RNA G-quadruplex structures exist and function in vivo in plants.

Gene regulation Plant development RNA G-quadruplex structure Selective 2′-hydroxyl acylation with lithium ion-based primer extension (SHALiPE) rG4-seq

Journal

Genome biology
ISSN: 1474-760X
Titre abrégé: Genome Biol
Pays: England
ID NLM: 100960660

Informations de publication

Date de publication:
01 09 2020
Historique:
received: 26 03 2020
accepted: 08 08 2020
entrez: 3 9 2020
pubmed: 3 9 2020
medline: 16 6 2021
Statut: epublish

Résumé

Guanine-rich sequences are able to form complex RNA structures termed RNA G-quadruplexes in vitro. Because of their high stability, RNA G-quadruplexes are proposed to exist in vivo and are suggested to be associated with important biological relevance. However, there is a lack of direct evidence for RNA G-quadruplex formation in living eukaryotic cells. Therefore, it is unclear whether any purported functions are associated with the specific sequence content or the formation of an RNA G-quadruplex structure. Using rG4-seq, we profile the landscape of those guanine-rich regions with the in vitro folding potential in the Arabidopsis transcriptome. We find a global enrichment of RNA G-quadruplexes with two G-quartets whereby the folding potential is strongly influenced by RNA secondary structures. Using in vitro and in vivo RNA chemical structure profiling, we determine that hundreds of RNA G-quadruplex structures are strongly folded in both Arabidopsis and rice, providing direct evidence of RNA G-quadruplex formation in living eukaryotic cells. Subsequent genetic and biochemical analyses show that RNA G-quadruplex folding is able to regulate translation and modulate plant growth. Our study reveals the existence of RNA G-quadruplex in vivo and indicates that RNA G-quadruplex structures act as important regulators of plant development and growth.

Sections du résumé

BACKGROUND
Guanine-rich sequences are able to form complex RNA structures termed RNA G-quadruplexes in vitro. Because of their high stability, RNA G-quadruplexes are proposed to exist in vivo and are suggested to be associated with important biological relevance. However, there is a lack of direct evidence for RNA G-quadruplex formation in living eukaryotic cells. Therefore, it is unclear whether any purported functions are associated with the specific sequence content or the formation of an RNA G-quadruplex structure.
RESULTS
Using rG4-seq, we profile the landscape of those guanine-rich regions with the in vitro folding potential in the Arabidopsis transcriptome. We find a global enrichment of RNA G-quadruplexes with two G-quartets whereby the folding potential is strongly influenced by RNA secondary structures. Using in vitro and in vivo RNA chemical structure profiling, we determine that hundreds of RNA G-quadruplex structures are strongly folded in both Arabidopsis and rice, providing direct evidence of RNA G-quadruplex formation in living eukaryotic cells. Subsequent genetic and biochemical analyses show that RNA G-quadruplex folding is able to regulate translation and modulate plant growth.
CONCLUSIONS
Our study reveals the existence of RNA G-quadruplex in vivo and indicates that RNA G-quadruplex structures act as important regulators of plant development and growth.

Identifiants

pubmed: 32873317
doi: 10.1186/s13059-020-02142-9
pii: 10.1186/s13059-020-02142-9
pmc: PMC7466424
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

226

Subventions

Organisme : Biotechnology and Biological Sciences Research Council
ID : BBS/E/J/000PR9788
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/L025000/1
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/N022572/1
Pays : United Kingdom

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Auteurs

Xiaofei Yang (X)

Department of Cell and Developmental Biology, John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, UK.

Jitender Cheema (J)

Department of Cell and Developmental Biology, John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, UK.

Yueying Zhang (Y)

Department of Cell and Developmental Biology, John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, UK.

Hongjing Deng (H)

Department of Cell and Developmental Biology, John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, UK.
College of Life Sciences, University of Chinese Academy of Sciences, Beijing, 100049, China.
State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Beijing, 100101, China.

Susan Duncan (S)

Department of Cell and Developmental Biology, John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, UK.

Mubarak Ishaq Umar (MI)

Department of Chemistry, City University of Hong Kong, Kowloon Tong, Hong Kong SAR, China.

Jieyu Zhao (J)

Department of Chemistry, City University of Hong Kong, Kowloon Tong, Hong Kong SAR, China.

Qi Liu (Q)

Department of Cell and Developmental Biology, John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, UK.
Present Address: School of Life Sciences, University of Sussex, Brighton, BN1 9QG, UK.

Xiaofeng Cao (X)

College of Life Sciences, University of Chinese Academy of Sciences, Beijing, 100049, China. xfcao@genetics.ac.cn.
State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Beijing, 100101, China. xfcao@genetics.ac.cn.

Chun Kit Kwok (CK)

Department of Chemistry, City University of Hong Kong, Kowloon Tong, Hong Kong SAR, China. ckkwok42@cityu.edu.hk.
Shenzhen Research Institute of City University of Hong Kong, Shenzhen, 518057, China. ckkwok42@cityu.edu.hk.

Yiliang Ding (Y)

Department of Cell and Developmental Biology, John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, UK. yiliang.ding@jic.ac.uk.

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