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      Genome-wide identification and expression analyses of Sm genes reveal their involvement in early somatic embryogenesis in Dimocarpus longan Lour

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          Abstract

          The Sm proteins are a conserved protein family with Sm motifs. The family includes Sm and Sm-like proteins, which play important roles in pre-mRNA splicing. Most research on the Sm proteins have been conducted in herbaceous plants, and less in woody plants such as Dimocarpus longan (longan). And the embryo development status significantly affects the quality and yield of longan. In this study, we conducted a genome-wide analysis of longan Sm genes ( DlSm) to clarify their roles during somatic embryogenesis (SE) and identified 29 Sm genes. Phylogenetic analysis deduced longan Sm proteins clustered into 17 phylogenetic groups with the homologous Sm proteins of Arabidopsis thaliana. We also analyzed the gene structures, motif compositions, and conserved domains of the longan Sm proteins. The promoter sequences of the DlSm genes contained many light, endosperm development, hormone, and temperature response elements, which suggested their possible functions. In the non-embryogenic callus(NEC) and during early SE in longan, the alternative splicing(AS) events of DlSm genes indicated that these genes may influence SE development by changing gene structures and sequences. The kinetin(KT) hormone, and blue and white light treatments affected the differentiation and growth of longan embryonic callus(EC) probably by affecting the AS events of DlSm genes. Expression profiles showed the possible functional divergence among Sm genes, and different hormones and light qualities affected their expression levels. The expression trends of the DlSm genes determined by RNA sequencing as fragments per kilobase of exon model per million mapped reads (FPKM) and by real-time quantitative PCR(qRT-PCR) during early SE in longan showed that the expression of the DlSm genes was affected by the growth and differentiation of longan SE, and decreased as the somatic embryo differentiation progressed. The results will contributed to understanding the longan Sm gene family and provide a basis for future functional validation studies.

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          Most cited references52

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          The evolution of spliceosomal introns: patterns, puzzles and progress.

          The origins and importance of spliceosomal introns comprise one of the longest-abiding mysteries of molecular evolution. Considerable debate remains over several aspects of the evolution of spliceosomal introns, including the timing of intron origin and proliferation, the mechanisms by which introns are lost and gained, and the forces that have shaped intron evolution. Recent important progress has been made in each of these areas. Patterns of intron-position correspondence between widely diverged eukaryotic species have provided insights into the origins of the vast differences in intron number between eukaryotic species, and studies of specific cases of intron loss and gain have led to progress in understanding the underlying molecular mechanisms and the forces that control intron evolution.
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            Spliceosomal UsnRNP biogenesis, structure and function.

            Significant advances have been made in elucidating the biogenesis pathway and three-dimensional structure of the UsnRNPs, the building blocks of the spliceosome. U2 and U4/U6*U5 tri-snRNPs functionally associate with the pre-mRNA at an earlier stage of spliceosome assembly than previously thought, and additional evidence supporting UsnRNA-mediated catalysis of pre-mRNA splicing has been presented.
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              A self-regulatory circuit of CIRCADIAN CLOCK-ASSOCIATED1 underlies the circadian clock regulation of temperature responses in Arabidopsis.

              The circadian clock synchronizes biological processes to daily cycles of light and temperature. Clock components, including CIRCADIAN CLOCK-ASSOCIATED1 (CCA1), are also associated with cold acclimation. However, it is unknown how CCA1 activity is modulated in coordinating circadian rhythms and cold acclimation. Here, we report that self-regulation of Arabidopsis thaliana CCA1 activity by a splice variant, CCA1β, links the clock to cold acclimation. CCA1β interferes with the formation of CCA1α-CCA1α and LATE ELONGATED HYPOCOTYL (LHY)-LHY homodimers, as well as CCA1α-LHY heterodimers, by forming nonfunctional heterodimers with reduced DNA binding affinity. Accordingly, the periods of circadian rhythms were shortened in CCA1β-overexpressing transgenic plants (35S:CCA1β), as observed in the cca1 lhy double mutant. In addition, the elongated hypocotyl and leaf petiole phenotypes of CCA1α-overexpressing transgenic plants (35S:CCA1α) were repressed by CCA1β coexpression. Notably, low temperatures suppressed CCA1 alternative splicing and thus reduced CCA1β production. Consequently, whereas the 35S:CCA1α transgenic plants exhibited enhanced freezing tolerance, the 35S:CCA1β transgenic plants were sensitive to freezing, indicating that cold regulation of CCA1 alternative splicing contributes to freezing tolerance. On the basis of these findings, we propose that dynamic self-regulation of CCA1 underlies the clock regulation of temperature responses in Arabidopsis.
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                Author and article information

                Contributors
                Role: Data curationRole: Formal analysisRole: SoftwareRole: Writing – original draft
                Role: Data curationRole: Formal analysis
                Role: Software
                Role: Software
                Role: Software
                Role: Software
                Role: ConceptualizationRole: Funding acquisitionRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: SupervisionRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                3 April 2020
                2020
                : 15
                : 4
                : e0230795
                Affiliations
                [1 ] College of Horticulture, Fujian Agriculture and Forestry University, Fuzhou, Fujian, China
                [2 ] Institute of Horticultural Biotechnology, Fujian Agriculture and Forestry University, Fuzhou, Fujian, China
                Wuhan University, CHINA
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0002-2911-9780
                Article
                PONE-D-20-00319
                10.1371/journal.pone.0230795
                7122786
                32243451
                1bd72bc5-fccb-4923-b34e-b916b40a713d
                © 2020 Li 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.

                History
                : 5 January 2020
                : 8 March 2020
                Page count
                Figures: 12, Tables: 1, Pages: 25
                Funding
                Funded by: National Natural Science Foundation of China
                Award ID: 31672127
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100005270, Fujian Provincial Department of Science and Technology;
                Award ID: 102/712201801101
                Award Recipient :
                Funded by: Technology Innovation Fund of Fujian agriculture and forestry university
                Award ID: CXZX2017187 and CXZX2018078
                Award Recipient :
                The fees for high-throughput sequencing and data processing were supported by the National Natural Science Foundation of China (31672127), the fees for quantitative real time polymerase chain reaction detection were supported by the Constructions of Plateau Discipline of Fujian Province (102/712201801101), the publication fees were supported by the Technology Innovation Fund of Fujian agriculture and forestry university (CXZX2017187 and CXZX2018078). 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
                Proteins
                Protein Domains
                Research and Analysis Methods
                Animal Studies
                Experimental Organism Systems
                Model Organisms
                Arabidopsis Thaliana
                Research and Analysis Methods
                Model Organisms
                Arabidopsis Thaliana
                Biology and Life Sciences
                Organisms
                Eukaryota
                Plants
                Brassica
                Arabidopsis Thaliana
                Research and Analysis Methods
                Animal Studies
                Experimental Organism Systems
                Plant and Algal Models
                Arabidopsis Thaliana
                Research and Analysis Methods
                Database and Informatics Methods
                Bioinformatics
                Sequence Analysis
                Sequence Motif Analysis
                Physical Sciences
                Physics
                Electromagnetic Radiation
                Light
                Visible Light
                White Light
                Research and Analysis Methods
                Database and Informatics Methods
                Bioinformatics
                Sequence Analysis
                Amino Acid Sequence 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
                Custom metadata
                The genome database of Dimocarpus longan has been upload at NCBI (accession number: BioProject PRJNA305337). The transcriptome datasets of four developmental stages (EC, ICpEC, GE and NEC) have been upload to NCBI (SRA accession: PRJNA565345). The transcriptome datasets of nine organs of 'Sijimi' was deposited at NCBI under GSE84467. Other unpublished datasets presented in this study are provided either in the manuscript or supporting information.

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