Genome-wide discovery and characterization of maize long non-coding RNAs

Genome Biology

Volumn 15, Issue 2, 2014, Pages

  Li, Lin ^a   Eichten, Steven R ^a   Shimizu, Rena ^b   Petsch, Katherine ^c   Yeh, Cheng Ting ^d   Wu, Wei ^d,h   Chettoor, Antony M ^e   Givan, Scott A ^f   Cole, Rex A ^g   Fowler, John E ^g   Evans, Matthew M S ^e   Scanlon, Michael J ^b   Yu, Jianming ^d   Schnable, Patrick S ^d   Timmermans, Marja C P ^c   Springer, Nathan M ^a   Muehlbauer, Gary J ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b Department of Plant Biology University of Minnesota ^*  (United States)

^c Simons Center for Quantitative Biology   (United States)

^d IOWA STATE UNIVERSITY   (United States)

^e GEOPHYSICAL LABORATORY   (United States)

^f UNIVERSITY OF MISSOURI   (United States)

^g OREGON STATE UNIVERSITY   (United States)

^h PIONEER HI BRED INTERNATIONAL INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LONG UNTRANSLATED RNA;

ARTICLE; CONTROLLED STUDY; EPIGENETICS; EXON; EXPRESSED SEQUENCE TAG; GENE EXPRESSION; GENOTYPE; INHERITANCE; MAIZE; NONHUMAN; PLANT GENE; PLANT GENOME; QUANTITATIVE TRAIT LOCUS MAPPING; RECOMBINANT INBRED STRAIN; RNA SEQUENCE; SEQUENCE DATABASE; TISSUE DISTRIBUTION; TRANSCRIPTOMICS; GENE FUNCTION; GENE IDENTIFICATION; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOME ANALYSIS; MOLECULAR DYNAMICS; PREDICTION; SEQUENCE ANALYSIS; TISSUE SPECIFICITY; TRANSGENICS; GENE EXPRESSION REGULATION; GENETIC DATABASE; GENETIC TRANSCRIPTION; GENETICS; ISOLATION AND PURIFICATION; MOLECULAR GENETICS; OPEN READING FRAME;

EUKARYOTA; ZEA MAYS;

DATABASES, GENETIC; EXONS; GENE EXPRESSION REGULATION, PLANT; GENOME, PLANT; MOLECULAR SEQUENCE ANNOTATION; OPEN READING FRAMES; RNA, LONG NONCODING; TRANSCRIPTION, GENETIC; ZEA MAYS;

EID: 84899045771     PISSN: None     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2014-15-2-r40     Document Type: Article

References (78)

1. Zhu QH, Wang MB. Molecular functions of long non-coding RNAs in plants. Genes 2012, 3:176-190.
2. Rinn JL, Chang HY. Genome regulation by long noncoding RNAs. Annu Rev Biochem 2012, 81:145-166. 10.1146/annurev-biochem-051410-092902, 3858397, 22663078.
3. Cabili MN, Trapnell C, Goff L, Koziol M, Tazon-Vega B, Regev A, Rinn JL. Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev 2011, 25:1915-1927. 10.1101/gad.17446611, 3185964, 21890647.
4. Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S, Tilgner H, Guernec G, Martin D, Merkel A, Knowles DG, Lagarde J, Veeravalli L, Ruan X, Ruan Y, Lassmann T, Carninci P, Brown JB, Lipovich L, Gonzalez JM, Thomas M, Davis CA, Shiekhattar R, Gingeras TR, Hubbard TJ, Notredame C, Harrow J, Guigó R. The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res 2012, 22:1775-1789. 10.1101/gr.132159.111, 3431493, 22955988.
5. Maeda N, Kasukawa T, Oyama R, Gough J, Frith M, Engström PG, Lenhard B, Aturaliya RN, Batalov S, Beisel KW, Bult CJ, Fletcher CF, Forrest AR, Furuno M, Hill D, Itoh M, Kanamori-Katayama M, Katayama S, Katoh M, Kawashima T, Quackenbush J, Ravasi T, Ring BZ, Shibata K, Sugiura K, Takenaka Y, Teasdale RD, Wells CA, Zhu Y, Kai C, et al. Transcript annotation in FANTOM3: Mouse gene catalog based on physical cDNAs. PLoS Genet 2006, 2:e62. 10.1371/journal.pgen.0020062, 1449903, 16683036.
6. Khachane AN, Harrison PM. Mining mammalian transcript data for functional long non-coding RNAs. PLoS One 2010, 5:e10316. 10.1371/journal.pone.0010316, 2859052, 20428234.
7. Li L, Wang X, Stolc V, Li X, Zhang D, Su N, Tongprasit W, Li S, Cheng Z, Wang J, Deng XW. Genome-wide transcription analyses in rice using tiling microarrays. Nat Genet 2006, 38:124-129. 10.1038/ng1704, 16369532.
8. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 2008, 5:621-628. 10.1038/nmeth.1226, 18516045.
9. Khalil AM, Guttman M, Huarte M, Garber M, Raj A, Rivea Morales D, Thomas K, Presser A, Bernstein BE, van Oudenaarden A, Regev A, Lander ES, Rinn JL. Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc Natl Acad Sci U S A 2009, 106:11667-11672. 10.1073/pnas.0904715106, 2704857, 19571010.
10. Guttman M, Amit I, Garber M, French C, Lin MF, Feldser D, Huarte M, Zuk O, Carey BW, Cassady JP, Cabili MN, Jaenisch R, Mikkelsen TS, Jacks T, Hacohen N, Bernstein BE, Kellis M, Regev A, Rinn JL, Lander ES. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 2009, 458:223-227. 10.1038/nature07672, 2754849, 19182780.
11. Loewer S, Cabili MN, Guttman M, Loh YH, Thomas K, Park IH, Garber M, Curran M, Onder T, Agarwal S, Manos PD, Datta S, Lander ES, Schlaeger TM, Daley GQ, Rinn JL. Large intergenic non-coding RNA-RoR modulates reprogramming of human induced pluripotent stem cells. Nat Genet 2010, 42:1113-1117. 10.1038/ng.710, 3040650, 21057500.
12. Huarte M, Guttman M, Feldser D, Garber M, Koziol MJ, Kenzelmann-Broz D, Khalil AM, Zuk O, Amit I, Rabani M, Attardi LD, Regev A, Lander ES, Jacks T, Rinn JL. A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response. Cell 2010, 142:409-419. 10.1016/j.cell.2010.06.040, 2956184, 20673990.
13. Letswaart R, Wu Z, Dean C. Flowering time control: another window to the connection between antisense RNA and chromatin. Trends Genet 2012, 28:445-453. 10.1016/j.tig.2012.06.002, 22785023.
14. Wapinski O, Chang HY. Long noncoding RNAs and human disease. Trends Cell Biol 2011, 21:354-361. 10.1016/j.tcb.2011.04.001, 21550244.
15. Swiezewski S, Liu F, Magusin A, Dean C. Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nature 2009, 462:799-802. 10.1038/nature08618, 20010688.
16. Heo JB, Sung S. Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 2010, 331:76-79.
17. Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI, Rubio-Somoza I, Leyva A, Weigel D, García JA, Paz-Ares J. Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 2007, 39:1033-1037. 10.1038/ng2079, 17643101.
18. Rymarquis LA, Kastenmayer JP, Huttenhofer AG, Green P. Diamonds in the rough: mRNA-like non-coding RNAs. Trends Plant Sci 2008, 13:329-334. 10.1016/j.tplants.2008.02.009, 18448381.
19. Campalans A, Kondorosi A, Crespi M. Enod40, a short open reading frame-containing mRNA, induces cytoplasmic localization of a nuclear RNA binding protein in Medicago truncatula. Plant Cell 2004, 16:1047-1059. 10.1105/tpc.019406, 412876, 15037734.
20. Gultyaev AP, Roussis A. Identification of conserved secondary structures and expansion segments in enod40 RNAs reveals new enod40 homologues in plants. Nucleic Acids Res 2007, 35:3144-3152. 10.1093/nar/gkm173, 1888808, 17452360.
21. MacIntosh GC, Wilkerson C, Green PJ. Identification and analysis of Arabidopsis expressed sequence tags characteristic of non-coding RNAs. Plant Physiol 2001, 127:765-776. 10.1104/pp.010501, 129250, 11706161.
22. Marker C, Zemann A, Terhörst T, Kiefmann M, Kastenmayer JP, Green P, Bachellerie JP, Brosius J, Hüttenhofer A. Experimental RNomics: Identification of 140 candidates for small non-messenger RNAs in the plant Arabidopsis thaliana. Curr Biol 2002, 12:2002-2013. 10.1016/S0960-9822(02)01304-0, 12477388.
23. Hirsch J, Lefort V, Vankersschaver M, Boualem A, Lucas A, Thermes C, d'Aubenton-Carafa Y, Crespi M. Characterization of 43 non-protein-coding mRNA genes in Arabidopsis, including the MIR162a-derived transcripts. Plant Physiol 2006, 140:1192-1204. 10.1104/pp.105.073817, 1435803, 16500993.
24. Matsui A, Ishida J, Morosawa T, Mochizuki Y, Kaminuma E, Endo TA, Okamoto M, Nambara E, Nakajima M, Kawashima M, Satou M, Kim JM, Kobayashi N, Toyoda T, Shinozaki K, Seki M. Arabidopsis transcriptome analysis under drought, cold, high-salinity and ABA treatment conditions using a tiling array. Plant Cell Physiol 2008, 49:1135-1149. 10.1093/pcp/pcn101, 18625610.
25. Ben Amor B, Wirth S, Merchan F, Laporte P, d'Aubenton-Carafa Y, Hirsch J, Maizel A, Mallory A, Lucas A, Deragon JM, Vaucheret H, Thermes C, Crespi M. Novel long non-protein coding RNAs involved in Arabidopsis differentiation and stress responses. Genome Res 2009, 19:57-69. 2612962, 18997003.
26. Song D, Yang Y, Yu B, Zheng B, Deng Z, Lu BL, Chen X, Jiang T. Computational prediction of novel non-coding RNAs in Arabidopsis thaliana. BMC Bioinforma 2009, 10:S36.
27. Liu J, Jung C, Xu J, Wang H, Deng S, Bernad L, Arenas-Huertero C, Chua NH. Genome-wide analysis uncovers regulation of long intergenic noncoding RNAs in Arabidopsis. Plant Cell 2012, 24:4333-4345. 10.1105/tpc.112.102855, 3531837, 23136377.
28. Wen J, Parker BJ, Weiller GF. In silico identification and characterization of mRNA-like noncoding transcripts in Medicago truncatula. In Silico Biol 2007, 7:485-505.
29. Zhang Y, Liu J, Jia C, Li T, Wu R, Wang J, Chen Y, Zou X, Chen R, Wang XJ, Zhu D. Systematic identification and evolutionary features of rhesus monkey small nucleolar RNAs. BMC Genomics 2010, 11:61. 10.1186/1471-2164-11-61, 2832892, 20100322.
30. Boerner S, McGinnis KM. Computational identification and functional predictions of long noncoding RNA in Zea mays. PLoS One 2012, 7:e43047. 10.1371/journal.pone.0043047, 3420876, 22916204.
31. Li L, Petsch K, Shimizu R, Liu S, Xu WW, Ying K, Yu J, Scanlon MJ, Schnable PS, Timmermans MC, Springer NM, Muehlbauer GJ. Mendelian and non-Mendelian regulation of gene expression in maize. PLoS Genet 2013, 9:e1003202. 10.1371/journal.pgen.1003202, 3547793, 23341782.
32. 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, et al. The B73 maize genome: complexity, diversity, and dynamics. Science 2009, 326:1112-1115. 10.1126/science.1178534, 19965430.
33. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 2009, 25:1105-1111. 10.1093/bioinformatics/btp120, 2672628, 19289445.
34. Li P, Ponnala L, Gandotra N, Wang L, Si Y, Tausta SL, Kebrom TH, Provart N, Patel R, Myers CR, Reidel EJ, Turgeon R, Liu P, Sun Q, Nelson T, Brutnell TP. The developmental dynamics of the maize leaf transcriptome. Nat Genet 2010, 42:1060-1067. 10.1038/ng.703, 21037569.
35. Davidson RM, Hansey CN, Gowda M, Childs KL, Lin H, Vaillancourt B, Sekhon RS, de Leon N, Kaeppler SM, Jiang N, Buell CR. Utility of RNA sequencing for analysis of maize reproductive transcriptomes. Plant Genome 2011, 4:191-203.
36. Chang YM, Liu WY, Shih AC, Shen MN, Lu CH, Lu MY, Yang HW, Wang TY, Chen SC, Chen SM, Li WH, Ku MS. Characterizing regulatory and functional differentiation between maize mesophyll and bundle sheath cells by transcriptomic analysis. Plant Physiol 2012, 160:165-177. 10.1104/pp.112.203810, 3440195, 22829318.
37. Bolduc N, Yilmaz A, Mejia-Guerra MK, Morohashi K, O'Connor D, Grotewold E, Hake S. Unraveling the KNOTTED1 regulatory network in maize meristems. Genes Dev 2012, 26:1685-1690. 10.1101/gad.193433.112, 3418586, 22855831.
38. Paschold A, Jia Y, Marcon C, Lund S, Larson NB, Yeh CT, Ossowski S, Lanz C, Nettleton D, Schnable PS, Hochholdinger F. Complementation contributes to transcriptome complexity in maize (Zea mays L.) hybrids relative to their inbred parents. Genome Res 2012, 22:2445-2454. 10.1101/gr.138461.112, 3514674, 23086286.
39. Waters AJ, Makarevitch I, Eichten SR, Swanson-Wagner RA, Yeh CT, Xu W, Schnable PS, Vaughn MW, Gehring M, Springer NM. Parent-of-origin effects on gene expression and DNA methylation in the maize endosperm. Plant Cell 2011, 23:4221-4233. 10.1105/tpc.111.092668, 3269861, 22198147.
40. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 2010, 28:511-515. 10.1038/nbt.1621, 3146043, 20436464.
41. Kong L, Zhang Y, Ye ZQ, Liu XQ, Zhao SQ, Wei L, Gao G. CPC: assess the protein-coding potential of transcripts using sequence features and support vector machine. Nucleic Acids Res 2007, 35:W345-W349. 10.1093/nar/gkm391, 1933232, 17631615.
42. Kapusta A, Kronenberg Z, Lynch VJ, Zhuo X, Ramsay L, Bourque G, Yandell M, Feschotte C. Transposable elements are major contributors to the origin, diversification, and regulation of vertebrate long noncoding RNAs. PLoS Genet 2013, 9:e1003470. 10.1371/journal.pgen.1003470, 3636048, 23637635.
43. Eichten SR, Ellis NA, Makarevitch I, Yeh CT, Gent JI, Guo L, McGinnis KM, Zhang X, Schnable PS, Vaughn MW, Dawe RK, Springer NM. Spreading of heterochromatin is limited to specific families of maize retrotransposons. PLoS Genet 2012, 8:e1003127. 10.1371/journal.pgen.1003127, 3521669, 23271981.
44. Zilberman D, Gehring M, Tran RK, Ballinger T, Henikoff S. Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet 2007, 39:61-69. 10.1038/ng1929, 17128275.
45. Schug J, Schuller WP, Kappen C, Salbaum JM, Bucan M, Stoeckert CJ. Promoter features related to tissue specificity as measured by Shannon entropy. Genome Biol 2005, 6:R33. 10.1186/gb-2005-6-4-r33, 1088961, 15833120.
46. Makarevitch I, Eichten SR, Briskine R, Waters AJ, Danilevskaya ON, Meeley RB, Myers CL, Vaughn MW, Springer NM. Genomic distribution of maize facultative heterochromatin marked by trimethylation of H3K27. Plant Cell 2013, 25:780-793. 10.1105/tpc.112.106427, 3634688, 23463775.
47. Kliebenstein D. Quantitative genomics: analyzing intraspecific variation using global gene expression polymorphisms or eQTLs. Annu Rev Plant Biol 2009, 60:93-114. 10.1146/annurev.arplant.043008.092114, 19012536.
48. Stam M, Belele C, Ramakrishna W, Dorweiler JE, Bennetzen JL, Chandler VL. The regulatory regions required for B' paramutation and expression are located far upstream of the maize b1 transcribed sequences. Genetics 2002, 162:917-930. 1462281, 12399399.
49. Arteaga-Vazquez M, Sidorenko L, Rabanal FA, Shrivistava R, Nobuta K, Green PJ, Meyers BC, Chandler VL. RNA-mediated trans-communication can establish paramutation at the b1 locus in maize. Proc Natl Acad Sci USA 2010, 107:12986-12991. 10.1073/pnas.1007972107, 2919911, 20616013.
50. Alleman M, Sidorenko L, McGinnis K, Seshadri V, Dorweiler JE, White J, Sikkink K, Chandler VL. An RNA-dependent RNA polymerase is required for paramutation in maize. Nature 2006, 442:295-298. 10.1038/nature04884, 16855589.
51. Sidorenko L, Dorweiler JE, Cigan AM, Arteaga-Vazquez M, Vyas M, Kermicle J, Jurcin D, Brzeski J, Cai Y, Chandler VL. A dominant mutation in mediator of paramutation2, one of three second-largest subunits of a plant-specific RNA polymerase, disrupts multiple siRNA silencing processes. PLoS Genet 2009, 5:e1000725. 10.1371/journal.pgen.1000725, 2774164, 19936058.
52. Salvi S, Sponza G, Morgante M, Tomes D, Niu X, Fengler KA, Meeley R, Ananiev EV, Svitashev S, Bruggemann E, Li B, Hainey CF, Radovic S, Zaina G, Rafalski JA, Tingey SV, Miao GH, Phillips RL, Tuberosa R. Conserved noncoding genomic sequences associated with a flowering-time quantitative trait locus in maize. Proc Natl Acad Sci U S A 2007, 104:11376-11381. 10.1073/pnas.0704145104, 2040906, 17595297.
53. Doebley J, Stec A, Gustus C. Teosinte branched1 and the origin of maize: evidence for epistasis and the evolution of dominance. Genetics 1995, 141:333-346. 1206731, 8536981.
54. Clark RM, Wagler TN, Quijada P, Doebley J. A distant upstream enhancer at the maize domestication gene tb1 has pleiotropic effects on plant and inflorescent architecture. Nat Genet 2006, 38:594-597. 10.1038/ng1784, 16642024.
55. Studer AJ, Doebley JF. Do large effect QTL fractionate? A case study at the maize domestication QTL teosinte branched1. Genetics 2011, 188:673-681. 10.1534/genetics.111.126508, 3176526, 21515578.
56. Carles CC, Fletcher JC. Shoot apical meristem maintenance: the art of a dynamic balance. Trends Plant Sci 2003, 8:394-401. 10.1016/S1360-1385(03)00164-X, 12927973.
57. Takacs EM, Li J, Du C, Ponnala L, Janick-Buckner D, Yu J, Muehlbauer GJ, Schnable PS, Timmermans MC, Sun Q, Nettleton D, Scanlon MJ. Ontogeny of the maize shoot apical meristem. Plant Cell 2012, 24:3219-3234. 10.1105/tpc.112.099614, 3462627, 22911570.
58. Berretta J, Morillon A. Pervasive transcription constitutes a new level of eukaryotic genome regulation. EMBO Rep 2009, 10:973-982. 10.1038/embor.2009.181, 2750061, 19680288.
59. Dinger ME, Amaral PP, Mercer TR, Mattick JS. Pervasive transcription of the eukaryotic genome: functional indices and conceptual implications. Brief Funct Genomic Proteomic 2009, 8:407-423. 10.1093/bfgp/elp038, 19770204.
60. Ghildiyal M, Zamore PD. Small silencing RNAs: an expanding universe. Nat Rev Genet 2009, 10:94-108. 10.1038/nrg2504, 2724769, 19148191.
61. Sekhon RS, Briskine R, Hirsch CN, Myers CL, Springer NM, Buell CR, de Leon N, Kaeppler SM. Maize gene atlas developed by RNA sequencing and comparative evaluation of transcriptomes based on RNA sequencing and microarrays. PLoS One 2013, 23:e61005.
62. Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, Goodnough LH, Helms JA, Farnham PJ, Segal E, Chang HY. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 2007, 129:1311-1323. 10.1016/j.cell.2007.05.022, 2084369, 17604720.
63. Duret L, Chureau C, Samain S, Weissenbach J, Avner P. The Xist RNA gene evolved in eutherians by pseudogenization of a protein-coding gene. Science 2006, 312:1653-1655. 10.1126/science.1126316, 16778056.
64. Kanduri C. Kcnq1ot1: a chromatin regulatory RNA. Semin Cell Dev Biol 2011, 22:343-350. 10.1016/j.semcdb.2011.02.020, 21345374.
65. The sequence read archive. [http://www.ncbi.nlm.nih.gov/Traces/sra/].
66. GenBank. [http://www.ncbi.nlm.nih.gov/genbank/].
67. Frith MC, Forrest AR, Nourbakhsh E, Pang KC, Kai C, Kawai J, Carninci P, Hayashizaki Y, Bailey TL, Grimmond SM. The abundance of short proteins in the mammalian proteome. PLoS Genet 2006, 2:e52. 10.1371/journal.pgen.0020052, 1449894, 16683031.
68. Genomic tRNA database. [http://gtrnadb.ucsc.edu/].
69. TIGR maize database. [http://maize.jcvi.org/].
70. NONCODE. [http://noncode.org/].
71. Small RNA datasets. [http://mpss.udel.edu/maize_sRNA/].
72. Wang X, Elling AA, Li X, Li N, Peng Z, He G, Sun H, Qi Y, Liu XS, Deng XW. Genome-wide and organ-specific landscapes of epigenetic modifications and their relationships to mRNA and small RNA transcriptomes in maize. Plant Cell 2009, 21:1053-1069. 10.1105/tpc.109.065714, 2685623, 19376930.
73. Nobuta K, Lu C, Shrivastava R, Pillay M, De Paoli E, Accerbi M, Arteaga-Vazquez M, Sidorenko L, Jeong DH, Yen Y, Green PJ, Chandler VL, Meyers BC. A novel size distribution of endogeneous siRNAs in maize: evidence from deep sequencing in the mop1-1 mutant. Proc Natl Acad Sci USA 2008, 5:14958-14963.
74. Nobuta K, Venu RC, Lu C, Beló A, Vemaraju K, Kulkarni K, Wang W, Pillay M, Green PJ, Wang GL, Meyers BC. An expression atlas of rice mRNA and small RNA. Nat Biotechnol 2007, 25:473-477. 10.1038/nbt1291, 17351617.
75. RepeatMasker. [http://repeatmasker.org].
76. Repetitive database version 20130422. [http://www.girinst.org].
77. The pipeline for the identification of long noncoding RNAs. [https://github.com/caulilin/lncRNA_Finder].
78. Lee M, Sharopova N, Beavis WD, Grant D, Katt M, Blair D, Hallauer A. Expanding the genetic map of maize with the intermated B73 × Mo17 (IBM) population. Plant Mol Biol 2002, 48:453-461. 10.1023/A:1014893521186, 11999829.