High-throughput sequencing reveals microRNAs in response to heat stress in the head kidney of rainbow trout (Oncorhynchus mykiss)

Ma, Fengwang; Liu, Zhe; Huang, Jinxin; Li, Yongjuan; Kang, Yujun; Liu, Xiaoxia; Wang, Jianfu

doi:10.1007/s10142-019-00682-3

Cited by 31 publications

(9 citation statements)

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“…miRNAs play vital regulatory roles in plant growth and development and respond to environmental factors by negatively regulating protein-coding genes at the posttranscriptional level, thus regulating various biological processes ( Song et al, 2019 ). It has been shown that miRNAs are involved throughout the development of reproductive organs, leaves, and stems and respond to high salinity, drought, and low-temperature stress ( Ma et al, 2019 ). The application of high-throughput sequencing techniques to investigate the effects of cold stress on the expression of the conserved and nonconserved miRNAs in plants has been reported in Arabidopsis thaliana ( Sunkar and Zhu, 2004 ), Oryza sativa ( Lv et al, 2010 ), Zea mays ( Yang et al, 2011 ), Glycine max ( Xu et al, 2016 ), and Triticum aestivum ( Wang et al, 2014 ).…”

Section: Introductionmentioning

confidence: 99%

Small RNA Sequencing Revealed that miR4415, a Legume-Specific miRNA, was Involved in the Cold Acclimation of Ammopiptanthus nanus by Targeting an L-Ascorbate Oxidase Gene and Regulating the Redox State of Apoplast

et al. 2022

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MicroRNAs (miRNAs) are small endogenous single-stranded RNAs that regulate plant growth, development, and environmental stress response posttranscriptionally. Ammopiptanthus nanus, a rare evergreen broad-leaved shrub in the temperate area of Central Asia, can tolerate freezing stress as low as –30 degrees centigrade in winter, and miRNA might be involved in the cold acclimation which enables A. nanus to obtain tolerance to freezing stress. Systematic identification and functional analysis of the miRNAs involved in the cold acclimation in A. nanus may promote understanding of the miRNA-mediated gene regulation network underlying cold acclimation. Here, based on small RNA and degradome sequencing, 256 miRNAs and 1,808 miRNA-target pairs were identified in A. nanus. A total of 39 cold-responsive miRNAs were identified, of which 29 were upregulated and ten were downregulated. These cold-responsive miRNAs may participate in the cold acclimation by regulating redox homeostasis (miR398, miR4415, and miR408), calcium signaling (miR5225 and miR5211), growth and development (miR159 and miR390), and small RNA–mediated gene silencing (miR168 and miR1515). We found that miR4415, a legume-specific miRNA, is involved in the cold acclimation of A. nanus by targeting an L-ascorbate oxidase gene and then regulating the redox state of the apoplast. Our study provides important data for understanding the regulatory role of miRNA in the cold acclimation of A. nanus.

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Section: Introductionmentioning

confidence: 99%

Small RNA Sequencing Revealed that miR4415, a Legume-Specific miRNA, was Involved in the Cold Acclimation of Ammopiptanthus nanus by Targeting an L-Ascorbate Oxidase Gene and Regulating the Redox State of Apoplast

et al. 2022

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“…Previous studies have shown that the adaptive regulation of organisms in response to heat stress was mainly in the differences in transcription levels [6][7][8], and was also accompanied by the regulatory effect of noncoding RNA on protein metabolism, immune response, apoptosis, etc. [9].…”

Section: Introductionmentioning

confidence: 99%

Integrated analysis of the responses of a circRNA-miRNA-mRNA ceRNA network to heat stress in rainbow trout (Oncorhynchus mykiss) liver

et al. 2021

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Background With the intensification of global warming, rainbow trout (Oncorhynchus mykiss) suffer from varying degrees of thermal stimulation, leads to mass mortality, which severely restrict the development of aquaculture. Understanding the molecular regulatory mechanisms of rainbow trout under heat stress is useful to develop approaches to relieve symptoms. Results Changes in nonspecific immune parameters revealed that a strong stress response was caused in rainbow trout at 24 °C, so we performed multiple transcriptomic analyses of rainbow trout liver under heat stress (HS, 24 °C) and control conditions (CG, 18 °C). A total of 324 DEcircRNAs, 105 DEmiRNAs, and 1885 DEmRNAs were identified. A ceRNA regulatory network was constructed and a total of 301 circRNA-miRNA and 51 miRNA-mRNA negative correlation pairs were screened, and three regulatory correlation pairs were predicted: novel_circ_003889 - novel-m0674-3p - hsp90ab1, novel_circ_002325 - miR-18-y - HSPA13 and novel_circ_002446 - novel-m0556-3p - hsp70. Some target genes involved in metabolic processes, biological regulation or response to stimulus were highly induced at high temperatures. Several important pathways involved in heat stress were characterized, such as protein processing in the ER, the estrogen signaling pathway, and the HIF-1 signaling pathway. Conclusions These results extend our understanding of the molecular mechanisms of the heat stress response and provide novel insight for the development of strategies that relieve heat stress.

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“…In our previous studies, we demonstrated that 24°C is the ‘critical high temperature’ that leads to serious adverse effects in rainbow trout (Wang et al ., 2016; Xia et al ., 2017). At present, our research group is investigating miRNAs that are induced at optimal (18°C) and high (24°C) temperatures in the head kidney tissues of rainbow trout (Ma et al ., 2019). Our previous research shows that the unique small RNA sequences generated from rainbow trout head kidney were aligned against the miRBase 20.0 (http://www.mirbase.org/) with complete matches to detect the conserved miRNAs in rainbow trout (Ma et al ., 2019).…”

Section: Introductionmentioning

confidence: 99%

“…At present, our research group is investigating miRNAs that are induced at optimal (18°C) and high (24°C) temperatures in the head kidney tissues of rainbow trout (Ma et al ., 2019). Our previous research shows that the unique small RNA sequences generated from rainbow trout head kidney were aligned against the miRBase 20.0 (http://www.mirbase.org/) with complete matches to detect the conserved miRNAs in rainbow trout (Ma et al ., 2019). MiRDeep2 (Friedländer et al ., 2011) and srna‐tools‐cli (http://srna-tools.…”

Section: Introductionmentioning

confidence: 99%

“…Herein our core objective was to validate if HSPA4L and CRT are indeed the target genes of novel miR‐434 and ‐242, respectively, and for this purpose we used the dual‐luciferase reporter assay system. Subsequently, we combined the results of Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment (Ma et al ., 2019) to analyse the main biological functions of the novel miRNA and their target genes, and to evaluate the related regulatory mechanisms. We believe that the findings of this study should provide insights into the regulatory role of miRNAs in heat stress and also enhance our understanding of how rainbow trout copes with heat stress.…”

Section: Introductionmentioning

confidence: 99%

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miR‐434 and miR‐242 have a potential role in heat stress response in rainbow trout (Oncorhynchus mykiss)

Liu

Wang

Liu

et al. 2021

Journal of Fish Biology

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MicroRNAs (miRNAs) are being extensively studied as they function as key metabolic regulators which play a role in the heat stress response. However, the role of miRNAs in heat stress remains uncertain and many new miRNAs have not yet been discovered. In a previous study, we performed high‐throughput sequencing of differentially expressed miRNAs identified on exposing rainbow trout (Oncorhynchus mykiss) to heat stress (18 vs. 24°C), which led to the identification of two novel miRNAs, temporarily named novel miR‐434 and ‐242. The differential expression level of these miRNAs was extremely significant (P < 0.01); we analysed target gene mRNA transcripts by bioinformatics software (miRanda). We found novel miR‐434 and ‐242 were predicted to regulate the transcripts of heat shock 70‐kDa protein 4‐like (HSPA4L) and calreticulin (CRT), respectively, by bioinformatics software. Here our core objective was to validate if HSPA4L and CRT are indeed the target genes of novel miR‐434 and ‐242, respectively, and for this purpose we used the dual‐luciferase reporter assay system. Target gene sequences were synthesized and cloned into a dual‐luciferase vector. To better understand the function of the target genes, we combined the previous sequencing results of Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment analysis. We found that novel miR‐434 regulated HSPA4L expression by binding to a putative binding site in the 3′‐UTR of HSPA4L, and luciferase activity inhibition was observed. In contrast, novel miR‐242 was not involved in regulating CRT expression. To conclude, we believe our results should serve as a foundation for future studies aiming to comprehensively understand the mechanisms used by rainbow trout to cope with heat stress.

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High-throughput sequencing reveals microRNAs in response to heat stress in the head kidney of rainbow trout (Oncorhynchus mykiss)

Cited by 31 publications

References 90 publications

Small RNA Sequencing Revealed that miR4415, a Legume-Specific miRNA, was Involved in the Cold Acclimation of Ammopiptanthus nanus by Targeting an L-Ascorbate Oxidase Gene and Regulating the Redox State of Apoplast

Small RNA Sequencing Revealed that miR4415, a Legume-Specific miRNA, was Involved in the Cold Acclimation of Ammopiptanthus nanus by Targeting an L-Ascorbate Oxidase Gene and Regulating the Redox State of Apoplast

Integrated analysis of the responses of a circRNA-miRNA-mRNA ceRNA network to heat stress in rainbow trout (Oncorhynchus mykiss) liver

miR‐434 and miR‐242 have a potential role in heat stress response in rainbow trout (Oncorhynchus mykiss)

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