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: Contribution to journalArticle

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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
Genes
Arabidopsis
GC Rich Sequence
Untranslated Regions
RNA Sequence Analysis
Oryza
DNA Transposable Elements
Photosynthesis
Poaceae
Epigenomics
Introns
Gene Expression
Food
Peptides

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: Contribution to journalArticle

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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