Systematic identification and characterization of circular RNAs involved in flag leaf senescence of rice

Abstract

Main conclusion Circular RNAs (circRNAs) identification, expression profiles, and construction of circRNA-parental gene relationships and circRNA-miRNA-mRNA ceRNA networks indicate that circRNAs are involved in flag leaf senescence of rice. Abstract Circular RNAs (circRNAs) are a class of 3′-5′ head-to-tail covalently closed non-coding RNAs which have been proved to play important roles in various biological processes. However, no systematic identification of circRNAs associated with leaf senescence in rice has been studied. In this study, a genome-wide high-throughput sequencing analysis was performed using rice flag leaves developing from normal to senescence. Here, a total of 6612 circRNAs were identified, among which, 113 circRNAs were differentially expressed (DE) during the leaf senescence process. Moreover, 4601 (69.59%) circRNAs were derived from the exons or introns of their parental genes, while 2110 (71%) of the parental genes produced only one circRNA. The sequence alignment analysis showed that hundreds of rice circRNAs were conserved among different plant species. Gene Ontology (GO) enrichment analysis revealed that parental genes of DE circRNAs were enriched in many biological processes closely related to leaf senescence. Through weighted gene co-expression network analysis (WGCNA), six continuously down-expressed circRNAs, 18 continuously up-expressed circRNAs and 15 turn-point high-expressed circRNAs were considered to be highly associated with leaf senescence. Additionally, a total of 17 senescence-associated circRNAs were predicted to have parental genes, in which, regulations of three circRNAs to their parental genes were validated by qRT-PCR. The competing endogenous RNA (ceRNA) networks were also constructed. And a total of 11 senescence-associated circRNAs were predicted to act as miRNA sponges to regulate mRNAs, in which, regulation of two circRNAs to eight mRNAs was validated by qRT-PCR. It is discussed that senescence-associated circRNAs were involved in flag leaf senescence probably through mediating their parental genes and ceRNA networks, to participate in several well-studied senescence-associated processes, mainly including the processes of transcription, translation, and posttranslational modification (especially protein glycosylation), oxidation–reduction process, involvement of senescence-associated genes, hormone signaling pathway, proteolysis, and DNA damage repair. This study not only showed the systematic identification of circRNAs involved in leaf senescence of rice, but also laid a foundation for functional research on candidate circRNAs.

Identification and Functional Prediction of Poplar Root circRNAs Involved in Treatment With Different Forms of Nitrogen

“…Moreover, miRNAs, as noncoding RNAs also play a key role in regulating poplar root responses to different N forms (Zhou and Wu, 2022a). CircRNAs, as another noncoding RNA, exist widely in different tissues of plants and play a key role in plant regulation of growth and development and resistance to abiotic stress (Zhang et al, 2020;Huang et al, 2021;Li et al, 2021;Ma et al, 2021). However, circRNAs in poplar root responses to different N forms have not been reported.…”

Identification and Characterization of Circular RNAs Involved in the Flower Development and Senescence of Rhododendron delavayi Franch

“…It was not until the first discovery of circRNAs in Arabidopsis thaliana in 2014 [ 15 ] that research on circRNA in plants began. Since then, a large number of circRNAs have been identified in various plants, such as cucumber [ 32 ], corn [ 33 ], wheat [ 34 ], rice [ 2 ], and sweet pepper [ 19 ]. These studies revealed the essential roles of circRNAs in various biological processes in plants.…”

“…For example, it has been reported that 53 differentially expressed circRNAs in the circRNA-miRNA-mRNA network of sea-buckthorn fruits might function as the miRNA sponge in fruits development [ 35 ]. In another study of circRNAs in rice flag leaves, three networks were constructed and several key circRNAs were found to act as the miRNA sponge, which is involved in large-scale gene regulation related to leaf senescence [ 2 ]. In this study, we identified 10 differentially expressed circRNAs that can potentially bind to miRNAs, and constructed 7 circRNA-miRNA-mRNA networks.…”

“…Flowers undergo a series of developmental, physiological, and metabolic changes in an orderly manner. Senescence is a fundamental developmental process involving complex regulation at multiple levels [ 2 ]. Moreover, development and senescence have a significant influence on the length of flower lifespans of plants, which is of great significance to the ornamental value of flowers.…”

Multiple Layers of Regulation on Leaf Senescence: New Advances and Perspectives

“…For example, miR156, miR164, miR172, and miR840 regulate leaf senescence by suppressing their target genes ( Kim et al, 2009 ; Wu et al, 2016 , 2020 ; Tian et al, 2019 ; Yujun et al, 2019 ; Roussin-Leveillee et al, 2020 ). In addition to miRNAs, circular RNA (circRNA), and long non-coding RNA (lncRNAs) participate in leaf senescence of rice by a competitive endogenous RNA (CeRNA) network ( Huang et al, 2021a , b ). Interestingly, EIN3 and clock-associated PSEUDO-RESPONSE REGULATOR 9 (PRR9) up-regulate the transcription level of ORE1 by inhibiting the transcription of miR164 ( Li et al, 2013 ; Kim H. et al, 2018 ).…”