From “Dark Matter” to “Star”: Insight Into the Regulation Mechanisms of Plant Functional Long Non-Coding RNAs

Chen, Qingshuai; Liu, Kui; Ru, Yu; Zhou, Bailing; Huang, Pingping; Cao, Zanxia; Zhou, Yaoqi; Wang, Jihua

doi:10.3389/fpls.2021.650926

Cited by 23 publications

(28 citation statements)

References 90 publications

(142 reference statements)

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“…In recent years, long non‐coding RNAs (lncRNAs) have been emerging as cryptic but important regulators of gene expression in various biological processes (Chen et al., 2021; Rinn & Chang, 2012). LncRNAs are generally defined as non‐protein‐coding RNA transcripts longer than 200 nucleotides (Guttman et al., 2013; Sun & Kraus, 2015), although a few studies have suggested some lncRNAs might also produce small polypeptides (Ruiz‐Orera et al., 2014).…”

Section: Introductionmentioning

confidence: 99%

Role of lncRNAs in cis‐ and trans‐regulatory responses to salt in Populus trichocarpa

Wang

Zhao

et al. 2022

The Plant Journal

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Long non-coding RNAs (lncRNAs) are emerging as versatile regulators in diverse biological processes. However, little is known about their cisand trans-regulatory contributions in gene expression under salt stress. Using 27 RNA-seq data sets from Populus trichocarpa leaves, stems and roots, we identified 2988 highconfidence lncRNAs, including 1183 salt-induced differentially expressed lncRNAs. Among them, 301 lncRNAs have potential for positively affecting their neighboring genes, predominantly in a cis-regulatory manner rather than by co-transcription. Additionally, a co-expression network identified six striking saltassociated modules with a total of 5639 genes, including 426 lncRNAs, and in these lncRNA sequences, the DNA/RNA binding motifs are enriched. This suggests that lncRNAs might contribute to distant gene expression of the salt-associated modules in a trans-regulatory manner. Moreover, we found 30 lncRNAs that have potential to simultaneously cisand trans-regulate salt-responsive homologous genes, and Ptlinc-NAC72, significantly induced under long-term salt stress, was selected for validating its regulation of the expression and functional roles of the homologs PtNAC72.A and PtNAC72.B (PtNAC72.A/B). The transient transformation of Ptlinc-NAC72 and a dual-luciferase assay of Ptlinc-NAC72 and PtNAC72.A/B promoters confirmed that Ptlinc-NAC72 can directly upregulate PtNAC72.A/B expression, and a presence/absence assay was further conducted to show that the regulation is probably mediated by Ptlinc-NAC72 recognizing the tandem elements (GAAAAA) in the PtNAC72.A/B 5 0 untranslated region (5 0 -UTR). Finally, the overexpression of Ptlinc-NAC72 produces a hypersensitive phenotype under salt stress. Altogether, our results shed light on the cisand trans-regulation of gene expression by lncRNAs in Populus and provides an example of longterm salt-induced Ptlinc-NAC72 that could be used to mitigate growth costs by conferring plant resilience to salt stress.

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Section: Introductionmentioning

confidence: 99%

Role of lncRNAs in cis‐ and trans‐regulatory responses to salt in Populus trichocarpa

Wang

Zhao

et al. 2022

The Plant Journal

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“…Their functions yet remain largely unknown. However, more and more studies have shown that some LncRNAs play a vital role in some biological progress ( Chen et al, 2021 ). For instance, in Arabidopsis , several functional LncRNAs were identified and involved in cell phosphate homeostasis ( Shin et al, 2006 ); in strawberry, one LncRNA was identified to play a role in fruit ripening ( Tang et al, 2021 ).…”

Section: Introductionmentioning

confidence: 99%

“…For instance, in Arabidopsis , several functional LncRNAs were identified and involved in cell phosphate homeostasis ( Shin et al, 2006 ); in strawberry, one LncRNA was identified to play a role in fruit ripening ( Tang et al, 2021 ). Functional LncRNAs were also detected in other plant species, for example, rice, maize, lemon, etc., ( Chen et al, 2021 ). In the Solanaceae family, functional LncRNAs were identified only in tomato ( Solanum Lycopersicum ) and relevant with disease resistance, hormone signal pathway, and nitrogen deficiency ( Cui et al, 2017 ; Wang et al, 2018 ; Jiang et al, 2020 ).…”

Section: Introductionmentioning

confidence: 99%

Comprehensive Transcriptome Analysis Uncovers Hub Long Non-coding RNAs Regulating Potassium Use Efficiency in Nicotiana tabacum

Chen

Meng

et al. 2022

Front. Plant Sci.

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Potassium (K) is the essential element for plant growth. It is one of the critical factors that determine crop yield, quality, and especially leaf development in tobacco. However, the molecular mechanism of potassium use efficiency (KUE), especially non-coding RNA, is still unknown. In this study, tobacco seedlings were employed, and their hydro-cultivation with K treatments of low and sufficient concentrations was engaged. Physiological analysis showed that low potassium treatment could promote malondialdehyde (MDA) accumulation and antioxidant enzyme activities such as peroxidase (POD), ascorbate-peroxidase (APX). After transcriptomic analysis, a total of 10,585 LncRNA transcripts were identified, and 242 of them were significantly differently expressed under potassium starvation. Furthermore, co-expression networks were constructed and generated 78 potential regulation modules in which coding gene and LncRNAs are involved and functional jointly. By further module-trait analysis and module membership (MM) ranking, nine modules, including 616 coding RNAs and 146 LncRNAs, showed a high correlation with K treatments, and 20 hub K-responsive LncRNAs were finally predicted. Following gene ontology (GO) analysis, the results showed potassium starvation inducing the pathway of antioxidative stress which is consistent with the physiology result mentioned above. Simultaneously, a part of detected LncRNAs, such as MSTRG.6626.1, MSTRG.11330.1, and MSTRG.16041.1, were co-relating with a bench of MYB, C3H, and NFYC transcript factors in response to the stress. Overall, this research provided a set of LncRNAs that respond to K concentration from starvation and sufficient supply. Simultaneously, the regulation network and potential co-functioning genes were listed as well. This massive dataset would serve as an outstanding clue for further study in tobacco and other plant species for nutrient physiology and molecular regulation mechanism.

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“…Therefore, there is a close regulatory relationship among lncRNAs, miRNAs, and mRNAs ( Voshall et al, 2017 ). In recent years, studies on lncRNA-miRNA-mRNA regulatory networks have revealed that lncRNAs, as a type of competing endogenous RNA (ceRNA), competitively bind the same miRNA as mRNAs, which reduces the probability of miRNA-mRNA binding and increases the expression of mRNAs ( Chen et al, 2021 ). To date, many lncRNAs involved in the nitrogen deficiency response have been identified in model plants ( Chen et al, 2016 ; Fukuda et al, 2019 , 2020 ; Liu et al, 2019 ; Lu et al, 2019 ; Wang et al, 2020a ).…”

Section: Introductionmentioning

confidence: 99%

Genome-Wide Identification and Characterization of Long Noncoding RNAs in Populus × canescens Roots Treated With Different Nitrogen Fertilizers

et al. 2022

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Nitrate (NO3−) and ammonium (NH4+) are the primary forms of inorganic nitrogen acquired by plant roots. LncRNAs, as key regulators of gene expression, are a class of non-coding RNAs larger than 200 bp. However, knowledge about the regulatory role of lncRNAs in response to different nitrogen forms remains limited, particularly in woody plants. Here, we performed strand-specific RNA-sequencing of P. × canescens roots under three different nitrogen fertilization treatments. In total, 324 lncRNAs and 6,112 mRNAs were identified as showing significantly differential expression between the NO3− and NH4NO3 treatments. Moreover, 333 lncRNAs and 6,007 mRNAs showed significantly differential expression between the NH4+ and NH4NO3 treatments. Further analysis suggested that these lncRNAs and mRNAs have different response mechanisms for different nitrogen forms. In addition, functional annotation of cis and trans target mRNAs of differentially expressed lncRNAs indicated that 60 lncRNAs corresponding to 49 differentially expressed cis and trans target mRNAs were involved in plant nitrogen metabolism and amino acid biosynthesis and metabolism. Furthermore, 42 lncRNAs were identified as putative precursors of 63 miRNAs, and 28 differentially expressed lncRNAs were potential endogenous target mimics targeted by 96 miRNAs. Moreover, ceRNA regulation networks were constructed. MSTRG.6097.1, MSTRG.13550.1, MSTRG.2693.1, and MSTRG.12899.1, as hub lncRNAs in the ceRNA networks, are potential candidate lncRNAs for studying the regulatory mechanism in poplar roots under different nitrogen fertilization treatments. The results provide a basis for obtaining insight into the molecular mechanisms of lncRNA responses to different nitrogen forms in woody plants.

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From “Dark Matter” to “Star”: Insight Into the Regulation Mechanisms of Plant Functional Long Non-Coding RNAs

Cited by 23 publications

References 90 publications

Role of lncRNAs in cis‐ and trans‐regulatory responses to salt in Populus trichocarpa

Role of lncRNAs in cis‐ and trans‐regulatory responses to salt in Populus trichocarpa

Comprehensive Transcriptome Analysis Uncovers Hub Long Non-coding RNAs Regulating Potassium Use Efficiency in Nicotiana tabacum

Genome-Wide Identification and Characterization of Long Noncoding RNAs in Populus × canescens Roots Treated With Different Nitrogen Fertilizers

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