Advertisement

Circular RNAs pp 329-343 | Cite as

CircRNAs in Plants

  • Xuelei Lai
  • Jérémie Bazin
  • Stuart Webb
  • Martin Crespi
  • Chloe ZubietaEmail author
  • Simon J. ConnEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1087)

Abstract

Circular RNAs (circRNAs) are covalently closed, single-stranded transcripts that are ubiquitously expressed in all eukaryotes and even prokaryotic archaea. Although once regarded as splicing artifacts, circRNAs are a novel class of regulatory molecules with diverse biological functions, including regulation of transcription, modulation of alternative splicing, and binding of miRNAs and proteins. The majority of studies of circRNAs have been performed in animals with a focus on the biogenesis, function, and mechanistic characterization of these molecules. In contrast, the study of circRNAs in plants is just emerging. Interestingly, recent circRNA profiling studies in model plant systems show distinct features of plant circRNAs compared with those from animals, including putative roles in stress response, differences in expression patterns, and novel biogenesis mechanisms. This provides a great opportunity to broaden our knowledge of circRNAs using plant model systems, such as Arabidopsis and rice, which are ideal for phenotypic characterization and genetic studies. In this review, we summarize current knowledge of plant circRNAs, discuss their identification and biogenesis, describe potential functions, and propose future perspectives for plant circRNA study.

Keywords

circRNAs Plants Transcriptomics Genome-wide profiling 

Notes

Acknowledgments

This work was supported by Australian Research Council Future Fellowship (FT160100318 to S.C.), Action Thématique et Incitative sur Programme (ATIP)-Avenir (to C.Z.), Agence Nationale de la Recherche (project FloPiNet to C.Z. and X.L.), Grenoble Alliance for Integrated Structural Cell Biology (ANR-10-LABX-49-01 to C.Z.), and the “Laboratoire d’Excellence (LABEX)” Saclay Plant Sciences (SPS; ANR-10-LABX-40) and the ANR grant SPLISIL, France (to M.C.).

Competing Financial Interests

The authors declare no competing financial interests.

References

  1. 1.
    Chen LL (2016) The biogenesis and emerging roles of circular RNAs. Nat Rev Mol Cell Biol 17(4):205–211CrossRefGoogle Scholar
  2. 2.
    Nigro JM, Cho KR, Fearon ER et al (1991) Scrambled exons. Cell 64(3):607–613CrossRefGoogle Scholar
  3. 3.
    Cocquerelle C, Mascrez B, Hetuin D et al (1993) Mis-splicing yields circular RNA molecules. FASEB J 7(1):155–160PubMedPubMedCentralGoogle Scholar
  4. 4.
    Wang PL, Bao Y, Yee MC et al (2014) Circular RNA is expressed across the eukaryotic tree of life. PLoS One 9(4):e95116Google Scholar
  5. 5.
    Danan M, Schwartz S, Edelheit S et al (2012) Transcriptome-wide discovery of circular RNAs in Archaea. Nucleic Acids Res 40(7):3131–3142CrossRefGoogle Scholar
  6. 6.
    Kopp F, Mendell JT (2018) Functional classification and experimental dissection of long noncoding RNAs. Cell 172(3):393–407CrossRefGoogle Scholar
  7. 7.
    Salzman J, Chen RE, Olsen MN et al (2013) Cell-type specific features of circular RNA expression. PLoS Genet 9(9):e1003777PubMedPubMedCentralGoogle Scholar
  8. 8.
    Salzman J, Gawad C, Wang PL et al (2012) Circular RNAs are the predominant transcript isoform from hundreds of human genes in diverse cell types. PLoS One 7(2):e30733CrossRefGoogle Scholar
  9. 9.
    Memczak S, Jens M, Elefsinioti A et al (2013) Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 495(7441):333–338CrossRefGoogle Scholar
  10. 10.
    Gao Y, Wang J, Zhao F (2015) CIRI: an efficient and unbiased algorithm for de novo circular RNA identification. Genome Biol 16:4CrossRefGoogle Scholar
  11. 11.
    Conn SJ, Pillman KA, Toubia J et al (2015) The RNA binding protein quaking regulates formation of circRNAs. Cell 160(6):1125–1134CrossRefGoogle Scholar
  12. 12.
    Hansen TB, Jensen TI, Clausen BH et al (2013) Natural RNA circles function as efficient microRNA sponges. Nature 495(7441):384–388CrossRefGoogle Scholar
  13. 13.
    Piwecka M, Glazar P, Hernandez-Miranda LR et al (2017) Loss of a mammalian circular RNA locus causes miRNA deregulation and affects brain function. Science 357(6357):eaam8526CrossRefGoogle Scholar
  14. 14.
    Greene J, Baird AM, Brady L et al (2017) Circular RNAs: biogenesis, function and role in human diseases. Front Mol Biosci 4:38CrossRefGoogle Scholar
  15. 15.
    Pamudurti NR, Bartok O, Jens M et al (2017) Translation of CircRNAs. Mol Cell 66(1):9–21 e27CrossRefGoogle Scholar
  16. 16.
    Granados-Riveron JT, Aquino-Jarquin G (2016) The complexity of the translation ability of circRNAs. Biochim Biophys Acta 1859(10):1245–1251CrossRefGoogle Scholar
  17. 17.
    Abe N, Matsumoto K, Nishihara M et al (2015) Rolling circle translation of circular RNA in living human cells. Sci Rep 5:16435CrossRefGoogle Scholar
  18. 18.
    Yang Y, Fan X, Mao M et al (2017) Extensive translation of circular RNAs driven by N(6)-methyladenosine. Cell Res 27(5):626–641CrossRefGoogle Scholar
  19. 19.
    Barrett SP, Salzman J (2016) Circular RNAs: analysis, expression and potential functions. Development 143(11):1838–1847CrossRefGoogle Scholar
  20. 20.
    Lasda E, Parker R (2014) Circular RNAs: diversity of form and function. RNA 20(12):1829–1842CrossRefGoogle Scholar
  21. 21.
    Salzman J (2016) Circular RNA expression: its potential regulation and function. Trends Genet 32(5):309–316CrossRefGoogle Scholar
  22. 22.
    Cortés-López M, Miura P (2016) Emerging functions of circular RNAs. Yale J Biol Med 89(4):527PubMedPubMedCentralGoogle Scholar
  23. 23.
    Fischer JW, Leung AK (2017) CircRNAs: a regulator of cellular stress. Crit Rev Biochem Mol Biol 52(2):220–233CrossRefGoogle Scholar
  24. 24.
    Patop IL, Kadener S (2018) circRNAs in Cancer. Curr Opin Genet Dev 48:121–127CrossRefGoogle Scholar
  25. 25.
    Toubia J, Conn VM, Conn SJ (2018) Don’t go in circles: confounding factors in gene expression profiling. EMBO J 37(11):e97945CrossRefGoogle Scholar
  26. 26.
    Darbani B, Noeparvar S, Borg S (2016) Identification of circular RNAs from the parental genes involved in multiple aspects of cellular metabolism in barley. Front Plant Sci 7:776CrossRefGoogle Scholar
  27. 27.
    Ye CY, Chen L, Liu C et al (2015) Widespread noncoding circular RNAs in plants. New Phytol 208(1):88–95CrossRefGoogle Scholar
  28. 28.
    Jeck WR, Sorrentino JA, Wang K et al (2013) Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA 19(2):141–157CrossRefGoogle Scholar
  29. 29.
    Chen G, Cui J, Wang L et al (2017) Genome-wide identification of circular RNAs in Arabidopsis thaliana. Front Plant Sci 8:1678CrossRefGoogle Scholar
  30. 30.
    Lu T, Cui L, Zhou Y et al (2015) Transcriptome-wide investigation of circular RNAs in rice. RNA 21(12):2076–2087CrossRefGoogle Scholar
  31. 31.
    Zhao W, Cheng Y, Zhang C et al (2017) Genome-wide identification and characterization of circular RNAs by high throughput sequencing in soybean. Sci Rep 7(1):5636CrossRefGoogle Scholar
  32. 32.
    Zuo J, Wang Q, Zhu B et al (2016) Deciphering the roles of circRNAs on chilling injury in tomato. Biochem Biophys Res Commun 479(2):132–138CrossRefGoogle Scholar
  33. 33.
    Wang ZP, Liu YF, Li DW et al (2017) Identification of circular RNAs in kiwifruit and their species-specific response to bacterial canker pathogen invasion. Front Plant Sci 8:413PubMedPubMedCentralGoogle Scholar
  34. 34.
    Szabo L, Morey R, Palpant NJ et al (2015) Statistically based splicing detection reveals neural enrichment and tissue-specific induction of circular RNA during human fetal development. Genome Biol 16:126CrossRefGoogle Scholar
  35. 35.
    Chen L, Zhang P, Fan Y et al (2018) Circular RNAs mediated by transposons are associated with transcriptomic and phenotypic variation in maize. New Phytol 217(3):1292–1306CrossRefGoogle Scholar
  36. 36.
    Feracci M, Foot JN, Grellscheid SN et al (2016) Structural basis of RNA recognition and dimerization by the STAR proteins T-STAR and Sam68. Nat Commun 7:10355CrossRefGoogle Scholar
  37. 37.
    Chu Q, Zhang X, Zhu X et al (2017) PlantcircBase: a database for plant circular RNAs. Mol Plant 10(8):1126–1128CrossRefGoogle Scholar
  38. 38.
    Chen L, Yu Y, Zhang X et al (2016) PcircRNA_finder: a software for circRNA prediction in plants. Bioinformatics 32(22):3528–3529PubMedPubMedCentralGoogle Scholar
  39. 39.
    Szabo L, Salzman J (2016) Detecting circular RNAs: bioinformatic and experimental challenges. Nat Rev Genet 17(11):679–692CrossRefGoogle Scholar
  40. 40.
    Hansen TB, Veno MT, Damgaard CK et al (2016) Comparison of circular RNA prediction tools. Nucleic Acids Res 44(6):e58CrossRefGoogle Scholar
  41. 41.
    Westholm JO, Miura P, Olson S et al (2014) Genome-wide analysis of Drosophila circular RNAs reveals their structural and sequence properties and age-dependent neural accumulation. Cell Rep 9(5):1966–1980CrossRefGoogle Scholar
  42. 42.
    Ashwal-Fluss R, Meyer M, Pamudurti NR et al (2014) circRNA biogenesis competes with pre-mRNA splicing. Mol Cell 56(1):55–66CrossRefGoogle Scholar
  43. 43.
    Liang D, Wilusz JE (2014) Short intronic repeat sequences facilitate circular RNA production. Genes Dev 28(20):2233–2247CrossRefGoogle Scholar
  44. 44.
    Barrett SP, Wang PL, Salzman J (2015) Circular RNA biogenesis can proceed through an exon-containing lariat precursor. Elife 4:e07540CrossRefGoogle Scholar
  45. 45.
    Rybak-Wolf A, Stottmeister C, Glazar P et al (2015) Circular RNAs in the mammalian brain are highly abundant, conserved, and dynamically expressed. Mol Cell 58(5):870–885CrossRefGoogle Scholar
  46. 46.
    Errichelli L, Dini Modigliani S, Laneve P et al (2017) FUS affects circular RNA expression in murine embryonic stem cell-derived motor neurons. Nat Commun 8:14741CrossRefGoogle Scholar
  47. 47.
    Aktas T, Avsar Ilik I, Maticzka D et al (2017) DHX9 suppresses RNA processing defects originating from the Alu invasion of the human genome. Nature 544(7648):115–119CrossRefGoogle Scholar
  48. 48.
    Foot JN, Feracci M, Dominguez C (2014) Screening protein--single stranded RNA complexes by NMR spectroscopy for structure determination. Methods 65(3):288–301CrossRefGoogle Scholar
  49. 49.
    Teplova M, Hafner M, Teplov D et al (2013) Structure-function studies of STAR family quaking proteins bound to their in vivo RNA target sites. Genes Dev 27(8):928–940CrossRefGoogle Scholar
  50. 50.
    Ryder SP, Williamson JR (2004) Specificity of the STAR/GSG domain protein Qk1: implications for the regulation of myelination. RNA 10(9):1449–1458CrossRefGoogle Scholar
  51. 51.
    Ryder SP, Frater LA, Abramovitz DL et al (2004) RNA target specificity of the STAR/GSG domain post-transcriptional regulatory protein GLD-1. Nat Struct Mol Biol 11(1):20–28CrossRefGoogle Scholar
  52. 52.
    Hall MP, Nagel RJ, Fagg WS et al (2013) Quaking and PTB control overlapping splicing regulatory networks during muscle cell differentiation. RNA 19(5):627–638CrossRefGoogle Scholar
  53. 53.
    Cheng Y, Kato N, Wang W et al (2003) Two RNA binding proteins, HEN4 and HUA1, act in the processing of AGAMOUS pre-mRNA in Arabidopsis thaliana. Dev Cell 4(1):53–66CrossRefGoogle Scholar
  54. 54.
    Mockler TC, Yu X, Shalitin D et al (2004) Regulation of flowering time in Arabidopsis by K homology domain proteins. Proc Natl Acad Sci USA 101(34):12759–12764CrossRefGoogle Scholar
  55. 55.
    Rodriguez-Cazorla E, Ripoll JJ, Andujar A et al (2015) K-homology nuclear ribonucleoproteins regulate floral organ identity and determinacy in Arabidopsis. PLoS Genet 11(2):e1004983CrossRefGoogle Scholar
  56. 56.
    Jiang J, Wang B, Shen Y et al (2013) The Arabidopsis RNA binding protein with K homology motifs, SHINY1, interacts with the C-terminal domain phosphatase-like 1 (CPL1) to repress stress-inducible gene expression. PLoS Genet 9(7):e1003625CrossRefGoogle Scholar
  57. 57.
    Guan Q, Wen C, Zeng H et al (2013) A KH domain-containing putative RNA-binding protein is critical for heat stress-responsive gene regulation and thermotolerance in Arabidopsis. Mol Plant 6(2):386–395CrossRefGoogle Scholar
  58. 58.
    Jeong IS, Fukudome A, Aksoy E et al (2013) Regulation of abiotic stress signalling by Arabidopsis C-terminal domain phosphatase-like 1 requires interaction with a k-homology domain-containing protein. PLoS One 8(11):e80509CrossRefGoogle Scholar
  59. 59.
    Thatcher LF, Kamphuis LG, Hane JK et al (2015) The Arabidopsis KH-domain RNA-binding protein ESR1 functions in components of Jasmonate Signalling, unlinking growth restraint and resistance to stress. PLoS One 10(5):e0126978CrossRefGoogle Scholar
  60. 60.
    Lorkovic ZJ, Barta A (2002) Genome analysis: RNA recognition motif (RRM) and K homology (KH) domain RNA-binding proteins from the flowering plant Arabidopsis thaliana. Nucleic Acids Res 30(3):623–635CrossRefGoogle Scholar
  61. 61.
    Du WW, Yang W, Liu E et al (2016) Foxo3 circular RNA retards cell cycle progression via forming ternary complexes with p21 and CDK2. Nucleic Acids Res 44(6):2846–2858CrossRefGoogle Scholar
  62. 62.
    Zheng QP, Bao CY, Guo WJ et al (2016) Circular RNA profiling reveals an abundant circHIPK3 that regulates cell growth by sponging multiple miRNAs. Nat Commun 7:11215CrossRefGoogle Scholar
  63. 63.
    Hsiao KY, Lin YC, Gupta SK et al (2017) Noncoding effects of circular RNA CCDC66 promote Colon Cancer growth and metastasis. Cancer Res 77(9):2339–2350CrossRefGoogle Scholar
  64. 64.
    Liu T, Zhang L, Chen G et al (2017) Identifying and characterizing the circular RNAs during the lifespan of Arabidopsis leaves. Front Plant Sci 8:1278CrossRefGoogle Scholar
  65. 65.
    Mendes ND, Freitas AT, Sagot MF (2009) Current tools for the identification of miRNA genes and their targets. Nucleic Acids Res 37(8):2419–2433CrossRefGoogle Scholar
  66. 66.
    Wang XJ, Reyes JL, Chua NH et al (2004) Prediction and identification of Arabidopsis thaliana microRNAs and their mRNA targets. Genome Biol 5(9):R65CrossRefGoogle Scholar
  67. 67.
    Bulow L, Bolivar JC, Ruhe J et al (2012) ‘MicroRNA Targets’, a new AthaMap web-tool for genome-wide identification of miRNA targets in Arabidopsis thaliana. BioData Min 5(1):7CrossRefGoogle Scholar
  68. 68.
    Bonnet E, He Y, Billiau K et al (2010) TAPIR, a web server for the prediction of plant microRNA targets, including target mimics. Bioinformatics 26(12):1566–1568CrossRefGoogle Scholar
  69. 69.
    Srivastava PK, Moturu TR, Pandey P et al (2014) A comparison of performance of plant miRNA target prediction tools and the characterization of features for genome-wide target prediction. BMC Genomics 15:348CrossRefGoogle Scholar
  70. 70.
    Chi SW, Zang JB, Mele A et al (2009) Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature 460(7254):479–486CrossRefGoogle Scholar
  71. 71.
    Suzuki N, Rivero RM, Shulaev V et al (2014) Abiotic and biotic stress combinations. New Phytol 203(1):32–43CrossRefGoogle Scholar
  72. 72.
    Phillips JR, Dalmay T, Bartels D (2007) The role of small RNAs in abiotic stress. FEBS Lett 581(19):3592–3597CrossRefGoogle Scholar
  73. 73.
    Khraiwesh B, Zhu JK, Zhu J (2012) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim Biophys Acta 1819(2):137–148CrossRefGoogle Scholar
  74. 74.
    Wang YX, Yang M, Wei SM et al (2017) Identification of circular RNAs and their targets in leaves of Triticum aestivum L under dehydration stress. Front Plant Sci 7:2024PubMedPubMedCentralGoogle Scholar
  75. 75.
    Conn VM, Hugouvieux V, Nayak A et al (2017) A circRNA from SEPALLATA3 regulates splicing of its cognate mRNA through R-loop formation. Nat Plants 3(5):17053CrossRefGoogle Scholar
  76. 76.
    Chen Y, Li C, Tan C et al (2016) Circular RNAs: a new frontier in the study of human diseases. J Med Genet 53(6):359–365CrossRefGoogle Scholar
  77. 77.
    Huang S, Yang B, Chen BJ et al (2017) The emerging role of circular RNAs in transcriptome regulation. Genomics 109(5–6):401–407CrossRefGoogle Scholar
  78. 78.
    Meng S, Zhou H, Feng Z et al (2017) CircRNA: functions and properties of a novel potential biomarker for cancer. Mol Cancer 16(1):94CrossRefGoogle Scholar
  79. 79.
    Han YN, Xia SQ, Zhang YY et al (2017) Circular RNAs: a novel type of biomarker and genetic tools in cancer. Oncotarget 8(38):64551–64563PubMedPubMedCentralGoogle Scholar
  80. 80.
    Zhang HD, Jiang LH, Sun DW et al (2018) CircRNA: a novel type of biomarker for cancer. Breast Cancer 25(1):1–7CrossRefGoogle Scholar
  81. 81.
    Huang YS, Jie N, Zou KJ et al (2017) Expression profile of circular RNAs in human gastric cancer tissues. Mol Med Rep 16(3):2469–2476CrossRefGoogle Scholar
  82. 82.
    Lu LS, Sun J, Shi PY et al (2017) Identification of circular RNAs as a promising new class of diagnostic biomarkers for human breast cancer. Oncotarget 8(27):44096–44107PubMedPubMedCentralGoogle Scholar
  83. 83.
    Shao Y, Li J, Lu R et al (2017) Global circular RNA expression profile of human gastric cancer and its clinical significance. Cancer Med 6(6):1173–1180CrossRefGoogle Scholar
  84. 84.
    Zhu X, Wang X, Wei S et al (2017) hsa_circ_0013958: a circular RNA and potential novel biomarker for lung adenocarcinoma. FEBS J 284(14):2170–2182CrossRefGoogle Scholar
  85. 85.
    Yang XS, Wu J, Ziegler TE et al (2011) Gene expression biomarkers provide sensitive indicators of in planta nitrogen status in maize. Plant Physiol 157(4):1841–1852CrossRefGoogle Scholar
  86. 86.
    Yan X, Gurtler J, Fratamico P et al (2011) Comprehensive approaches to molecular biomarker discovery for detection and identification of Cronobacter spp. (Enterobacter sakazakii) and Salmonella spp. Appl Environ Microbiol 77(5):1833–1843CrossRefGoogle Scholar
  87. 87.
    Steinfath M, Strehmel N, Peters R et al (2010) Discovering plant metabolic biomarkers for phenotype prediction using an untargeted approach. Plant Biotechnol J 8(8):900–911CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  1. 1.Laboratoire de Physiologie Cellulaire et Végétale, CNRS Univ. Grenoble Alpes, CEA, INRA, BIG GrenobleGrenobleFrance
  2. 2.Institute of Plant Sciences Paris-Saclay, IPS2, CNRS-INRA-University of Paris Sud, Paris-Diderot and EvryUniversity of Paris SaclayGif sur YvetteFrance
  3. 3.Flinders Centre for Innovation in CancerCollege of Medicine & Public Health, Flinders UniversityBedford ParkAustralia

Personalised recommendations