Non-coding RNA expression analysis revealed the molecular mechanism of flag leaf heterosis in inter-subspecific hybrid rice

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Abstract

Heterosis has been used widespread in agriculture, but its molecular mechanism is inadequately understood. Plants have a large number of non-coding RNAs (ncRNAs), among them, functional ncRNAs that have been studied widely containing long non-coding RNA (lncRNA) and circular RNA (circRNA) that play a role in varied biological processes, as well as microRNA (miRNA), which can not only regulate the post-transcriptional expression of target genes, but also target lncRNA and circRNA then participate the competing endogenous RNA (ceRNA) regulatory network. However, the influence of these three ncRNAs and their regulatory relationships on heterosis is unknown in rice. In this study, the expression profile of ncRNAs and the ncRNA regulatory network related to heterosis were comprehensively analyzed in inter-subspecific hybrid rice. A total of 867 miRNAs, 3,278 lncRNAs and 2,521 circRNAs were identified in the hybrid and its parents. Analysis of the global profiles of these three types of ncRNAs indicated that significant differences existed in the distribution and sequence characteristics of the corresponding genes. The numbers of miRNA and lncRNA in hybrid were higher than those in its parents. A total of 784 ncRNAs (169 miRNAs, 573 lncRNAs and 42 circRNAs) showed differentially expressed in the hybrid, and their target/host genes were vital in stress tolerance, growth and development in rice. These discoveries suggested that the expression plasticity of ncRNA has an important role of inter-subspecific hybrid rice heterosis. It is worth mentioning that miRNAs exhibited substantially more variations between hybrid and parents compared with observed variation for lncRNA and circRNA. Non-additive expression ncRNAs and allele-specific expression genes-related ncRNAs in hybrid were provided in this study, and multiple sets of ncRNA regulatory networks closely related to heterosis were obtained. Meanwhile, heterosis-related regulatory networks of ceRNA (lncRNA and circRNA) and miRNA were also demonstrated.

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Most cited references 55

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Origin, biogenesis, and activity of plant microRNAs.

Olivier Voinnet (2009)

MicroRNAs (miRNAs) are key posttranscriptional regulators of eukaryotic gene expression. Plants use highly conserved as well as more recently evolved, species-specific miRNAs to control a vast array of biological processes. This Review discusses current advances in our understanding of the origin, biogenesis, and mode of action of plant miRNAs and draws comparisons with their metazoan counterparts.

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Expanded identification and characterization of mammalian circular RNAs

Junjie U. Guo, Vikram Agarwal, Huili Guo … (2014)

Background The recent reports of two circular RNAs (circRNAs) with strong potential to act as microRNA (miRNA) sponges suggest that circRNAs might play important roles in regulating gene expression. However, the global properties of circRNAs are not well understood. Results We developed a computational pipeline to identify circRNAs and quantify their relative abundance from RNA-seq data. Applying this pipeline to a large set of non-poly(A)-selected RNA-seq data from the ENCODE project, we annotated 7,112 human circRNAs that were estimated to comprise at least 10% of the transcripts accumulating from their loci. Most circRNAs are expressed in only a few cell types and at low abundance, but they are no more cell-type-specific than are mRNAs with similar overall expression levels. Although most circRNAs overlap protein-coding sequences, ribosome profiling provides no evidence for their translation. We also annotated 635 mouse circRNAs, and although 20% of them are orthologous to human circRNAs, the sequence conservation of these circRNA orthologs is no higher than that of their neighboring linear exons. The previously proposed miR-7 sponge, CDR1as, is one of only two circRNAs with more miRNA sites than expected by chance, with the next best miRNA-sponge candidate deriving from a gene encoding a primate-specific zinc-finger protein, ZNF91. Conclusions Our results provide a new framework for future investigation of this intriguing topological isoform while raising doubts regarding a biological function of most circRNAs. Electronic supplementary material The online version of this article (doi:10.1186/s13059-014-0409-z) contains supplementary material, which is available to authorized users.

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The Landscape of long noncoding RNA classification.

Georges St. Laurent, Claes Wahlestedt, Philipp Kapranov (2015)

Advances in the depth and quality of transcriptome sequencing have revealed many new classes of long noncoding RNAs (lncRNAs). lncRNA classification has mushroomed to accommodate these new findings, even though the real dimensions and complexity of the noncoding transcriptome remain unknown. Although evidence of functionality of specific lncRNAs continues to accumulate, conflicting, confusing, and overlapping terminology has fostered ambiguity and lack of clarity in the field in general. The lack of fundamental conceptual unambiguous classification framework results in a number of challenges in the annotation and interpretation of noncoding transcriptome data. It also might undermine integration of the new genomic methods and datasets in an effort to unravel the function of lncRNA. Here, we review existing lncRNA classifications, nomenclature, and terminology. Then, we describe the conceptual guidelines that have emerged for their classification and functional annotation based on expanding and more comprehensive use of large systems biology-based datasets. Copyright © 2015 Elsevier Ltd. All rights reserved.

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Author and article information

Contributors

Jianbo Wang: URI : https://loop.frontiersin.org/people/290226/overview

Journal

Journal ID (nlm-ta): Front Plant Sci

Journal ID (iso-abbrev): Front Plant Sci

Journal ID (publisher-id): Front. Plant Sci.

Title: Frontiers in Plant Science

Publisher: Frontiers Media S.A.

ISSN (Electronic): 1664-462X

Publication date (Electronic): 26 September 2022

Publication date Collection: 2022

Volume: 13

Electronic Location Identifier: 990656

Affiliations

State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan University , Wuhan, China

Author notes

Edited by: Jianping Wang, University of Florida, United States

Reviewed by: Shuxia Li, Chinese Academy of Tropical Agricultural Sciences, China; Tian Li, Institute of Crop Sciences (CAAS), China

*Correspondence: Jianbo Wang, jbwang@ 123456whu.edu.cn

This article was submitted to Plant Genetics, Epigenetics and Chromosome Biology, a section of the journal Frontiers in Plant Science

Article

DOI: 10.3389/fpls.2022.990656

PMC ID: 9549252

PubMed ID: 36226282

SO-VID: 01a334d3-5fc3-440f-91b8-503f72f21346

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

History

Date received : 10 July 2022

Date accepted : 31 August 2022

Page count

Figures: 8, Tables: 1, Equations: 1, References: 55, Pages: 19, Words: 11409

Funding

Funded by: State Key Basic Research and Development Plan of China

Award ID: 2013CB126900

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Non-coding RNA expression analysis revealed the molecular mechanism of flag leaf heterosis in inter-subspecific hybrid rice

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Plant MYBs

Most cited references 55

Origin, biogenesis, and activity of plant microRNAs.

Expanded identification and characterization of mammalian circular RNAs

The Landscape of long noncoding RNA classification.

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