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Analysis of Ribosome-Associated mRNAs in Rice Reveals the Importance of Transcript Size and GC Content in Translation.

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 5' 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.

SUBMITTER: Zhao D

PROVIDER: S-EPMC5217110 | biostudies-literature | 2017 Jan

REPOSITORIES: biostudies-literature

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Analysis of Ribosome-Associated mRNAs in Rice Reveals the Importance of Transcript Size and GC Content in Translation.

Zhao Dongyan D Hamilton John P JP Hardigan Michael M Yin Dongmei D He Tao T Vaillancourt Brieanne B Reynoso Mauricio M Pauluzzi Germain G Funkhouser Scott S Cui Yuehua Y Bailey-Serres Julia J Jiang Jiming J Buell C Robin CR Jiang Ning N

G3 (Bethesda, Md.) 20170105 1

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 (Ory ...[more]

PMID: 27852012

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Project description:BACKGROUND AND AIMS: Plant evolution is well known to be frequently associated with remarkable changes in genome size and composition; however, the knowledge of long-term evolutionary dynamics of these processes still remains very limited. Here a study is made of the fine dynamics of quantitative genome evolution in Festuca (fescue), the largest genus in Poaceae (grasses). METHODS: Using flow cytometry (PI, DAPI), measurements were made of DNA content (2C-value), monoploid genome size (Cx-value), average chromosome size (C/n-value) and cytosine + guanine (GC) content of 101 Festuca taxa and 14 of their close relatives. The results were compared with the existing phylogeny based on ITS and trnL-F sequences. KEY RESULTS: The divergence of the fescue lineage from related Poeae was predated by about a 2-fold monoploid genome and chromosome size enlargement, and apparent GC content enrichment. The backward reduction of these parameters, running parallel in both main evolutionary lineages of fine-leaved and broad-leaved fescues, appears to diverge among the existing species groups. The most dramatic reductions are associated with the most recently and rapidly evolving groups which, in combination with recent intraspecific genome size variability, indicate that the reduction process is probably ongoing and evolutionarily young. This dynamics may be a consequence of GC-rich retrotransposon proliferation and removal. Polyploids derived from parents with a large genome size and high GC content (mostly allopolyploids) had smaller Cx- and C/n-values and only slightly deviated from parental GC content, whereas polyploids derived from parents with small genome and low GC content (mostly autopolyploids) generally had a markedly increased GC content and slightly higher Cx- and C/n-values. CONCLUSIONS: The present study indicates the high potential of general quantitative characters of the genome for understanding the long-term processes of genome evolution, testing evolutionary hypotheses and their usefulness for large-scale genomic projects. Taken together, the results suggest that there is an evolutionary advantage for small genomes in Festuca.

Project description:Many mutations in genes for ribosomal proteins (r-proteins) and assembly factors cause cell stress and altered cell fate, resulting in congenital diseases collectively called ribosomopathies. Even though all such mutations depress the cell's protein synthesis capacity, they generate many different phenotypes, suggesting that the diseases are not due simply to insufficient protein synthesis capacity. To learn more, we investigated how the global transcriptome in Saccharomyces cerevisiae responds to reduced protein synthesis generated in two different ways: abolishing the assembly of new ribosomes and inhibiting ribosomal function. Our results showed that the mechanism by which protein synthesis is obstructed affects the ribosomal protein transcriptome differentially: ribosomal protein mRNA abundance increases during the abolition of ribosome formation but decreases during the inhibition of ribosome function. Interestingly, the ratio between mRNAs from some, but not all, pairs of paralogous ribosomal protein genes encoding slightly different versions of a given r-protein changed differently during the two types of stress, suggesting that expression of specific ribosomal protein paralogous mRNAs may contribute to the stress response. Unexpectedly, the abundance of transcripts for ribosome assembly factors and translation factors remained relatively unaffected by the stresses. On the other hand, the state of the translation apparatus did affect cell physiology: mRNA levels for some other proteins not directly related to the translation apparatus also changed differentially, though not coordinately with the r-protein genes, in response to the stresses. IMPORTANCE Mutations in genes for ribosomal proteins or assembly factors cause a variety of diseases called ribosomopathies. These diseases are typically ascribed to a reduction in the cell's capacity for protein synthesis. Paradoxically, ribosomal mutations result in a wide variety of disease phenotypes, even though they all reduce protein synthesis. Here, we show that the transcriptome changes differently depending on how the protein synthesis capacity is reduced. Most strikingly, inhibiting ribosome formation and ribosome function had opposite effects on the abundance of mRNA for ribosomal proteins, while genes for ribosome translation and assembly factors showed no systematic responses. Thus, the process by which the protein synthesis capacity is reduced contributes decisively to global mRNA composition. This emphasis on process is a new concept in understanding ribosomopathies and other stress responses.

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Analysis of Ribosome-Associated mRNAs in Rice Reveals the Importance of Transcript Size and GC Content in Translation.

Publications

Analysis of Ribosome-Associated mRNAs in Rice Reveals the Importance of Transcript Size and GC Content in Translation.

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