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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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          Most cited references 126

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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
                © 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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