Wheat in vivo RNA structure landscape reveals a prevalent role of RNA structure in modulating translational subgenome expression asymmetry

Abstract Background Polyploidy, especially allopolyploidy, which entails merging divergent genomes via hybridization and whole-genome duplication (WGD), is a major route to speciation in plants. The duplication among the parental genomes (subgenomes) often leads to one subgenome becoming dominant ov...

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Autores principales:	Xiaofei Yang, Haopeng Yu, Wenqing Sun, Ling Ding, Ji Li, Jitender Cheema, Ricardo Ramirez-Gonzalez, Xuebo Zhao, Azahara C. Martín, Fei Lu, Bao Liu, Cristobal Uauy, Yiliang Ding, Huakun Zhang
Formato:	article
Lenguaje:	EN
Publicado:	BMC 2021
Materias:	Polyploidy Wheat Translational regulation Homoeologous asymmetry RNA structure riboSNitches Biology (General) QH301-705.5 Genetics QH426-470
Acceso en línea:	https://doaj.org/article/0a63eaf5cdfc48b6b35fa36cf78aad94
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spelling	oai:doaj.org-article:0a63eaf5cdfc48b6b35fa36cf78aad942021-12-05T12:25:32ZWheat in vivo RNA structure landscape reveals a prevalent role of RNA structure in modulating translational subgenome expression asymmetry10.1186/s13059-021-02549-y1474-760Xhttps://doaj.org/article/0a63eaf5cdfc48b6b35fa36cf78aad942021-11-01T00:00:00Zhttps://doi.org/10.1186/s13059-021-02549-yhttps://doaj.org/toc/1474-760XAbstract Background Polyploidy, especially allopolyploidy, which entails merging divergent genomes via hybridization and whole-genome duplication (WGD), is a major route to speciation in plants. The duplication among the parental genomes (subgenomes) often leads to one subgenome becoming dominant over the other(s), resulting in subgenome asymmetry in gene content and expression. Polyploid wheats are allopolyploids with most genes present in two (tetraploid) or three (hexaploid) functional copies, which commonly show subgenome expression asymmetry. It is unknown whether a similar subgenome asymmetry exists during translation. We aim to address this key biological question and explore the major contributing factors to subgenome translation asymmetry. Results Here, we obtain the first tetraploid wheat translatome and reveal that subgenome expression asymmetry exists at the translational level. We further perform in vivo RNA structure profiling to obtain the wheat RNA structure landscape and find that mRNA structure has a strong impact on translation, independent of GC content. We discover a previously uncharacterized contribution of RNA structure in subgenome translation asymmetry. We identify 3564 single-nucleotide variations (SNVs) across the transcriptomes between the two tetraploid wheat subgenomes, which induce large RNA structure disparities. These SNVs are highly conserved within durum wheat cultivars but are divergent in both domesticated and wild emmer wheat. Conclusions We successfully determine both the translatome and in vivo RNA structurome in tetraploid wheat. We reveal that RNA structure serves as an important modulator of translational subgenome expression asymmetry in polyploids. Our work provides a new perspective for molecular breeding of major polyploid crops.Xiaofei YangHaopeng YuWenqing SunLing DingJi LiJitender CheemaRicardo Ramirez-GonzalezXuebo ZhaoAzahara C. MartínFei LuBao LiuCristobal UauyYiliang DingHuakun ZhangBMCarticlePolyploidyWheatTranslational regulationHomoeologous asymmetryRNA structureriboSNitchesBiology (General)QH301-705.5GeneticsQH426-470ENGenome Biology, Vol 22, Iss 1, Pp 1-26 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Polyploidy Wheat Translational regulation Homoeologous asymmetry RNA structure riboSNitches Biology (General) QH301-705.5 Genetics QH426-470
spellingShingle	Polyploidy Wheat Translational regulation Homoeologous asymmetry RNA structure riboSNitches Biology (General) QH301-705.5 Genetics QH426-470 Xiaofei Yang Haopeng Yu Wenqing Sun Ling Ding Ji Li Jitender Cheema Ricardo Ramirez-Gonzalez Xuebo Zhao Azahara C. Martín Fei Lu Bao Liu Cristobal Uauy Yiliang Ding Huakun Zhang Wheat in vivo RNA structure landscape reveals a prevalent role of RNA structure in modulating translational subgenome expression asymmetry
description	Abstract Background Polyploidy, especially allopolyploidy, which entails merging divergent genomes via hybridization and whole-genome duplication (WGD), is a major route to speciation in plants. The duplication among the parental genomes (subgenomes) often leads to one subgenome becoming dominant over the other(s), resulting in subgenome asymmetry in gene content and expression. Polyploid wheats are allopolyploids with most genes present in two (tetraploid) or three (hexaploid) functional copies, which commonly show subgenome expression asymmetry. It is unknown whether a similar subgenome asymmetry exists during translation. We aim to address this key biological question and explore the major contributing factors to subgenome translation asymmetry. Results Here, we obtain the first tetraploid wheat translatome and reveal that subgenome expression asymmetry exists at the translational level. We further perform in vivo RNA structure profiling to obtain the wheat RNA structure landscape and find that mRNA structure has a strong impact on translation, independent of GC content. We discover a previously uncharacterized contribution of RNA structure in subgenome translation asymmetry. We identify 3564 single-nucleotide variations (SNVs) across the transcriptomes between the two tetraploid wheat subgenomes, which induce large RNA structure disparities. These SNVs are highly conserved within durum wheat cultivars but are divergent in both domesticated and wild emmer wheat. Conclusions We successfully determine both the translatome and in vivo RNA structurome in tetraploid wheat. We reveal that RNA structure serves as an important modulator of translational subgenome expression asymmetry in polyploids. Our work provides a new perspective for molecular breeding of major polyploid crops.
format	article
author	Xiaofei Yang Haopeng Yu Wenqing Sun Ling Ding Ji Li Jitender Cheema Ricardo Ramirez-Gonzalez Xuebo Zhao Azahara C. Martín Fei Lu Bao Liu Cristobal Uauy Yiliang Ding Huakun Zhang
author_facet	Xiaofei Yang Haopeng Yu Wenqing Sun Ling Ding Ji Li Jitender Cheema Ricardo Ramirez-Gonzalez Xuebo Zhao Azahara C. Martín Fei Lu Bao Liu Cristobal Uauy Yiliang Ding Huakun Zhang
author_sort	Xiaofei Yang
title	Wheat in vivo RNA structure landscape reveals a prevalent role of RNA structure in modulating translational subgenome expression asymmetry
title_short	Wheat in vivo RNA structure landscape reveals a prevalent role of RNA structure in modulating translational subgenome expression asymmetry
title_full	Wheat in vivo RNA structure landscape reveals a prevalent role of RNA structure in modulating translational subgenome expression asymmetry
title_fullStr	Wheat in vivo RNA structure landscape reveals a prevalent role of RNA structure in modulating translational subgenome expression asymmetry
title_full_unstemmed	Wheat in vivo RNA structure landscape reveals a prevalent role of RNA structure in modulating translational subgenome expression asymmetry
title_sort	wheat in vivo rna structure landscape reveals a prevalent role of rna structure in modulating translational subgenome expression asymmetry
publisher	BMC
publishDate	2021
url	https://doaj.org/article/0a63eaf5cdfc48b6b35fa36cf78aad94
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Wheat in vivo RNA structure landscape reveals a prevalent role of RNA structure in modulating translational subgenome expression asymmetry

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