Translational gene regulation in plants: A green new deal

Camacho, Ricardo A. Urquidi; Lokdarshi, Ansul; Arnim, Albrecht G. von

doi:10.1002/wrna.1597

Cited by 45 publications

(38 citation statements)

References 360 publications

(677 reference statements)

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“…In 1995, the model plant Arabidopsis thaliana revealed tissue-specific expression of the many RP paralogs that exist in plants ( Williams and Sussex, 1995 ). Nowadays, among many examples, well-studied global translational regulators in plants couple external stimuli to translation, arguing for deeper investigation of translational control ( Urquidi Camacho et al., 2020 ) upon environmental cues.…”

Section: Introductionmentioning

confidence: 99%

Systematic Review of Plant Ribosome Heterogeneity and Specialization

et al. 2020

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Plants dedicate a high amount of energy and resources to the production of ribosomes. Historically, these multi-protein ribosome complexes have been considered static protein synthesis machines that are not subject to extensive regulation but only read mRNA and produce polypeptides accordingly. New and increasing evidence across various model organisms demonstrated the heterogeneous nature of ribosomes. This heterogeneity can constitute specialized ribosomes that regulate mRNA translation and control protein synthesis. A prominent example of ribosome heterogeneity is seen in the model plant, Arabidopsis thaliana , which, due to genome duplications, has multiple paralogs of each ribosomal protein (RP) gene. We support the notion of plant evolution directing high RP paralog divergence toward functional heterogeneity, underpinned in part by a vast resource of ribosome mutants that suggest specialization extends beyond the pleiotropic effects of single structural RPs or RP paralogs. Thus, Arabidopsis is a highly suitable model to study this phenomenon. Arabidopsis enables reverse genetics approaches that could provide evidence of ribosome specialization. In this review, we critically assess evidence of plant ribosome specialization and highlight steps along ribosome biogenesis in which heterogeneity may arise, filling the knowledge gaps in plant science by providing advanced insights from the human or yeast fields. We propose a data analysis pipeline that infers the heterogeneity of ribosome complexes and deviations from canonical structural compositions linked to stress events. This analysis pipeline can be extrapolated and enhanced by combination with other high-throughput methodologies, such as proteomics. Technologies, such as kinetic mass spectrometry and ribosome profiling, will be necessary to resolve the temporal and spatial aspects of translational regulation while the functional features of ribosomal subpopulations will become clear with the combination of reverse genetics and systems biology approaches.

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Section: Introductionmentioning

confidence: 99%

Systematic Review of Plant Ribosome Heterogeneity and Specialization

et al. 2020

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“…These systems identify aberrant transcripts and induce their quick decay. The Nonsense-mediated decay (NMD), the Non-stop decay (NSD) and the No-go decay (NGD) are translation-coupled quality control systems (Karamyshev and Karamysheva 2018 ; Urquidi Camacho et al 2020 ), while RNA silencing quality control system degrades both translated and non-translated transcripts (Lee et al 2020 ). Plant NMD degrades a transcript if its 3′UTR is unusually long or contains an intron more than 50 nt downstream from the stop codon (Arciga-Reyes et al 2006 ; Kertész et al 2006 ; Schwartz et al 2006 ; Gloggnitzer et al 2014 ).…”

Section: Introductionmentioning

confidence: 99%

The role of RST1 and RIPR proteins in plant RNA quality control systems

et al. 2021

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To keep mRNA homeostasis, the RNA degradation, quality control and silencing systems should act in balance in plants. Degradation of normal mRNA starts with deadenylation, then deadenylated transcripts are degraded by the SKI-exosome 3′-5′ and/or XRN4 5′-3′ exonucleases. RNA quality control systems identify and decay different aberrant transcripts. RNA silencing degrades double-stranded transcripts and homologous mRNAs. It also targets aberrant and silencing prone transcripts. The SKI-exosome is essential for mRNA homeostasis, it functions in normal mRNA degradation and different RNA quality control systems, and in its absence silencing targets normal transcripts. It is highly conserved in eukaryotes, thus recent reports that the plant SKI-exosome is associated with RST1 and RIPR proteins and that, they are required for SKI-exosome–mediated decay of silencing prone transcripts were unexpected. To clarify whether RST1 and RIPR are essential for all SKI-exosome functions or only for the elimination of silencing prone transcripts, degradation of different reporter transcripts was studied in RST1 and RIPR inactivated Nicotiana benthamiana plants. As RST1 and RIPR, like the SKI-exosome, were essential for Non-stop and No-go decay quality control systems, and for RNA silencing- and minimum ORF-mediated decay, we propose that RST1 and RIPR are essential components of plant SKI-exosome supercomplex.

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“…Protein synthesis level has long been shown to have poor correlations with mRNA abundance in eukaryotic organisms (Ingolia et al ., 2009; Battle et al ., 2015), which may be ascribed to translational regulation to a large extent (Urquidi Camacho et al ., 2020). In this study, by analysis of the three tissues in two parental varieties and their hybrid, we provide a comprehensive translational regulation profile and allelic TE divergence in rice.…”

Section: Discussionmentioning

confidence: 99%

Ribosome profiling reveals the translational landscape and allele-specific translation efficiency in rice

Zhu

Zhou

Che

et al. 2022

Preprint

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Translational regulation is a critical step in the process of gene expression and governs the synthesis of proteins from mRNAs. Many studies have revealed the translational regulation in plants in response to various environmental stimuli. However, there has been no comprehensive landscape of translational regulation and allele-specific translation efficiency in multiple tissues of plants, especially in rice, a main staple crop feeding nearly half of the world population. Here, we used RNA-seq and Ribo-seq data to analyze the transcriptome and translatome of an elite hybrid rice SY63 and its parental varieties ZS97 and MH63. The results revealed that gene expression patterns varied more significantly between tissues than between varieties at both transcriptional and translational levels. Besides, we identified 3,392 upstream open reading frames (uORFs), and most of the uORF-containing genes were enriched for transcription factors. Only 668 long non-coding RNAs could be translated into peptides. Finally, we discovered numerous genes with allele-specific translation efficiency in SY63, and further demonstrated that some cis-regulatory elements (secondary structures of mRNAs and the binding of miRNAs) may contribute to allelic divergence in translation efficiency. Overall, our findings may improve the understanding of translational regulation in rice and provide information for the molecular basis of breading research.

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Translational gene regulation in plants: A green new deal

Cited by 45 publications

References 360 publications

Systematic Review of Plant Ribosome Heterogeneity and Specialization

Systematic Review of Plant Ribosome Heterogeneity and Specialization

The role of RST1 and RIPR proteins in plant RNA quality control systems

Ribosome profiling reveals the translational landscape and allele-specific translation efficiency in rice

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