Abstract
Main conclusion
Comprehensive transcriptome profiling uncovers extensive intraspecific variation of circular RNAs in maize, shedding light on genomic and phenotypic variation among maize inbred lines.
Circular RNAs (circRNAs) are single-strand, covalently closed transcripts. A substantial number of circRNAs have been identified and shown to be associated with phenotypic variation in various species. However, little is known about the intraspecific variation of circRNAs in maize (Zea mays L.). Here, we collected a large transcriptomic dataset (by circRNA-seq and mRNA-seq) from seedling leaves of the reference maize inbred lines B73 and Mo17. We identified over 1500 circRNAs in these lines using two circRNA detection methods, CIRCexplorer2 and CIRI. Notably, a substantial proportion of circRNAs varied in terms of sequence or expression level between lines, pointing to extensive intraspecific variation of circRNAs in maize. GO and KEGG analyses showed that genes producing circRNAs with intraspecific variation were more likely to be enriched in multiple functional groups, compared with those that did not produce circRNAs. These findings suggest that circRNAs could be utilized as an indicator of genomic and phenotypic variation among maize inbred lines. Ribosomal profiling revealed that several circRNAs might have translational capacity in maize. These results uncover the extensive intraspecific variation of circRNAs and pave the way for further understanding the molecular mechanisms underlying phenotypic variation at the circRNA level in maize.
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References
Arabidopsis Genome I (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408(6814):796–815. https://doi.org/10.1038/35048692
Ashwal-Fluss R, Meyer M, Pamudurti NR, 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(1):55–66. https://doi.org/10.1016/j.molcel.2014.08.019
Bruce AB (1910) The Mendelian theory of heredity and the augmentation of vigor. Science 32(827):627–628. https://doi.org/10.1126/science.32.827.627-a
Burd CE, Jeck WR, Liu Y, Sanoff HK, Wang Z, Sharpless NE (2010) Expression of linear and novel circular forms of an INK4/ARF-associated non-coding RNA correlates with atherosclerosis risk. PLoS Genet 6(12):e1001233. https://doi.org/10.1371/journal.pgen.1001233
Burt AJ, Grainger CM, Shelp BJ, Lee EA (2011) Heterosis for carotenoid concentration and profile in maize hybrids. Genome 54(12):993–1004. https://doi.org/10.1139/g11-066
Chen CY, Sarnow P (1995) Initiation of protein synthesis by the eukaryotic translational apparatus on circular RNAs. Science 268(5209):415–417
Chen G, Cui J, Wang L, Zhu Y, Lu Z, Jin B (2017) Genome-wide identification of circular RNAs in Arabidopsis thaliana. Front Plant Sci 8:1678. https://doi.org/10.3389/fpls.2017.01678
Chen L, Zhang P, Fan Y, Lu Q, Li Q, Yan J, Muehlbauer GJ, Schnable PS, Dai M, Li L (2018) Circular RNAs mediated by transposons are associated with transcriptomic and phenotypic variation in maize. New Phytol 217(3):1292–1306. https://doi.org/10.1111/nph.14901
Chu Q, Zhang X, Zhu X, Liu C, Mao L, Ye C, Zhu QH, Fan L (2017) PlantcircBase: a database for plant circular RNAs. Mol Plant 10(8):1126–1128. https://doi.org/10.1016/j.molp.2017.03.003
Chu Q, Bai P, Zhu X, Zhang X, Mao L, Zhu QH, Fan L, Ye CY (2018) Characteristics of plant circular RNAs. Brief Bioinform. https://doi.org/10.1093/bib/bby111
Davenport CB (1908) Degeneration, albinism and inbreeding. Science 28(718):454–455. https://doi.org/10.1126/science.28.718.454-b
Fu H, Dooner HK (2002) Intraspecific violation of genetic colinearity and its implications in maize. Proc Natl Acad Sci USA 99(14):9573–9578. https://doi.org/10.1073/pnas.132259199
Gao Y, Wang J, Zhao F (2015) CIRI: an efficient and unbiased algorithm for de novo circular RNA identification. Genome Biol 16:4. https://doi.org/10.1186/s13059-014-0571-3
Garcia AA, Wang S, Melchinger AE, Zeng ZB (2008) Quantitative trait loci mapping and the genetic basis of heterosis in maize and rice. Genetics 180(3):1707–1724. https://doi.org/10.1534/genetics.107.082867
Guo B, Chen Y, Li C, Wang T, Wang R, Wang B, Hu S, Du X, Xing H, Song X, Yao Y, Sun Q, Ni Z (2014) Maize (Zea mays L.) seedling leaf nuclear proteome and differentially expressed proteins between a hybrid and its parental lines. Proteomics 14(9):1071–1087. https://doi.org/10.1002/pmic.201300147
Hansen KD, Wu Z, Irizarry RA, Leek JT (2011a) Sequencing technology does not eliminate biological variability. Nat Biotechnol 29(7):572–573. https://doi.org/10.1038/nbt.1910
Hansen TB, Wiklund ED, Bramsen JB, Villadsen SB, Statham AL, Clark SJ, Kjems J (2011b) miRNA-dependent gene silencing involving Ago2-mediated cleavage of a circular antisense RNA. EMBO J 30(21):4414–4422. https://doi.org/10.1038/emboj.2011.359
Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B, Damgaard CK, Kjems J (2013) Natural RNA circles function as efficient microRNA sponges. Nature 495(7441):384–388. https://doi.org/10.1038/nature11993
Hansen TB, Veno MT, Damgaard CK, Kjems J (2016) Comparison of circular RNA prediction tools. Nucleic Acids Res 44(6):e58. https://doi.org/10.1093/nar/gkv1458
International Rice Genome Sequencing P (2005) The map-based sequence of the rice genome. Nature 436(7052):793–800. https://doi.org/10.1038/nature03895
Jeck WR, Sorrentino JA, Wang K, Slevin MK, Burd CE, Liu J, Marzluff WF, Sharpless NE (2013) Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA 19(2):141–157. https://doi.org/10.1261/rna.035667.112
Jiao Y, Peluso P, Shi J, Liang T, Stitzer MC, Wang B, Campbell MS, Stein JC, Wei X, Chin CS, Guill K, Regulski M, Kumari S, Olson A, Gent J, Schneider KL, Wolfgruber TK, May MR, Springer NM, Antoniou E, McCombie WR, Presting GG, McMullen M, Ross-Ibarra J, Dawe RK, Hastie A, Rank DR, Ware D (2017) Improved maize reference genome with single-molecule technologies. Nature 546(7659):524–527. https://doi.org/10.1038/nature22971
Kaeppler S (2012) Heterosis: many genes, many mechanisms—end the search for an undiscovered unifying theory. ISRN Bot 2012:1–12. https://doi.org/10.5402/2012/682824
Lai J, Li R, Xu X, Jin W, Xu M, Zhao H, Xiang Z, Song W, Ying K, Zhang M, Jiao Y, Ni P, Zhang J, Li D, Guo X, Ye K, Jian M, Wang B, Zheng H, Liang H, Zhang X, Wang S, Chen S, Li J, Fu Y, Springer NM, Yang H, Wang J, Dai J, Schnable PS, Wang J (2010) Genome-wide patterns of genetic variation among elite maize inbred lines. Nat Genet 42(11):1027–1030. https://doi.org/10.1038/ng.684
Lei L, Shi J, Chen J, Zhang M, Sun S, Xie S, Li X, Zeng B, Peng L, Hauck A, Zhao H, Song W, Fan Z, Lai J (2015) Ribosome profiling reveals dynamic translational landscape in maize seedlings under drought stress. Plant J 84(6):1206–1218. https://doi.org/10.1111/tpj.13073
Lisch D (2009) Epigenetic regulation of transposable elements in plants. Annu Rev Plant Biol 60:43–66. https://doi.org/10.1146/annurev.arplant.59.032607.092744
Lisch D (2013) How important are transposons for plant evolution? Nat Rev Genet 14(1):49–61. https://doi.org/10.1038/nrg3374
Lu T, Cui L, Zhou Y, Zhu C, Fan D, Gong H, Zhao Q, Zhou C, Zhao Y, Lu D, Luo J, Wang Y, Tian Q, Feng Q, Huang T, Han B (2015) Transcriptome-wide investigation of circular RNAs in rice. RNA 21(12):2076–2087. https://doi.org/10.1261/rna.052282.115
Memczak S, Jens M, Elefsinioti A, Torti F, Krueger J, Rybak A, Maier L, Mackowiak SD, Gregersen LH, Munschauer M, Loewer A, Ziebold U, Landthaler M, Kocks C, le Noble F, Rajewsky N (2013) Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 495(7441):333–338. https://doi.org/10.1038/nature11928
Schnable PS, Springer NM (2013) Progress toward understanding heterosis in crop plants. Annu Rev Plant Biol 64:71–88. https://doi.org/10.1146/annurev-arplant-042110-103827
Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA, Minx P, Reily AD, Courtney L, Kruchowski SS, Tomlinson C, Strong C, Delehaunty K, Fronick C, Courtney B, Rock SM, Belter E, Du F, Kim K, Abbott RM, Cotton M, Levy A, Marchetto P, Ochoa K, Jackson SM, Gillam B, Chen W, Yan L, Higginbotham J, Cardenas M, Waligorski J, Applebaum E, Phelps L, Falcone J, Kanchi K, Thane T, Scimone A, Thane N, Henke J, Wang T, Ruppert J, Shah N, Rotter K, Hodges J, Ingenthron E, Cordes M, Kohlberg S, Sgro J, Delgado B, Mead K, Chinwalla A, Leonard S, Crouse K, Collura K, Kudrna D, Currie J, He R, Angelova A, Rajasekar S, Mueller T, Lomeli R, Scara G, Ko A, Delaney K, Wissotski M, Lopez G, Campos D, Braidotti M, Ashley E, Golser W, Kim H, Lee S, Lin J, Dujmic Z, Kim W, Talag J, Zuccolo A, Fan C, Sebastian A, Kramer M, Spiegel L, Nascimento L, Zutavern T, Miller B, Ambroise C, Muller S, Spooner W, Narechania A, Ren L, Wei S, Kumari S, Faga B, Levy MJ, McMahan L, Van Buren P, Vaughn MW, Ying K, Yeh CT, Emrich SJ, Jia Y, Kalyanaraman A, Hsia AP, Barbazuk WB, Baucom RS, Brutnell TP, Carpita NC, Chaparro C, Chia JM, Deragon JM, Estill JC, Fu Y, Jeddeloh JA, Han Y, Lee H, Li P, Lisch DR, Liu S, Liu Z, Nagel DH, McCann MC, SanMiguel P, Myers AM, Nettleton D, Nguyen J, Penning BW, Ponnala L, Schneider KL, Schwartz DC, Sharma A, Soderlund C, Springer NM, Sun Q, Wang H, Waterman M, Westerman R, Wolfgruber TK, Yang L, Yu Y, Zhang L, Zhou S, Zhu Q, Bennetzen JL, Dawe RK, Jiang J, Jiang N, Presting GG, Wessler SR, Aluru S, Martienssen RA, Clifton SW, McCombie WR, Wing RA, Wilson RK (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326(5956):1112–1115. https://doi.org/10.1126/science.1178534
Springer NM, Stupar RM (2007) Allelic variation and heterosis in maize: how do two halves make more than a whole? Genome Res 17(3):264–275. https://doi.org/10.1101/gr.5347007
Springer NM, Ying K, Fu Y, Ji T, Yeh CT, Jia Y, Wu W, Richmond T, Kitzman J, Rosenbaum H, Iniguez AL, Barbazuk WB, Jeddeloh JA, Nettleton D, Schnable PS (2009) Maize inbreds exhibit high levels of copy number variation (CNV) and presence/absence variation (PAV) in genome content. PLoS Genet 5(11):e1000734. https://doi.org/10.1371/journal.pgen.1000734
Stuber CW, Lincoln SE, Wolff DW, Helentjaris T, Lander ES (1992) Identification of genetic factors contributing to heterosis in a hybrid from two elite maize inbred lines using molecular markers. Genetics 132(3):823–839
Sun S, Zhou Y, Chen J, Shi J, Zhao H, Zhao H, Song W, Zhang M, Cui Y, Dong X, Liu H, Ma X, Jiao Y, Wang B, Wei X, Stein JC, Glaubitz JC, Lu F, Yu G, Liang C, Fengler K, Li B, Rafalski A, Schnable PS, Ware DH, Buckler ES, Lai J (2018) Extensive intraspecific gene order and gene structural variations between Mo17 and other maize genomes. Nat Genet 50(9):1289–1295. https://doi.org/10.1038/s41588-018-0182-0
Swanson-Wagner RA, Eichten SR, Kumari S, Tiffin P, Stein JC, Ware D, Springer NM (2010) Pervasive gene content variation and copy number variation in maize and its undomesticated progenitor. Genome Res 20(12):1689–1699. https://doi.org/10.1101/gr.109165.110
Szabo L, Salzman J (2016) Detecting circular RNAs: bioinformatic and experimental challenges. Nat Rev Genet 17(11):679–692. https://doi.org/10.1038/nrg.2016.114
Tang J, Yan J, Ma X, Teng W, Wu W, Dai J, Dhillon BS, Melchinger AE, Li J (2010) Dissection of the genetic basis of heterosis in an elite maize hybrid by QTL mapping in an immortalized F2 population. Theor Appl Genet Theoretische und angewandte Genetik 120(2):333–340. https://doi.org/10.1007/s00122-009-1213-0
Tang B, Hao Z, Zhu Y, Zhang H, Li G (2018) Genome-wide identification and functional analysis of circRNAs in Zea mays. PLoS One 13(12):e0202375. https://doi.org/10.1371/journal.pone.0202375
Tong W, Yu J, Hou Y, Li F, Zhou Q, Wei C, Bennetzen JL (2018) Circular RNA architecture and differentiation during leaf bud to young leaf development in tea (Camellia sinensis). Planta 248(6):1417–1429. https://doi.org/10.1007/s00425-018-2983-x
Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28(5):511–515. https://doi.org/10.1038/nbt.1621
Wang PL, Bao Y, Yee MC, Barrett SP, Hogan GJ, Olsen MN, Dinneny JR, Brown PO, Salzman J (2014) Circular RNA is expressed across the eukaryotic tree of life. PloS One. https://doi.org/10.1371/journal.pone.0090859
Wei L, Cao X (2016) The effect of transposable elements on phenotypic variation: insights from plants to humans. Sci China Life Sci 59(1):24–37. https://doi.org/10.1007/s11427-015-4993-2
Westholm JO, Miura P, Olson S, Shenker S, Joseph B, Sanfilippo P, Celniker SE, Graveley BR, Lai EC (2014) Genome-wide analysis of drosophila circular RNAs reveals their structural and sequence properties and age-dependent neural accumulation. Cell Rep 9(5):1966–1980
Xie C, Mao X, Huang J, Ding Y, Wu J, Dong S, Kong L, Gao G, Li CY, Wei L (2011) KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res. https://doi.org/10.1093/nar/gkr483
Yang Y, Gao X, Zhang M, Yan S, Sun C, Xiao F, Huang N, Yang X, Zhao K, Zhou H, Huang S, Xie B, Zhang N (2018) Novel role of FBXW7 circular rna in repressing glioma tumorigenesis. J Natl Cancer Inst. https://doi.org/10.1093/jnci/djx166
Ye CY, Chen L, Liu C, Zhu QH, Fan L (2015) Widespread noncoding circular RNAs in plants. New Phytol 208(1):88–95. https://doi.org/10.1111/nph.13585
Zeng X, Lin W, Guo M, Zou Q (2017) A comprehensive overview and evaluation of circular RNA detection tools. PLoS Comput Biol 13(6):e1005420. https://doi.org/10.1371/journal.pcbi.1005420
Zhang XO, Wang HB, Zhang Y, Lu X, Chen LL, Yang L (2014) Complementary sequence-mediated exon circularization. Cell 159(1):134–147. https://doi.org/10.1016/j.cell.2014.09.001
Zhang XO, Dong R, Zhang Y, Zhang JL, Luo Z, Zhang J, Chen LL, Yang L (2016) Diverse alternative back-splicing and alternative splicing landscape of circular RNAs. Genome Res 26(9):1277–1287. https://doi.org/10.1101/gr.202895.115
Zuo J, Wang Q, Zhu B, Luo Y, Gao L (2016) Deciphering the roles of circRNAs on chilling injury in tomato. Biochem Biophys Res Commun 479(2):132–138. https://doi.org/10.1016/j.bbrc.2016.07.032
Funding
This research was supported by the National Key Research and Development Program of China (2016YFD0100802) and Huazhong Agricultural University Scientific & Technological Self-innovation Foundation (Program No. 2015RC016). The authors declare no conflict of interest.
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Supplementary material 2 Table S1 Summary of circRNA-seq data obtained for B73 and Mo17. Table S2 Detailed information about circRNAs detected in B73 and Mo17. Table S3 Parental gene IDs of circRNAs in B73 and Mo17. Table S4 Overlapped circRNAs in B73 and Mo17. Table S5 Differentially expressed circRNAs in B73 and Mo17. Table S6 qRT-PCR validation of differentially expressed circRNAs in B73 and Mo17. Table S7 Enriched GO terms for the parental genes of B73- and Mo17-specific circRNAs. Table S8 Number of circRNAs with junction sites covered by Ribo-seq data in B73 and Mo17. Table S9 Enriched GO terms for the parental genes of circRNAs with junction sites covered by Ribo-seq data. Table S10 Sequences of validated translatable circRNAs in B73 and Mo17. Table S11 Primer information for the validation of translatable circRNAs and differentially expressed circRNAs (XLSX 263 kb)
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Luo, Z., Han, L., Qian, J. et al. Circular RNAs exhibit extensive intraspecific variation in maize. Planta 250, 69–78 (2019). https://doi.org/10.1007/s00425-019-03145-y
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DOI: https://doi.org/10.1007/s00425-019-03145-y