2022Plant CommunicationsOpen access

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

Xi-Tong Zhu, Run Zhou, Jian Che, Yuyu Zheng, Muhammad Tahir ul Qamar, Jia‐Wu Feng, Jianwei Zhang, Junxiang Gao, Ling‐Ling Chen

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Abstract

Translational regulation is a critical step in the process of gene expression and governs the synthesis of proteins from mRNAs. Many studies have revealed translational regulation in plants in response to various environmental stimuli. However, there have been no studies documenting the comprehensive landscape of translational regulation and allele-specific translational efficiency in multiple plant tissues, especially those of rice, a main staple crop that feeds nearly half of the world's population. Here we used RNA sequencing and ribosome profiling data to analyze the transcriptome and translatome of an elite hybrid rice, Shanyou 63 (SY63), and its parental varieties Zhenshan 97 and Minghui 63. The results revealed that gene expression patterns varied more among tissues than among varieties at the transcriptional and translational levels. We identified 3392 upstream open reading frames (uORFs), and the uORF-containing genes were enriched in transcription factors. Only 668 of 13 492 long non-coding RNAs could be translated into peptides. Finally, we discovered numerous genes with allele-specific translational efficiency in SY63 and demonstrated that some cis-regulatory elements may contribute to allelic divergence in translational efficiency. Overall, these findings may improve our understanding of translational regulation in rice and provide information for molecular breeding research.

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What this paper is about

Translational regulation is a critical step in the process of gene expression and governs the synthesis of proteins from mRNAs. Many studies have revealed translational regulation in plants in response to various environmental stimuli. However, there have been no studies documenting the comprehensive landscape of translational regulation and allele-specific translational efficiency in multiple plant tissues, especially those of rice, a main staple crop that feeds nearly half of the world's population. Here we used RNA sequencing and ribosome profiling data to analyze the transcriptome and translatome of an elite hybrid rice, Shanyou 63 (SY63), and its parental varieties Zhenshan 97 and Minghui 63. The results revealed that gene expression patterns varied more among tissues than among varieties at the transcriptional and translational levels. We identified 3392 upstream open reading frames (uORFs), and the uORF-containing genes were enriched in transcription factors. Only 668 of 13 492 long non-coding RNAs could be translated into peptides. Finally, we discovered numerous genes with allele-specific translational efficiency in SY63 and demonstrated that some cis-regulatory elements may contribute to allelic divergence in translational efficiency. Overall, these findings may improve our understanding of translational regulation in rice and provide information for molecular breeding research.

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Available abstract

Translational regulation is a critical step in the process of gene expression and governs the synthesis of proteins from mRNAs. Many studies have revealed translational regulation in plants in response to various environmental stimuli. However, there have been no studies documenting the comprehensive landscape of translational regulation and allele-specific translational efficiency in multiple plant tissues, especially those of rice, a main staple crop that feeds nearly half of the world's population. Here we used RNA sequencing and ribosome profiling data to analyze the transcriptome and translatome of an elite hybrid rice, Shanyou 63 (SY63), and its parental varieties Zhenshan 97 and Minghui 63. The results revealed that gene expression patterns varied more among tissues than among varieties at the transcriptional and translational levels. We identified 3392 upstream open reading frames (uORFs), and the uORF-containing genes were enriched in transcription factors. Only 668 of 13 492 long non-coding RNAs could be translated into peptides. Finally, we discovered numerous genes with allele-specific translational efficiency in SY63 and demonstrated that some cis-regulatory elements may contribute to allelic divergence in translational efficiency. Overall, these findings may improve our understanding of translational regulation in rice and provide information for molecular breeding research.

Key concepts: Ribosome profiling, Translational efficiency, Biology, Translational regulation, Gene, Genetics, Transcriptome, Allele

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