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Volume 49 Issue 12
Dec.  2022
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Article Contents

CircRNA: a rising star in plant biology

doi: 10.1016/j.jgg.2022.05.004
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This work was supported by grants of Key project of intergovernmental International Science and Technology Innovation Cooperation, MOST of China (2022YFE0100500) and the National Key Laboratory of Crop Genetic Improvement Self-research Program (ZW18B0102).

  • Received Date: 2022-03-26
  • Accepted Date: 2022-05-18
  • Rev Recd Date: 2022-05-17
  • Publish Date: 2022-05-27
  • Circular RNAs (circRNAs) are covalently closed single-stranded RNA molecules, which are widespread in eukaryotic cells. As regulatory molecules, circRNAs have various functions, such as regulating gene expression, binding miRNAs or proteins, and being translated into proteins, which are important for cell proliferation and cell differentiation, individual growth and development, as well as many other biological processes. However, compared with that in animal models, studies of circRNAs in plants lags behind and, particularly, the regulatory mechanisms of biogenesis and molecular functions of plant circRNAs remain elusive. Recent studies have shown that circRNAs are wide spread in plants with tissue- or development-specific expression patterns and are responsive to a variety of environmental stresses. In this review, we summarize these advances, focusing on the regulatory mechanisms of biogenesis, molecular and biological functions of circRNAs, and the methods for investigating circRNAs. We also discuss the challenges and the prospects of plant circRNA studies.
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  • Abdelmohsen, K., Panda, A.C., Munk, R., Grammatikakis, I., Dudekula, D.B., De, S., Kim, J., Noh, J.H., Kim, K.M., Martindale, J.L. et al., 2017. Identification of HuR target circular RNAs uncovers suppression of PABPN1 translation by CircPABPN1. RNA Biol. 14, 361-369
    Aktas, T., Ilik, I.A., Maticzka, D., Bhardwaj, V., Rodrigues, C.P., Mittler, G., Manke, T., Backofen, R.,Akhtar, A., 2017. DHX9 suppresses RNA processing defects originating from the Alu invasion of the human genome. Nature 544, 115-119
    Ashwal-Fluss, R., Meyer, M., Pamudurti, N.R., Ivanov, A., Bartok, O., Hanan, M., Evantal, N., Memczak, S., Rajewsky, N., Kadener, S., 2014. circRNA biogenesis competes with pre-mRNA splicing. Mol. Cell 56, 55-66
    Barrett, S.P., Wang, P.L.,Salzman, J., 2015. Circular RNA biogenesis can proceed through an exon-containing lariat precursor. Elife 4, e07540
    Chen, L.F., Ding, X.L., Zhang, H., He, T.T., Li, Y.W., Wang, T.L., Li, X.Q., Jin, L., Song, Q.J., Yang, S.P., et al., 2018b. Comparative analysis of circular RNAs between soybean cytoplasmic male-sterile line NJCMS1A and its maintainer NJCMS1B by high-throughput sequencing. BMC Genom. 19
    Chen, L., Yu, Y.Y., Zhang, X.C., Liu, C., Ye, C.Y., Fan, L.J., 2016. PcircRNA_finder: a software for circRNA prediction in plants. Bioinformatics 32, 3528-3529
    Chen, L., Zhang, P., Fan, Y., Lu, Q., Li, Q., Yan, J.B., Muehlbauer, G.J., Schnable, P.S., Dai, M.Q.,Li, L., 2018a. Circular RNAs mediated by transposons are associated with transcriptomic and phenotypic variation in maize. New Phytol. 217, 1292-1306
    Chen, S., Cao, X.F., Zhang, J.Y., Wu, W.Y., Zhang, B.,Zhao, F.Q., 2022. circVAMP3 drives CAPRIN1 phase separation and inhibits hepatocellular carcinoma by suppressing c-Myc translation. Adv. Sci. 9, e2103817
    Chen, X., Sun, S., Liu, F.J., Shen, E.H., Liu, L., Ye, C.Y., Xiao, B.G., Timko, M.P., Zhu, Q.H., Fan, L.J., et al., 2019. A transcriptomic profile of topping responsive non-coding RNAs in tobacco roots (Nicotiana tabacum). BMC Genom. 20, 856
    Cheng, J.P., Zhang, Y., Li, Z.W., Wang, T.Y., Zhang, X.T.,Zheng, B.L., 2018. A lariat-derived circular RNA is required for plant development in Arabidopsis. Sci. China Life Sci. 61, 204-213
    Chu, Q.J., Bai, P.P., Zhu, X.T., Zhang, X.C., Mao, L.F., Zhu, Q.H., Fan, L.J.,Ye, C.Y., 2020. Characteristics of plant circular RNAs. Briefings Bioinf. 21, 135-143
    Chu, Q.J., Ding, Y.W., Xu, X.X., Ye, C.Y., Zhu, Q.H., Guo, L.B.,Fan, L.J., 2022. Recent origination of circular RNAs in plants. New Phytol. 233, 515-525
    Chu, Q., Zhang, X., Zhu, X., Liu, C., Mao, L., Ye, C., Zhu, Q.H.,Fan, L., 2017. PlantcircBase: a database for plant circular RNAs. Mol. Plant 10, 1126-1128
    Conn, S.J., Pillman, K.A., Toubia, J., Conn, V.M., Salmanidis, M., Phillips, C.A., Roslan, S., Schreiber, A.W., Gregory, P.A.,Goodall, G.J., 2015. The RNA binding protein Quaking regulates formation of circRNAs. Cell 160, 1125-1134
    Conn, V.M., Hugouvieux, V., Nayak, A., Conos, S.A., Capovilla, G., Cildir, G., Jourdain, A., Tergaonkar, V., Schmid, M., Zubieta, C., et al., 2017. A circRNA from SEPALLATA3 regulates splicing of its cognate mRNA through R-loop formation. Native Plants 3, 17053
    Dahl, M., Daugaard, I., Andersen, M.S., Hansen, T.B., Gronbaek, K., Kjems, J.,Kristensen, L.S., 2018. Enzyme-free digital counting of endogenous circular RNA molecules in B-cell malignancies. Lab. Invest. 98, 1657-1669
    Di Timoteo, G., Dattilo, D., Centron-Broco, A., Colantoni, A., Guarnacci, M., Rossi, F., Incarnato, D., Oliviero, S., Fatica, A., Morlando, M., et al., 2020. Modulation of circRNA metabolism by m6A modification. Cell Rep. 31, 107641
    Fan, J., Quan, W., Li, G.B., Hu, X.H., Wang, Q., Wang, H., Li, X.P., Luo, X., Feng, Q., Hu, Z.J., et al., 2020. circRNAs are involved in the rice-magnaporthe oryzae interaction. Plant Physiol. 182, 272-286
    Ferreira, H.J., Davalos, V., de Moura, M.C., Soler, M., Perez-Salvia, M., Bueno-Costa, A., Setien, F., Moran, S., Villanueva, A.,Esteller, M., 2018. Circular RNA CpG island hypermethylation-associated silencing in human cancer. Oncotarget 9, 29208-29219
    Fu, X.Z., Zhang, X.Y., Qiu, J.Y., Zhou, X., Yuan, M., He, Y.Z., Chun, C.P., Cao, L., Ling, L.L.,Peng, L.Z., 2019. Whole-transcriptome RNA sequencing reveals the global molecular responses and ceRNA regulatory network of mRNAs, lncRNAs, miRNAs and circRNAs in response to copper toxicity in Ziyang Xiangcheng (Citrus junos Sieb. Ex Tanaka). BMC Plant Biol. 19, 509
    Gao, Y., Wang, J.F.,Zhao, F.Q., 2015. CIRI: an efficient and unbiased algorithm for de novo circular RNA identification. Genome Biol. 16, 4
    Gao, Z., Li, J., Luo, M., Li, H., Chen, Q.J., Wang, L., Song, S.R., Zhao, L.P., Xu, W.P., Zhang, C.X., et al., 2019. Characterization and cloning of grape circular RNAs identified the cold resistance-related Vv-circATS1. Plant Physiol. 180, 966-985
    Ghorbani, A., Izadpanah, K., Peters, J.R., Dietzgen, R.G.,Mitter, N., 2018. Detection and profiling of circular RNAs in uninfected and maize Iranian mosaic virus-infected maize. Plant Sci. 274, 402-409
    Guo, J.U., Agarwal, V., Guo, H.L.,Bartel, D.P., 2014. Expanded identification and characterization of mammalian circular RNAs. Genome Biol. 15, 409
    Hansen, T.B., 2018. Improved circRNA identification by combining prediction algorithms. Front. Cell Dev. Biol. 6, 20
    Hansen, T.B., Jensen, T.I., Clausen, B.H., Bramsen, J.B., Finsen, B., Damgaard, C.K.,Kjems, J., 2013. Natural RNA circles function as efficient microRNA sponges. Nature 495, 384-388
    Hansen, T.B., Veno, M.T., Damgaard, C.K.,Kjems, J., 2016. Comparison of circular RNA prediction tools. Nucleic Acids Res. 44, e58
    He, X.Y., Guo, S.R., Wang, Y., Wang, L.W., Shu, S.,Sun, J., 2020. Systematic identification and analysis of heat-stress-responsive lncRNAs, circRNAs and miRNAs with associated co-expression and ceRNA networks in cucumber (Cucumis sativus L.). Physiol. Plantarum 168, 736-754
    Hong, Y.H., Meng, J., Zhang, M.,Luan, Y.S., 2020. Identification of tomato circular RNAs responsive to Phytophthora infestans. Gene 746, 144652
    Hsu, M.T.,Cocaprados, M., 1979. Electron microscopic evidence for the circular form of RNA in the cytoplasm of eukaryotic cells. Nature 280, 339-340
    Huang, X.P., Zhang, H.Y., Guo, R., Wang, Q., Liu, X.Z., Kuang, W.G., Song, H.Y., Liao, J.L., Huang, Y.J.,Wang, Z.H., 2021. Systematic identification and characterization of circular RNAs involved in flag leaf senescence of rice. Planta 253, 26
    Ivanov, A., Memczak, S., Wyler, E., Torti, F., Porath, H.T., Orejuela, M.R., Piechotta, M., Levanon, E.Y., Landthaler, M., Dieterich, C., et al., 2015. Analysis of intron sequences reveals hallmarks of circular RNA biogenesis in animals. Cell Rep. 10, 170-177
    Jeck, W.R., Sorrentino, J.A., Wang, K., Slevin, M.K., Burd, C.E., Liu, J.Z., Marzluff, W.F.,Sharpless, N.E., 2013. Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA 19, 141-157
    Kramer, M.C., Liang, D.M., Tatomer, D.C., Gold, B., March, Z.M., Cherry, S.,Wilusz, J.E., 2015. Combinatorial control of Drosophila circular RNA expression by intronic repeats, hnRNPs, and SR proteins. Genes Dev. 29, 2168-2182
    Kristensen, L.S., Andersen, M.S., Stagsted, L.V.W., Ebbesen, K.K., Hansen, T.B.,Kjems, J., 2019. The biogenesis, biology and characterization of circular RNAs. Nat. Rev. Genet. 20, 675-691
    Li, Q.D., Wang, Y.C., Wu, S., Zhou, Z., Ding, X.J., Shi, R.H., Thorne, R.F., Zhang, X.D., Hu, W.L.,Wu, M.A., 2019. CircACC1 regulates assembly and activation of AMPK complex under metabolic stress. Cell Metabol. 30, 157-173
    Li, S.Q., Li, X., Xue, W., Zhang, L., Yang, L.Z., Cao, S.M., Lei, Y.N., Liu, C.X., Guo, S.K., Shan, L., et al., 2021. Screening for functional circular RNAs using the CRISPR-Cas13 system. Nat. Methods 18, 51-59
    Li, T.W., Shao, Y.F., Fu, L.Y., Xie, Y., Zhu, L.W., Sun, W.L., Yu, R., Xiao, B.X.,Guo, J.M., 2018. Plasma circular RNA profiling of patients with gastric cancer and their droplet digital RT-PCR detection. J. Mol. Med. 96, 85-96
    Li, X., Liu, C.X., Xue, W., Zhang, Y., Jiang, S., Yin, Q.F., Wei, J., Yao, R.W., Yang, L.,Chen, L.L., 2017. Coordinated circRNA biogenesis and function with NF90/NF110 in viral infection. Mol. Cell 67, 214-227
    Li, Z.Y., Huang, C., Bao, C., Chen, L., Lin, M., Wang, X.L., Zhong, G.L., Yu, B., Hu, W.C., Dai, L.M., et al., 2015 Exon-intron circular RNAs regulate transcription in the nucleus. Nat. Struct. Mol. Biol. 22, 256-264
    Li, Z.W., Wang, S.P., Cheng, J.P., Su, C.B., Zhong, S.X., Liu, Q., Fang, Y.D., Yu, Y., Lv, H., Zheng, Y., et al., 2016. Intron lariat RNA inhibits microRNA biogenesis by sequestering the dicing complex in Arabidopsis. PLoS Genet. 12, e1006422
    Liang, D.M., Tatomer, D.C., Luo, Z., Wu, H., Yang, L., Chen, L.L., Cherry, S.,Wilusz, J.E., 2017. The output of protein-coding genes shifts to circular RNAs when the pre-mRNA processing machinery is limiting. Mol. Cell 68, 940-954
    Liang, Y.W., Zhang, Y.Z., Xu, L.A., Zhou, D., Jin, Z.M., Zhou, H.Y., Lin, S., Cao, J.S.,Huang, L., 2019. CircRNA expression pattern and ceRNA and miRNA-mRNA networks involved in anther development in the CMS line of Brassica campestris. Int. J. Mol. Sci. 20, 4808
    Liao, X., Li, X.J., Zheng, G.T., Chang, F.R., Fang, L., Yu, H., Huang, J.,Zhang, Y.F., 2022. Mitochondrion-encoded circular RNAs are widespread and translatable in plants.
    Liu, C.X., Li, X., Nan, F., Jiang, S., Gao, X., Guo, S.K., Xue, W., Cui, Y.G., Dong, K.G., Ding, H.H., et al., 2019b. Structure and degradation of circular RNAs regulate PKR activation in innate immunity. Cell 177, 865-880
    Liu, S., Wang, Q.J., Li, X.Y., Wang, G.B.,Wan, Y.L., 2019a. Detecting of chloroplast circular RNAs in Arabidopsis thaliana. Plant Signal. Behav. 14, 1621088
    Liu, T.F., Zhang, L., Chen, G.,Shi, T.L., 2017. Identifying and characterizing the circular RNAs during the lifespan of Arabidopsis leaves. Front. Plant Sci. 8, 1278
    Liu, X.Q., Gao, Y.B., Liao, J.K., Miao, M., Chen, K., Xi, F.H., Wei, W.T., Wang, H.H., Wang, Y.S., Xu, X., et al., 2021. Genome-wide profiling of circular RNAs, alternative splicing, and R-loops in stem-differentiating xylem of Populus trichocarpa. J. Integr. Plant Biol. 63, 1294-1308
    Lu, T.T., Cui, L.L., Zhou, Y., Zhu, C.R., Fan, D.L., Gong, H., Zhao, Q., Zhou, C.C., Zhao, Y., Lu, D.F., et al., 2015. Transcriptome-wide investigation of circular RNAs in rice. RNA 21, 2076-2087
    Luo, Z., Han, L.Q., Qian, J.,Li, L., 2019. Circular RNAs exhibit extensive intraspecific variation in maize. Planta 250, 69-78
    Lv, L.L., Yu, K.Y., Lu, H.Y., Zhang, X.Q., Liu, X.Q., Sun, C.Y., Xu, H.Q., Zhang, J.Y., He, X.H.,Zhang, D., 2020. Transcriptome-wide identification of novel circular RNAs in soybean in response to low-phosphorus stress. PLoS One 15, e227243
    Ma, P., Gao, S., Zhang, H.Y., Li, B.Y., Zhong, H.X., Wang, Y.K., Hu, H.M., Zhang, H.K., Luo, B.W., Zhang, X., et al., 2021. Identification and characterization of circRNAs in maize seedlings under deficient nitrogen. Plant Biol. 23, 850-860
    Memczak, S., Jens, M., Elefsinioti, A., Torti, F., Krueger, J., Rybak, A., Maier, L., Mackowiak, S.D., Gregersen, L.H., Munschauer, M., et al., 2013. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 495, 333-338
    Muthusamy, M., Kim, J.H., Kim, J.A.,Lee, S.I., 2021. Plant RNA binding proteins as critical modulators in drought, high salinity, heat, and cold stress responses: an updated overview. Int. J. Mol. Sci. 22, 6731
    Pan, T., Sun, X.Q., Liu, Y.X., Li, H., Deng, G.B., Lin, H.H.,Wang, S.H., 2018. Heat stress alters genome-wide profiles of circular RNAs in Arabidopsis. Plant Mol. Biol. 96, 217-229
    Pan, Z.H., Cai, J.Y., Lin, J.T., Zhou, H.N., Peng, J.W., Liang, J.L., Xia, L., Yin, Q., Zou, B.J., Zheng, J., et al., 2020. A novel protein encoded by circFNDC3B inhibits tumor progression and EMT through regulating Snail in colon cancer. Mol. Cancer 19, 71
    Piwecka, M., Glazar, P., Hernandez-Miranda, L.R., Memczak, S., Wolf, S.A., Rybak-Wolf, A., Filipchyk, A., Klironomos, F., Jara, C.A.C., Fenske, P., et al., 2017. Loss of a mammalian circular RNA locus causes miRNA deregulation and affects brain function. Science 357, eaam8526
    Ren, Y.Z., Yue, H.F., Li, L., Xu, Y.H., Wang, Z.Q., Xin, Z.Y.,Lin, T.B., 2018. Identification and characterization of circRNAs involved in the regulation of low nitrogen-promoted root growth in hexaploid wheat. Biol. Res. 51, 43
    Salih, H., Wang, X., Chen, B.J., Jia, Y.H., Gong, W.F.,Du, X.M., 2021. Identification, characterization and expression profiling of circular RNAs in the early cotton fiber developmental stages. Genomics 113, 356-365
    Sanger, H.L., Klotz, G., Riesner, D., Gross, H.J.,Kleinschmidt, A.K., 1976. Viroids are single-stranded covalently closed circular RNA molecules existing as highly base-paired rod-like structures. Proc. Natl. Acad. Sci. U. S. A. 73, 3852-3856
    Seimiya, T., Otsuka, M., Iwata, T., Shibata, C., Tanaka, E., Suzuki, T., Koike, K., 2020. Emerging roles of exosomal circular RNAs in cancer. Front. Cell Dev. Biol. 8, 568366
    Szabo, L., Morey, R., Palpant, N.J., Wang, P.L., Afari, N., Jiang, C., Parast, M.M., Murry, C.E., Laurent, L.C., Salzman, J., 2015. Statistically based splicing detection reveals neural enrichment and tissue-specific induction of circular RNA during human fetal development. Genome Biol. 16, 126
    Tan, J.J., Zhou, Z.J., Niu, Y.J., Sun, X.Y.,Deng, Z.P., 2017 Identification and functional characterization of tomato circRNAs derived from genes involved in fruit pigment accumulation. Sci. Rep. 7, 8594
    Tang, C., Xie, Y., Yu, T., Liu, N., Wang, Z., Woolsey, R.J., Tang, Y., Zhang, X., Qin, W., Zhang, Y., et al., 2020. M6A-dependent biogenesis of circular RNAs in male germ cells. Cell Res. 30, 211-228
    Tong, W., Yu, J., Hou, Y., Li, F., Zhou, Q., Wei, C.,Bennetzen, J.L., 2018. Circular RNA architecture and differentiation during leaf bud to young leaf development in tea (Camellia sinensis). Planta 248, 1417-1429
    Vo, J.N., Cieslik, M., Zhang, Y., Shukla, S., Xiao, L., Zhang, Y., Wu, Y.M., Dhanasekaran, S.M., Engelke, C.G., Cao, X., et al., 2019. The landscape of circular RNA in cancer. Cell 176, 869-881
    Wang, H.Y., Wang, H.H., Zhang, H.X., Liu, S., Wang, Y.S., Gao, Y.B., Xi, F.H., Zhao, L.Z., Liu, B., Reddy, A.S.N., et al., 2019b. The interplay between microRNA and alternative splicing of linear and circular RNAs in eleven plant species. Bioinformatics 35, 3119-3126
    Wang, K., Wang, C., Guo, B.H., Song, K., Shi, C.H., Jiang, X., Wang, K.Y., Tan, Y.C., Wang, L.Q., Wang, L., et al., 2019c. CropCircDB: a Comprehensive Circular RNA Resource for Crops in Response to Abiotic Stress. Database-Oxford 2019, baz053
    Wang, P.L., Bao, Y., Yee, M.C., Barrett, S.P., Hogan, G.J., Olsen, M.N., Dinneny, J.R., Brown, P.O.,Salzman, J., 2014. Circular RNA is expressed across the eukaryotic tree of life. PLoS One 9, e90859
    Wang, W.H., Wang, J.L., Wei, Q.Z., Li, B.Y., Zhong, X.M., Hu, T.H., Hu, H.J.,Bao, C.L., 2019d. Transcriptome-wide identification and characterization of circular RNAs in leaves of Chinese Cabbage (Brassica rapa L. ssp. pekinensis) in Response to calcium deficiency-induced tip-burn. Sci. Rep. 9, 14544
    Wang, X.S., Chang, X.C., Jing, Y., Zhao, J.L., Fang, Q.W., Sun, M.Y., Zhang, Y.Z., Li, W.B.,Li, Y.G., 2020. Identification and functional prediction of soybean circRNAs involved in low-temperature responses. J. Plant Physiol. 250, 153188
    Wang, Y.X., Wang, Q., Gao, L.P., Zhu, B.Z., Luo, Y.B., Deng, Z.P.,Zuo, J.H., 2017b. Integrative analysis of circRNAs acting as ceRNAs involved in ethylene pathway in tomato. Physiol. Plantarum 161, 311-321
    Wang, Y., Xiong, Z.Y., Li, Q., Sun, Y.Y., Jin, J., Chen, H., Zou, Y., Huang, X.G.,Ding, Y., 2019a. Circular RNA profiling of the rice photo-thermosensitive genic male sterile line Wuxiang S reveals circRNA involved in the fertility transition. BMC Plant Biol. 19, 340
    Wang, Y.X., Yang, M., Wei, S.M., Qin, F.J., Zhao, H.J.,Suo, B., 2017a. Identification of circular RNAs and their targets in leaves of Triticum aestivum L. under dehydration stress. Front. Plant Sci. 7, 2024
    Westholm, J.O., Miura, P., Olson, S., Shenker, S., Joseph, B., Sanfilippo, P., Celniker, S.E., Graveley, B.R.,Lai, E.C., 2014. Genome-wide analysis of drosophila circular RNAs reveals their structural and sequence properties and age-dependent neural accumulation. Cell Rep. 9, 1966-1980
    Wu, Z.H., Huang, W., Qin, E.D., Liu, S., Liu, H., Grennan, A.K., Liu, H.,Qin, R., 2020. Comprehensive identification and expression profiling of circular RNAs during nodule development in Phaseolus vulgaris. Front. Plant Sci. 11, 587185
    Xiang, L.X., Cai, C.W., Cheng, J.R., Wang, L., Wu, C.F., Shi, Y.Z., Luo, J.Z., He, L., Deng, Y.S., Zhang, X., et al., 2018. Identification of circularRNAs and their targets in Gossypium under Verticillium wilt stress based on RNA-seq. PeerJ 6, e4500
    Xu, X.L., Zhang, J.W., Tian, Y.H., Gao, Y., Dong, X., Chen, W.B., Yuan, X.N., Yin, W.N., Xu, J.J., Chen, K., et al., 2020. CircRNA inhibits DNA damage repair by interacting with host gene. Mol. Cancer 19, 128
    Xu, Y.H., Ren, Y.Z., Lin, T.B.,Cui, D.Q., 2019. Identification and characterization of CircRNAs involved in the regulation of wheat root length. Biol. Res. 52, 19
    Yang, Y., Fan, X.J., Mao, M.W., Song, X.W., Wu, P., Zhang, Y., Jin, Y.F., Yang, Y., Chen, L.L., Wang, Y., et al., 2017. Extensive translation of circular RNAs driven by N6-methyladenosine. Cell Res. 27, 626-641
    Ye, C.Y., Chen, L., Liu, C., Zhu, Q.H.,Fan, L.J., 2015. Widespread noncoding circular RNAs in plants. New Phytol. 208, 88-95
    Ye, C.Y., Zhang, X.C., Chu, Q.J., Liu, C., Yu, Y.Y., Jiang, W.Q., Zhu, Q.H., Fan, L.J.,Guo, L.B., 2017. Full-length sequence assembly reveals circular RNAs with diverse non-GT/AG splicing signals in rice. RNA Biol. 14, 1055-1063
    Ye, J.Z., Wang, L., Li, S.Z., Zhang, Q.R., Zhang, Q.L., Tang, W.H., Wang, K., Song, K., Sablok, G., Sun, X.Y., et al., 2019. AtCircDB: a tissue-specific database for Arabidopsis circular RNAs. Briefings Bioinf. 20, 58-65
    Zaccara, S., Ries, R.J.,Jaffrey, S.R., 2019. Reading, writing and erasing mRNA methylation. Nat. Rev. Mol. Cell Biol. 20, 608-624
    Zeng, R.F., Zhou, J.J., Hu, C.G.,Zhang, J.Z., 2018. Transcriptome-wide identification and functional prediction of novel and flowering-related circular RNAs from trifoliate orange (Poncirus trifoliata L. Raf.). Planta 247, 1191-1202
    Zhang, H., Liu, S., Li, X.Y., Yao, L.J., Wu, H.Y., Baluska, F.,Wan, Y.L., 2021c. An antisense circular RNA regulates expression of RuBisCO small subunit genes in Arabidopsis. Front. Plant Sci. 12, 665014
    Zhang, J.Y., Hou, L.L., Zuo, Z.Q., Ji, P.F., Zhang, X.R., Xue, Y.C.,Zhao, F.Q., 2021a. Comprehensive profiling of circular RNAs with nanopore sequencing and CIRI-long. Nat. Biotechnol. 39, 836-845
    Zhang, J.J., Liu, R.Q., Zhu, Y.F., Gong, J.X., Yin, S.W., Sun, P.S., Feng, H., Wang, Q., Zhao, S.J., Wang, Z.Y., et al., 2020. Identification and characterization of circRNAs responsive to methyl jasmonate in Arabidopsis thaliana. Int. J. Mol. Sci. 21, 792
    Zhang, P., Fan, Y., Sun, X.P., Chen, L., Terzaghi, W., Bucher, E., Li, L.,Dai, M.Q., 2019. A large-scale circular RNA profiling reveals universal molecular mechanisms responsive to drought stress in maize and Arabidopsis. Plant J. 98, 697-713
    Zhang, X.O., Wang, H.B., Zhang, Y., Lu, X.H., Chen, L.L.,Yang, L., 2014. Complementary sequence-mediated exon circularization. Cell 159, 134-147
    Zhang, Y., Xue, W., Li, X., Zhang, J., Chen, S.Y., Zhang, J.L., Yang, L.,Chen, L.L., 2016. The biogenesis of nascent circular RNAs. Cell Rep. 15, 611-624
    Zhang, Y., Zhang, X.O., Chen, T., Xiang, J.F., Yin, Q.F., Xing, Y.H., Zhu, S.S., Yang, L.,Chen, L.L., 2013. Circular intronic long noncoding RNAs. Mol. Cell 51, 792-806
    Zhang, Z.Y., Wang, H.H., Wang, Y.S., Xi, F.H., Wang, H.Y., Kohnen, M.V., Gao, P.F., Wei, W.T., Chen, K., Liu, X.Q., et al., 2021a. Whole-genome characterization of chronological age-associated changes in methylome and circular RNAs in moso bamboo (Phyllostachys edulis) from vegetative to floral growth. Plant J. 106, 435-453
    Zhou, C., Molinie, B., Daneshvar, K., Pondick, J.V., Wang, J.K., Van Wittenberghe, N., Xing, Y., Giallourakis, C.C.,Mullen, A.C., 2017. Genome-wide maps of m6A circRNAs identify widespread and cell-type-specific methylation patterns that are distinct from mRNAs. Cell Rep. 20, 2262-2276
    Zhou, J.P., Yuan, M.Z., Zhao, Y.X., Quan, Q., Yu, D., Yang, H., Tang, X., Xin, X.H., Cai, G.Z., Qian, Q., et al., 2021b. Efficient deletion of multiple circle RNA loci by CRISPR-Cas9 reveals Os06circ02797 as a putative sponge for OsMIR408 in rice. Plant Biotechnol. J. 19, 1240-1252
    Zhou, R., Sanz-Jimenez, P., Zhu, X.T., Feng, J.W., Shao, L., Song, J.M.,Chen, L.L., 2021a. Analysis of rice transcriptome reveals the lncRNA/circRNA regulation in tissue development. Rice 14, 14
    Zhou, R., Xu, L.P., Zhao, L.P., Wang, Y.L.,Zhao, T.M., 2018a. Genome-wide identification of circRNAs involved in tomato fruit coloration. Biochem. Bioph. Res. Co. 499, 466-469
    Zhou, R., Zhu, Y.X., Zhao, J., Fang, Z.W., Wang, S.P., Yin, J.L., Chu, Z.H.,Ma, D.F., 2018b. Transcriptome-wide identification and characterization of potato circular RNAs in response to Pectobacterium carotovorum Subspecies brasiliense infection. Int. J. Mol. Sci. 19, 71
    Zhu, Y.X., Jia, J.H., Yang, L., Xia, Y.C., Zhang, H.L., Jia, J.B., Zhou, R., Nie, P.Y., Yin, J.L., Ma, D.F., et al., 2019. Identification of cucumber circular RNAs responsive to salt stress. BMC Plant Biol. 19, 164
    Zuo, J.H., Wang, Q., Zhu, B.Z., Luo, Y.B.,Gao, L.P., 2016. Deciphering the roles of circRNAs on chilling injury in tomato. Biochem. Bioph. Res. Co. 479, 132-138
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