Molecular Genetics and Genomics

, Volume 290, Issue 5, pp 1819–1831 | Cite as

Identification and characterization of paternal-preferentially expressed gene NF-YC8 in maize endosperm

  • Xiupeng Mei
  • Chaoxian Liu
  • Tingting Yu
  • Xiaoli Liu
  • De Xu
  • Jiuguang Wang
  • Guoqiang Wang
  • Yilin CaiEmail author
Original Paper


Gene imprinting describes an epigenetic phenomenon, whereby genetically identical alleles are differentially expressed dependent on parent-of-origin. Some imprinted genes belonged to NUCLEAR FACTOR Y (NF-Y) transcription factors, which were involved in many important metabolic processes in plant. The characterizations of imprinted genes are of great importance for their function exploration. In this paper, 15 non-redundant NF-YC genes were identified in the maize genome and the paternally expressed gene NF-YC8 was further analyzed. NF-YC8 primarily expressed in maize immature ear and tassel and phylogenetic analysis showed that NF-YC8 was highly homologous with Arabidopsis thaliana NF-YC2 genes which function in regulation of the flowering processes, ER stress response. Furthermore, NF-YC8 was a differential, gene-specific imprinted gene at 14 DAP and persistently imprinted throughout later endosperm development in the B73/Mo17 genetic background. Bisulfite sequencing for NF-YC8 in maize endosperm showed that the paternal alleles were higher methylated (CG, CHG and CHH contexts) than maternal alleles in the 5′ upstream region, and the coding region was highly methylated in CG context. Additionally, TE (CG, CHG and CHH contexts) and repetitive region (CG and CHG contexts) were all highly methylated. These results are the first description of evolution and molecular characterization of maize NF-YC8 and will provide new references for maize NF-YC genetic analysis.


NF-Y Gene imprinting Paternally expressed gene Maize endosperm 



The authors would like to thank the Major Research Projects of Chongqing (CSTC2012ggc80003) for providing financial support.

Supplementary material

438_2015_1043_MOESM1_ESM.docx (3.8 mb)
Supplementary material 1 (DOCX 3.75 MB)


  1. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res: gkp335Google Scholar
  2. Berger F (2003) Endosperm: the crossroad of seed development. Curr Opin Plant Biol 6:42–50CrossRefPubMedGoogle Scholar
  3. Bernardi J, Lanubile A, Li QB, Kumar D, Kladnik A, Cook SD, Ross JJ, Marocco A, Chourey PS (2012) Impaired auxin biosynthesis in the defective endosperm 18 mutant is due to mutational loss of expression in the ZmYuc1 gene encoding endosperm-specific YUCCA1 protein in maize. Plant Physiol 160:1318–1328CrossRefPubMedCentralPubMedGoogle Scholar
  4. Cao S, Kumimoto RW, Siriwardana CL, Risinger JR, Holt BF 3rd (2011) Identification and characterization of NF-Y transcription factor families in the monocot model plant Brachypodium distachyon. PLoS One 6:e21805CrossRefPubMedCentralPubMedGoogle Scholar
  5. Costa LM, Yuan J, Rouster J, Paul W, Dickinson H, Gutierrez-Marcos JF (2012) Maternal control of nutrient allocation in plant seeds by genomic imprinting. Curr Biol CB 22:160–165CrossRefPubMedGoogle Scholar
  6. Edwards D, Murray JA, Smith AG (1998) Multiple genes encoding the conserved CCAAT-box transcription factor complex are expressed in Arabidopsis. Plant Physiol 117:1015–1022CrossRefPubMedCentralPubMedGoogle Scholar
  7. Feng S, Jacobsen SE, Reik W (2010) Epigenetic reprogramming in plant and animal development. Science (New York, N.Y.) 330:622–627CrossRefGoogle Scholar
  8. Ferguson-Smith AC (2011) Genomic imprinting: the emergence of an epigenetic paradigm. Nature Rev Genet 12:565–575CrossRefPubMedGoogle Scholar
  9. Fitz Gerald JN, Hui PS, Berger F (2009) Polycomb group-dependent imprinting of the actin regulator AtFH5 regulates morphogenesis in Arabidopsis thaliana. Development 136:3399–3404CrossRefPubMedGoogle Scholar
  10. Gaut BS, Morton BR, McCaig BC, Clegg MT (1996) Substitution rate comparisons between grasses and palms: synonymous rate differences at the nuclear gene Adh parallel rate differences at the plastid gene rbcL. Proc Natl Acad Sci 93:10274–10279CrossRefPubMedCentralPubMedGoogle Scholar
  11. Gehring M, Choi Y, Fischer RL (2004) Imprinting and seed development. Plant Cell 16(Suppl):S203–S213CrossRefPubMedCentralPubMedGoogle Scholar
  12. Gehring M, Huh JH, Hsieh TF, Penterman J, Choi Y, Harada JJ, Goldberg RB, Fischer RL (2006) DEMETER DNA glycosylase establishes MEDEA polycomb gene self-imprinting by allele-specific demethylation. Cell 124:495–506CrossRefPubMedCentralPubMedGoogle Scholar
  13. Gehring M, Missirian V, Henikoff S (2011) Genomic analysis of parent-of-origin allelic expression in Arabidopsis thaliana seeds. PLoS One 6:e23687CrossRefPubMedCentralPubMedGoogle Scholar
  14. Grossniklaus U, Vielle-Calzada JP, Hoeppner MA, Gagliano WB (1998) Maternal control of embryogenesis by MEDEA, a polycomb group gene in Arabidopsis. Science (New York, N.Y.) 280:446–450CrossRefGoogle Scholar
  15. Gutierrez-Marcos JF, Costa LM, Biderre-Petit C, Khbaya B, O’Sullivan DM, Wormald M, Perez P, Dickinson HG (2004) Maternally expressed gene1 is a novel maize endosperm transfer cell-specific gene with a maternal parent-of-origin pattern of expression. Plant Cell 16:1288–1301CrossRefPubMedCentralPubMedGoogle Scholar
  16. Gutierrez-Marcos JF, Costa LM, Dal Pra M, Scholten S, Kranz E, Perez P, Dickinson HG (2006) Epigenetic asymmetry of imprinted genes in plant gametes. Nature Genet 38:876–878CrossRefPubMedGoogle Scholar
  17. Hackenberg D, Keetman U, Grimm B (2012) Homologous NF-YC2 subunit from Arabidopsis and tobacco is activated by photooxidative stress and induces flowering. Int J Mol Sci 13:3458–3477CrossRefPubMedCentralPubMedGoogle Scholar
  18. Haun WJ, Laoueille-Duprat S, O’Connell MJ, Spillane C, Grossniklaus U, Phillips AR, Kaeppler SM, Springer NM (2007) Genomic imprinting, methylation and molecular evolution of maize Enhancer of zeste (Mez) homologs. Plant J Cell Mol Biol 49:325–337CrossRefGoogle Scholar
  19. Hermon P, Srilunchang KO, Zou J, Dresselhaus T, Danilevskaya ON (2007) Activation of the imprinted Polycomb Group Fie1 gene in maize endosperm requires demethylation of the maternal allele. Plant Mol Biol 64:387–395CrossRefPubMedGoogle Scholar
  20. Hsieh TF, Shin J, Uzawa R, Silva P, Cohen S, Bauer MJ, Hashimoto M, Kirkbride RC, Harada JJ, Zilberman D, Fischer RL (2011) Regulation of imprinted gene expression in Arabidopsis endosperm. Proc Natl Acad Sci USA 108:1755–1762CrossRefPubMedCentralPubMedGoogle Scholar
  21. Huh JH, Rim HJ (2013) DNA demethylation and gene imprinting in flowering plants. In: Grafi G, Ohad N (eds) Epigentic memory and control in plants. Signaling and communication in plants, vol 18. Springer, Berlin, Heidelberg, pp 201–232Google Scholar
  22. Huh JH, Bauer MJ, Hsieh TF, Fischer RL (2008) Cellular programming of plant gene imprinting. Cell 132:735–744CrossRefPubMedGoogle Scholar
  23. Ingouff M, Haseloff J, Berger F (2005) Polycomb group genes control developmental timing of endosperm. Plant J 42:663–674CrossRefPubMedGoogle Scholar
  24. Jahnke S, Scholten S (2009) Epigenetic resetting of a gene imprinted in plant embryos. Curr Biol CB 19:1677–1681CrossRefPubMedGoogle Scholar
  25. Jiang H, Kohler C (2012) Evolution, function, and regulation of genomic imprinting in plant seed development. J Exp Botany 63:4713–4722CrossRefGoogle Scholar
  26. Kermicle JL (1970) Dependence of R-mottled aleurone phenotype in maize on mode of sexual transmission. Genetics 66:69–85PubMedCentralPubMedGoogle Scholar
  27. Kinoshita T, Miura A, Choi Y, Kinoshita Y, Cao X, Jacobsen SE, Fischer RL, Kakutani T (2004) One-way control of FWA imprinting in Arabidopsis endosperm by DNA methylation. Science (New York, N.Y.) 303:521–523CrossRefGoogle Scholar
  28. Kohler C, Wolff P, Spillane C (2012) Epigenetic mechanisms underlying genomic imprinting in plants. Ann Rev Plant Biol 63:331–352CrossRefGoogle Scholar
  29. Kumimoto RW, Zhang Y, Siefers N, Holt BF (2010) NF–YC3, NF–YC4 and NF–YC9 are required for CONSTANS-mediated, photoperiod-dependent flowering in Arabidopsis thaliana. Plant J 63:379–391CrossRefPubMedGoogle Scholar
  30. Liang M, Yin X, Lin Z, Zheng Q, Liu G, Zhao G (2014) Identification and characterization of NF-Y transcription factor families in Canola (Brassica napus L.). Planta 239:107–126CrossRefPubMedGoogle Scholar
  31. Lin YX, Jiang HY, Chu ZX, Tang XL, Zhu SW, Cheng BJ (2011) Genome-wide identification, classification and analysis of heat shock transcription factor family in maize. BMC Genom 12:76CrossRefGoogle Scholar
  32. Liu J-X, Howell SH (2010) bZIP28 and NF-Y transcription factors are activated by ER stress and assemble into a transcriptional complex to regulate stress response genes in Arabidopsis. Plant Cell Online 22:782–796CrossRefGoogle Scholar
  33. Luo M, Bilodeau P, Dennis ES, Peacock WJ, Chaudhury A (2000) Expression and parent-of-origin effects for FIS2, MEA, and FIE in the endosperm and embryo of developing Arabidopsis seeds. Proc Natl Acad Sci USA 97:10637–10642CrossRefPubMedCentralPubMedGoogle Scholar
  34. Makarevich G, Villar CB, Erilova A, Kohler C (2008) Mechanism of PHERES1 imprinting in Arabidopsis. J Cell Sci 121:906–912CrossRefPubMedGoogle Scholar
  35. Peng X, Zhao Y, Cao J, Zhang W, Jiang H, Li X, Ma Q, Zhu S, Cheng B (2012) CCCH-type zinc finger family in maize: genome-wide identification, classification and expression profiling under abscisic acid and drought treatments. PLoS One 7:e40120CrossRefPubMedCentralPubMedGoogle Scholar
  36. Petroni K, Kumimoto RW, Gnesutta N, Calvenzani V, Fornari M, Tonelli C, Holt BF III, Mantovani R (2012) The promiscuous life of plant NUCLEAR FACTOR Y transcription factors. Plant Cell 24:4777–4792CrossRefPubMedCentralPubMedGoogle Scholar
  37. Pignatta D, Gehring M (2012) Imprinting meets genomics: new insights and new challenges. Curr Opin Plant Biol 15:530–535CrossRefPubMedGoogle Scholar
  38. Reik W, Walter J (2001) Genomic imprinting: parental influence on the genome. Nature Rev Genet 2:21–32CrossRefPubMedGoogle Scholar
  39. Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497CrossRefPubMedGoogle Scholar
  40. Sato H, Mizoi J, Tanaka H, Maruyama K, Qin F, Osakabe Y, Morimoto K, Ohori T, Kusakabe K, Nagata M (2014) Arabidopsis DPB3-1, a DREB2A interactor, specifically enhances heat stress-induced gene expression by forming a heat stress-specific transcriptional complex with NF-Y subunits. Plant Cell Online tpc 114:132928Google Scholar
  41. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA (2009) The B73 maize genome: complexity, diversity, and dynamics. Science (New York, N.Y.) 326:1112–1115CrossRefGoogle Scholar
  42. Scholten S (2010) Genomic imprinting in plant embryos. Epigenet Offi J DNA Methylation Soc 5:455–459CrossRefGoogle Scholar
  43. Stephenson TJ, McIntyre CL, Collet C, Xue GP (2007) Genome-wide identification and expression analysis of the NF-Y family of transcription factors in Triticum aestivum. Plant Mol Biol 65:77–92CrossRefPubMedGoogle Scholar
  44. Takuno S, Gaut BS (2013a) Gene body methylation is conserved between plant orthologs and is of evolutionary consequence. Proc Natl Acad Sci USA 110:1797–1802CrossRefPubMedCentralPubMedGoogle Scholar
  45. Takuno S, Gaut BS (2013b) Gene body methylation is conserved between plant orthologs and is of evolutionary consequence. Proc Natl Acad Sci USA 110:1797–1802CrossRefPubMedCentralPubMedGoogle Scholar
  46. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evolut 24:1596–1599CrossRefGoogle Scholar
  47. Thiel T, Kota R, Grosse I, Stein N, Graner A (2004) SNP2CAPS: a SNP and INDEL analysis tool for CAPS marker development. Nucleic Acids Res 32:e5–e5CrossRefPubMedCentralPubMedGoogle Scholar
  48. Thirumurugan T, Ito Y, Kubo T, Serizawa A, Kurata N (2008) Identification, characterization and interaction of HAP family genes in rice. Mol Genet Genom MGG 279:279–289CrossRefGoogle Scholar
  49. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882CrossRefPubMedCentralPubMedGoogle Scholar
  50. Tiwari S, Schulz R, Ikeda Y, Dytham L, Bravo J, Mathers L, Spielman M, Guzman P, Oakey RJ, Kinoshita T, Scott RJ (2008) MATERNALLY EXPRESSED PAB C-TERMINAL, a novel imprinted gene in Arabidopsis, encodes the conserved C-terminal domain of polyadenylate binding proteins. Plant Cell 20:2387–2398CrossRefPubMedCentralPubMedGoogle Scholar
  51. Vielle-Calzada JP, Baskar R, Grossniklaus U (2000) Delayed activation of the paternal genome during seed development. Nature 404:91–94CrossRefPubMedGoogle Scholar
  52. Vu TM, Nakamura M, Calarco JP, Susaki D, Lim PQ, Kinoshita T, Higashiyama T, Martienssen RA, Berger F (2013) RNA-directed DNA methylation regulates parental genomic imprinting at several loci in Arabidopsis. Development 140:2953–2960CrossRefPubMedCentralPubMedGoogle Scholar
  53. Wang X, Soloway PD, Clark AG (2011) A survey for novel imprinted genes in the mouse placenta by mRNA-seq. Genetics 189:109–122CrossRefPubMedCentralPubMedGoogle Scholar
  54. Waters AJ, Makarevitch I, Eichten SR, Swanson-Wagner RA, Yeh CT, Xu W, Schnable PS, Vaughn MW, Gehring M, Springer NM (2011) Parent-of-origin effects on gene expression and DNA methylation in the maize endosperm. Plant Cell 23:4221–4233CrossRefPubMedCentralPubMedGoogle Scholar
  55. Waters AJ, Bilinski P, Eichten SR, Vaughn MW, Ross-Ibarra J, Gehring M, Springer NM (2013) Comprehensive analysis of imprinted genes in maize reveals allelic variation for imprinting and limited conservation with other species. Proc Natl Acad Sci USA 110:19639–19644CrossRefPubMedCentralPubMedGoogle Scholar
  56. Wei F, Coe E, Nelson W, Bharti AK, Engler F, Butler E, Kim H, Goicoechea JL, Chen M, Lee S (2007) Physical and genetic structure of the maize genome reflects its complex evolutionary history. PLoS Genet 3:e123CrossRefPubMedCentralPubMedGoogle Scholar
  57. Wenkel S, Turck F, Singer K, Gissot L, Le Gourrierec J, Samach A, Coupland G (2006) CONSTANS and the CCAAT box binding complex share a functionally important domain and interact to regulate flowering of Arabidopsis. Plant Cell Online 18:2971–2984CrossRefGoogle Scholar
  58. Wolff P, Weinhofer I, Seguin J, Roszak P, Beisel C, Donoghue MT, Spillane C, Nordborg M, Rehmsmeier M, Kohler C (2011) High-resolution analysis of parent-of-origin allelic expression in the Arabidopsis endosperm. PLoS Genet 7:e1002126CrossRefPubMedCentralPubMedGoogle Scholar
  59. Xin M, Yang R, Li G, Chen H, Laurie J, Ma C, Wang D, Yao Y, Larkins BA, Sun Q, Yadegari R, Wang X, Ni Z (2013) Dynamic expression of imprinted genes associates with maternally controlled nutrient allocation during maize endosperm development. Plant Cell 25:3212–3227CrossRefPubMedCentralPubMedGoogle Scholar
  60. Yamamoto A, Kagaya Y, Toyoshima R, Kagaya M, Takeda S, Hattori T (2009) Arabidopsis NF-YB subunits LEC1 and LEC1-LIKE activate transcription by interacting with seed-specific ABRE-binding factors. Plant J 58:843–856CrossRefPubMedGoogle Scholar
  61. Zemach A, McDaniel IE, Silva P, Zilberman D (2010) Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science (New York, N.Y.) 328:916–919CrossRefGoogle Scholar
  62. Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SW, Chen H, Henderson IR, Shinn P, Pellegrini M, Jacobsen SE, Ecker JR (2006) Genome-wide high-resolution mapping and functional analysis of DNA methylation in arabidopsis. Cell 126:1189–1201CrossRefPubMedGoogle Scholar
  63. Zhang M, Zhao H, Xie S, Chen J, Xu Y, Wang K, Zhao H, Guan H, Hu X, Jiao Y, Song W, Lai J (2011) Extensive, clustered parental imprinting of protein-coding and noncoding RNAs in developing maize endosperm. Proc Natl Acad Sci USA 108:20042–20047CrossRefPubMedCentralPubMedGoogle Scholar
  64. Zhang M, Xie S, Dong X, Zhao X, Zeng B, Chen J, Li H, Yang W, Zhao H, Wang G, Chen Z, Sun S, Hauck A, Jin W, Lai J (2014) Genome-wide high resolution parental-specific DNA and histone methylation maps uncover patterns of imprinting regulation in maize. Genom Res 24:167–176CrossRefGoogle Scholar
  65. Zhu JK (2009) Active DNA demethylation mediated by DNA glycosylases. Ann Rev Genet 43:143–166CrossRefPubMedCentralPubMedGoogle Scholar
  66. Zilberman D, Gehring M, Tran RK, Ballinger T, Henikoff S (2007) Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nature Genet 39:61–69CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Xiupeng Mei
    • 1
  • Chaoxian Liu
    • 1
  • Tingting Yu
    • 1
  • Xiaoli Liu
    • 1
  • De Xu
    • 1
  • Jiuguang Wang
    • 1
  • Guoqiang Wang
    • 1
  • Yilin Cai
    • 1
    Email author
  1. 1.Maize Research Institute, Key Laboratory of Biotechnology and Crop Quality Improvement, Ministry of AgricultureSouthwest UniversityChongqingChina

Personalised recommendations