and development.

      Author summary

      SR proteins were identified to be important splicing factors. This work generated mutants of different subfamilies of the classic Arabidopsis SR proteins. Genetic analysis revealed that loss of the function of SC35/SCL proteins influences the plant development. This study revealed SC35/SCL proteins regulate alternative splicing, preferentially bind a specific RNA motif, interact with NRPB4, and affect the transcription of a subset of genes. This study further revealed that SC35/SCL proteins control flowering by regulating the splicing and transcription of FLC. These results shed light on the functions of SR proteins in plants.

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      Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.

      The Agrobacterium vacuum infiltration method has made it possible to transform Arabidopsis thaliana without plant tissue culture or regeneration. In the present study, this method was evaluated and a substantially modified transformation method was developed. The labor-intensive vacuum infiltration process was eliminated in favor of simple dipping of developing floral tissues into a solution containing Agrobacterium tumefaciens, 5% sucrose and 500 microliters per litre of surfactant Silwet L-77. Sucrose and surfactant were critical to the success of the floral dip method. Plants inoculated when numerous immature floral buds and few siliques were present produced transformed progeny at the highest rate. Plant tissue culture media, the hormone benzylamino purine and pH adjustment were unnecessary, and Agrobacterium could be applied to plants at a range of cell densities. Repeated application of Agrobacterium improved transformation rates and overall yield of transformants approximately twofold. Covering plants for 1 day to retain humidity after inoculation also raised transformation rates twofold. Multiple ecotypes were transformable by this method. The modified method should facilitate high-throughput transformation of Arabidopsis for efforts such as T-DNA gene tagging, positional cloning, or attempts at targeted gene replacement.
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        Alternative Isoform Regulation in Human Tissue Transcriptomes

        Through alternative processing of pre-mRNAs, individual mammalian genes often produce multiple mRNA and protein isoforms that may have related, distinct or even opposing functions. Here we report an in-depth analysis of 15 diverse human tissue and cell line transcriptomes based on deep sequencing of cDNA fragments, yielding a digital inventory of gene and mRNA isoform expression. Analysis of mappings of sequence reads to exon-exon junctions indicated that 92-94% of human genes undergo alternative splicing (AS), ∼86% with a minor isoform frequency of 15% or more. Differences in isoform-specific read densities indicated that a majority of AS and of alternative cleavage and polyadenylation (APA) events vary between tissues, while variation between individuals was ∼2- to 3-fold less common. Extreme or ‘switch-like’ regulation of splicing between tissues was associated with increased sequence conservation in regulatory regions and with generation of full-length open reading frames. Patterns of AS and APA were strongly correlated across tissues, suggesting coordinated regulation of these processes, and sequence conservation of a subset of known regulatory motifs in both alternative introns and 3′ UTRs suggested common involvement of specific factors in tissue-level regulation of both splicing and polyadenylation.
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          The KEGG resource for deciphering the genome.

          A grand challenge in the post-genomic era is a complete computer representation of the cell and the organism, which will enable computational prediction of higher-level complexity of cellular processes and organism behavior from genomic information. Toward this end we have been developing a knowledge-based approach for network prediction, which is to predict, given a complete set of genes in the genome, the protein interaction networks that are responsible for various cellular processes. KEGG at http://www.genome.ad.jp/kegg/ is the reference knowledge base that integrates current knowledge on molecular interaction networks such as pathways and complexes (PATHWAY database), information about genes and proteins generated by genome projects (GENES/SSDB/KO databases) and information about biochemical compounds and reactions (COMPOUND/GLYCAN/REACTION databases). These three types of database actually represent three graph objects, called the protein network, the gene universe and the chemical universe. New efforts are being made to abstract knowledge, both computationally and manually, about ortholog clusters in the KO (KEGG Orthology) database, and to collect and analyze carbohydrate structures in the GLYCAN database.
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            Author and article information

            Affiliations
            National key Laboratory of Plant Molecular Genetics, Chinese Academy of Sciences Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences; University of Chinese Academy of Sciences, Shanghai, China
            Peking University, CHINA
            Author notes

            The authors have declared that no competing interests exist.

            • Conceptualization: QY YF.

            • Data curation: QY.

            • Formal analysis: QY.

            • Funding acquisition: YF ZS.

            • Investigation: QY.

            • Methodology: QY XX ZS.

            • Project administration: XX YF.

            • Supervision: YF.

            • Validation: QY ZS.

            • Visualization: QY YF.

            • Writing – original draft: QY YF.

            • Writing – review & editing: QY ZS YF.

            Contributors
            Role: Editor
            Journal
            PLoS Genet
            PLoS Genet
            plos
            plosgen
            PLoS Genetics
            Public Library of Science (San Francisco, CA USA )
            1553-7390
            1553-7404
            8 March 2017
            March 2017
            : 13
            : 3
            28273088
            5362245
            10.1371/journal.pgen.1006663
            PGENETICS-D-16-02312
            (Editor)
            © 2017 Yan et al

            This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

            Counts
            Figures: 10, Tables: 0, Pages: 29
            Product
            Funding
            Funded by: funder-id http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;
            Award ID: 91319304
            Award Recipient : ORCID: http://orcid.org/0000-0002-7391-0246
            Funded by: National Natural Science Foundation of China
            Award ID: 31401041
            Award Recipient :
            This work was supported by the grants from National Natural Science Foundation of China ( http://www.nsfc.gov.cn/) (grant 91319304 to YF and 31401041 to ZS) The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
            Categories
            Research Article
            Biology and Life Sciences
            Biochemistry
            Plant Biochemistry
            Biology and Life Sciences
            Plant Science
            Plant Biochemistry
            Research and Analysis Methods
            Database and Informatics Methods
            Bioinformatics
            Sequence Analysis
            Sequence Motif Analysis
            Biology and Life Sciences
            Genetics
            Gene Expression
            Biology and Life Sciences
            Computational Biology
            Genome Complexity
            Introns
            Biology and Life Sciences
            Genetics
            Genomics
            Genome Complexity
            Introns
            Biology and Life Sciences
            Genetics
            Gene Expression
            Gene Regulation
            Biology and Life Sciences
            Molecular Biology
            Molecular Biology Techniques
            Artificial Gene Amplification and Extension
            Polymerase Chain Reaction
            Reverse Transcriptase-Polymerase Chain Reaction
            Research and Analysis Methods
            Molecular Biology Techniques
            Artificial Gene Amplification and Extension
            Polymerase Chain Reaction
            Reverse Transcriptase-Polymerase Chain Reaction
            Research and Analysis Methods
            Experimental Organism Systems
            Model Organisms
            Arabidopsis Thaliana
            Research and Analysis Methods
            Model Organisms
            Arabidopsis Thaliana
            Biology and Life Sciences
            Organisms
            Plants
            Brassica
            Arabidopsis Thaliana
            Research and Analysis Methods
            Experimental Organism Systems
            Plant and Algal Models
            Arabidopsis Thaliana
            Biology and Life Sciences
            Genetics
            Phenotypes
            Custom metadata
            vor-update-to-uncorrected-proof
            2017-03-22
            RNA-seq data associated with this paper are available at http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE93910 under the NCBI GEO identifier: GSE93910

            Genetics

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