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

Zhu, Xitong; Zhou, Run; Che, Jian; Zheng, Yuyu; Qamar, Muhammad Tahir ul; Feng, Jia-Wu; Zhang, Jianwei; Gao, Junxiang

doi:10.1016/j.xplc.2022.100457

Cited by 11 publications

(3 citation statements)

References 94 publications

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“…The characteristic three-nucleotide periodicity of ribosomes during translation facilitates the detection of unannotated translational events. − In addition, computational tools such as RiboTaper, RiboToolkit, and RiboFlow have been developed to identify ORFs based on this 3-nt periodicity. These methodologies have unveiled upstream ORFs (uORFs) in the 5′ untranslated region (5′-UTR) and small ORFs (sORFs) in previously unannotated genomic regions of Arabidopsis (Arabidopsis thaliana), tomato (Solanum lycopersicum), Medicago (Medicago truncatula), and rice (Oryza sativa). ,,− These comprehensive analyses suggest that uORFs can modulate the translation of the downstream main ORFs (mORFs). Moreover, certain noncoding RNAs have been found to produce small peptides comprising fewer than 100 amino acids. , Despite their significant roles, uORF and sORF often remain unacknowledged in genome annotation.…”

Section: Introductionmentioning

confidence: 99%

Translatome and Transcriptome Analyses Reveal the Mechanism that Underlies the Enhancement of Salt Stress by the Small Peptide Ospep5 in Plants

Wang,

Li,

et al. 2024

J. Agric. Food Chem.

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Salt stress significantly impedes plant growth and the crop yield. This study utilized de novo transcriptome assembly and ribosome profiling to explore mRNA translation's role in rice salt tolerance. We identified unrecognized translated open reading frames (ORFs), including 42 upstream transcripts and 86 unannotated transcripts. A noteworthy discovery was the role of a small ORF, Ospep5, in conferring salt tolerance. Overexpression of Ospep5 in plants increased salt tolerance, while its absence led to heightened sensitivity. This hypothesis was corroborated by the findings that exogenous application of the synthetic small peptide Ospep5 bolstered salt tolerance in both rice and Arabidopsis. We found that the mechanism underpinning the Ospep5-mediated salt tolerance involves the maintenance of intracellular Na + /K + homeostasis, facilitated by upregulation of high-affinity potassium transporters (HKT) and Na + /H + exchangers (SOS1). Furthermore, a comprehensive multiomics approach, particularly ribosome profiling, is instrumental in uncovering unannotated ORFs and elucidating their functions in plant stress responses.

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Section: Introductionmentioning

confidence: 99%

Translatome and Transcriptome Analyses Reveal the Mechanism that Underlies the Enhancement of Salt Stress by the Small Peptide Ospep5 in Plants

Wang,

Li,

et al. 2024

J. Agric. Food Chem.

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“…These unannotated translated ORFs include small ORFs (sORFs) encoded by presumed noncoding RNAs (ncRNAs), as well as short uORFs present in the 5′ UTRs of protein-coding RNAs (i.e. mRNAs) ( Liu et al 2013 ; Juntawong et al 2014 ; Lei et al 2015 ; Hsu et al 2016 ; Bazin et al 2017 ; Wu et al 2019 ; Kurihara et al 2020 ; Li and Liu 2020 ; Sotta et al 2022 ; Qanmber et al 2023 ; Zhu et al 2023 ; Guo, Chen, et al 2023 ). Lately, downstream ORFs (dORFs) in the 3′ UTRs of mRNAs were also reported in vertebrates ( Wu et al 2020 ).…”

Section: Introductionmentioning

confidence: 99%

Improved super-resolution ribosome profiling reveals prevalent translation of upstream ORFs and small ORFs in Arabidopsis

Wu,

Ai,

Teixeira

et al. 2023

The Plant Cell

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A crucial step in functional genomics is identifying actively translated ORFs and linking them to biological functions. The challenge lies in identifying short ORFs, as their identification is greatly influenced by data quality and depth. Here, we improved the coverage of super-resolution Ribo-seq in Arabidopsis (Arabidopsis thaliana), revealing uncharacterized translation events for nuclear, chloroplastic, and mitochondrial genes. Assisted by a transcriptome assembly, we identified 7,751 unconventional translation events, comprising 6,996 upstream ORFs (uORFs) and 209 downstream ORFs on annotated protein-coding genes, as well as 546 ORFs in presumed noncoding RNAs. Proteomic data confirmed the production of stable proteins from some of these unannotated translation events. We present evidence of active translation from primary transcripts of trans-acting small interfering RNAs (TAS1–4) and microRNAs (pri-MIR163 and pri-MIR169) and periodic ribosome stalling supporting cotranslational decay. Additionally, we developed a method for identifying extremely short uORFs, including 370 minimum uORFs (AUG-stop), and 2,921 tiny uORFs (2 to 10 amino acids) and 681 uORFs that overlap with each other. Remarkably, these short uORFs exhibit strong translational repression as do longer uORFs. We also systematically discovered 594 uORFs regulated by alternative splicing, suggesting widespread isoform-specific translational control. Finally, these prevalent uORFs are associated with numerous important pathways. In summary, our improved Arabidopsis translational landscape provides valuable resources to study gene expression regulation.

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“…It has become increasingly clear that a substantial fraction of the transcriptomes in diverse plant species has prevalent unannotated translated ORFs. These unannotated translated ORFs include small ORFs (sORFs) encoded by presumed non-coding RNAs, as well as short upstream ORFs (uORFs) present in the 5′ untranslated regions (5′ UTRs) of protein-coding RNAs (i.e., mRNAs) (Liu et al, 2013; Juntawong et al, 2014; Lei et al, 2015; Hsu et al, 2016; Bazin et al, 2017; Wu et al, 2019; Li and Liu, 2020; Kurihara et al, 2020; Sotta et al, 2022; Guo et al, 2023; Qanmber et al, 2023; Zhu et al, 2023). More recently, even downstream ORFs (dORFs) in the 3′ UTRs of mRNAs have been reported in vertebrates (Wu et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

Improved Super-Resolution Ribosome Profiling Revealed Prevalent Translation of Upstream ORFs and Small ORFs in Arabidopsis

Wu,

Ai,

Teixeira

et al. 2023

Preprint

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A crucial step in functional genomics is identifying actively translated open reading frames (ORFs) that link biological functions. The challenge lies in identifying short ORFs, as they are greatly impacted by data quality and depth. Here, we improved the coverage of super-resolution Ribo-seq in Arabidopsis, revealing uncharacterized translation events in nucleus-, chloroplast-, and mitochondria-encoded genes. We identified 7,751 unconventional translation events, including 6,996 upstream ORFs (uORFs) and 209 downstream ORFs on annotated protein-coding genes, as well as 546 ncORFs on presumed non-coding RNAs. Proteomics data confirmed the production of stable proteins from some of the unannotated translation events. We present evidence of active translation on primary transcripts of tasiRNAs (TAS1-4) and microRNAs (pri-miR163, pri-miR169), and periodic ribosome stalling supporting co-translational decay. Additionally, we developed a method for identifying extremely short uORFs, including 370 minimum uORF (AUG-stop), and 2,984 tiny uORFs (2-10 aa), as well as 681 uORFs that overlap with each other. Remarkably, these short uORFs exhibit strong translational repression as longer uORFs. We also systematically discovered 594 uORFs regulated by alternative splicing, suggesting widespread isoform-specific translational control. Finally, these prevalent uORFs are associated with numerous important pathways. In summary, our improved Arabidopsis translational landscape provides valuable resources to study gene expression regulation.

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

Cited by 11 publications

References 94 publications

Translatome and Transcriptome Analyses Reveal the Mechanism that Underlies the Enhancement of Salt Stress by the Small Peptide Ospep5 in Plants

Translatome and Transcriptome Analyses Reveal the Mechanism that Underlies the Enhancement of Salt Stress by the Small Peptide Ospep5 in Plants

Improved super-resolution ribosome profiling reveals prevalent translation of upstream ORFs and small ORFs in Arabidopsis

Improved Super-Resolution Ribosome Profiling Revealed Prevalent Translation of Upstream ORFs and Small ORFs in Arabidopsis

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