Analysis of ribosome-associated mRNAs in rice reveals the importance of transcript size and GC content in translation

Dongyan Zhao, John P. Hamilton, Michael Hardigan, Dongmei Yin, Tao He, Brieanne Vaillancourt, Mauricio Reynoso, Germain Pauluzzi, Scott Funkhouser, Yuehua Cui, Julia Bailey-Serres, Jiming Jiang, C. Robin Buell, Ning Jiang

    Research output: Research - peer-reviewArticle

    • 3 Citations

    Abstract

    Gene expression is controlled at transcriptional and post-transcriptional levels including decoding of messenger RNA (mRNA) into polypeptides via ribosome-mediated translation. Translational regulation has been intensively studied in the model dicot plant Arabidopsis thaliana, and in this study, we assessed the translational status [proportion of steady-state mRNA associated with ribosomes] of mRNAs by Translating Ribosome Affinity Purification followed by mRNA-sequencing (TRAP-seq) in rice (Oryza sativa), a model monocot plant and the most important food crop. A survey of three tissues found that most transcribed rice genes are translated whereas few transposable elements are associated with ribosomes. Genes with short and GC-rich coding regions are overrepresented in ribosome-associated mRNAs, suggesting that the GC-richness characteristic of coding sequences in grasses may be an adaptation that favors efficient translation. Transcripts with retained introns and extended 59 untranslated regions are underrepresented on ribosomes, and rice genes belonging to different evolutionary lineages exhibited differential enrichment on the ribosomes that was associated with GC content. Genes involved in photosynthesis and stress responses are preferentially associated with ribosomes, whereas genes in epigenetic regulation pathways are the least enriched on ribosomes. Such variation is more dramatic in rice than that in Arabidopsis and is correlated with the wide variation of GC content of transcripts in rice. Taken together, variation in the translation status of individual transcripts reflects important mechanisms of gene regulation, which may have a role in evolution and diversification.

    LanguageEnglish (US)
    Pages203-219
    Number of pages17
    JournalG3: Genes, Genomes, Genetics
    Volume7
    Issue number1
    DOIs
    StatePublished - 2017

    Profile

    Base Composition
    Ribosomes
    Messenger RNA
    Oryza
    Genes
    Arabidopsis
    GC Rich Sequence
    Untranslated Regions
    RNA Sequence Analysis
    DNA Transposable Elements
    Photosynthesis
    Poaceae
    Epigenomics
    Introns
    Gene Expression
    Food
    Peptides
    Surveys and Questionnaires

    Keywords

    • GC content
    • mRNA length
    • Oryza sativa
    • Purification sequencing
    • Translating ribosome affinity

    ASJC Scopus subject areas

    • Molecular Biology
    • Genetics
    • Genetics(clinical)

    Cite this

    Analysis of ribosome-associated mRNAs in rice reveals the importance of transcript size and GC content in translation. / Zhao, Dongyan; Hamilton, John P.; Hardigan, Michael; Yin, Dongmei; He, Tao; Vaillancourt, Brieanne; Reynoso, Mauricio; Pauluzzi, Germain; Funkhouser, Scott; Cui, Yuehua; Bailey-Serres, Julia; Jiang, Jiming; Buell, C. Robin; Jiang, Ning.

    In: G3: Genes, Genomes, Genetics, Vol. 7, No. 1, 2017, p. 203-219.

    Research output: Research - peer-reviewArticle

    Zhao, D, Hamilton, JP, Hardigan, M, Yin, D, He, T, Vaillancourt, B, Reynoso, M, Pauluzzi, G, Funkhouser, S, Cui, Y, Bailey-Serres, J, Jiang, J, Buell, CR & Jiang, N 2017, 'Analysis of ribosome-associated mRNAs in rice reveals the importance of transcript size and GC content in translation' G3: Genes, Genomes, Genetics, vol 7, no. 1, pp. 203-219. DOI: 10.1534/g3.116.036020
    Zhao D, Hamilton JP, Hardigan M, Yin D, He T, Vaillancourt B et al. Analysis of ribosome-associated mRNAs in rice reveals the importance of transcript size and GC content in translation. G3: Genes, Genomes, Genetics. 2017;7(1):203-219. Available from, DOI: 10.1534/g3.116.036020
    Zhao, Dongyan ; Hamilton, John P. ; Hardigan, Michael ; Yin, Dongmei ; He, Tao ; Vaillancourt, Brieanne ; Reynoso, Mauricio ; Pauluzzi, Germain ; Funkhouser, Scott ; Cui, Yuehua ; Bailey-Serres, Julia ; Jiang, Jiming ; Buell, C. Robin ; Jiang, Ning. / Analysis of ribosome-associated mRNAs in rice reveals the importance of transcript size and GC content in translation. In: G3: Genes, Genomes, Genetics. 2017 ; Vol. 7, No. 1. pp. 203-219
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