Global RNA sequencing reveals that genotype-dependent allele-specific expression contributes to differential expression in rice F1 hybrids
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  • 作者:Gaoyuan Song (21)
    Zhibin Guo (21)
    Zhenwei Liu (21)
    Qin Cheng (21)
    Xuefeng Qu (21)
    Rong Chen (21)
    Daiming Jiang (21)
    Chuan Liu (21)
    Wei Wang (21)
    Yunfang Sun (21)
    Liping Zhang (21)
    Yingguo Zhu (21)
    Daichang Yang (21)
  • 关键词:Allele ; specific expression ; Complementary effects ; Differentially expressed genes ; Genotype ; dependent monoallelic expression ; Rice hybrids
  • 刊名:BMC Plant Biology
  • 出版年:2013
  • 出版时间:December 2013
  • 年:2013
  • 卷:13
  • 期:1
  • 全文大小:1,040 KB
  • 参考文献:1. Shull GH: The composition of a field of maize. / Am Breeders Assoc Rep 1908, 4:296-01.
    2. Darwin CR: / The effects of cross and self fertilization in the vegetable kingdom. London: John Murray; 1876.
    3. East EM: Inbreeding in corn. / Conn Agric Exp Sta Rep 1907, 1908:419-28.
    4. Crow JF: Alternative hypotheses of hybrid vigor. / Genetics 1948,33(5):477-87.
    5. Zhou G, Chen Y, Yao W, Zhang C, Xie W, Hua J, Xing Y, Xiao J, Zhang Q: Genetic composition of yield heterosis in an elite rice hybrid. / Proc Natl Acad Sci U S A 2012,109(39):15847-5852. CrossRef
    6. Lariepe A, Mangin B, Jasson S, Combes V, Dumas F, Jamin P, Lariagon C, Jolivot D, Madur D, Fievet J, / et al.: The genetic basis of heterosis: multiparental quantitative trait loci mapping reveals contrasted levels of apparent overdominance among traits of agronomical interest in maize (Zea mays L.). / Genetics 2012,190(2):795-11. CrossRef
    7. Meyer RC, Kusterer B, Lisec J, Steinfath M, Becher M, Scharr H, Melchinger AE, Selbig J, Schurr U, Willmitzer L, / et al.: QTL analysis of early stage heterosis for biomass in Arabidopsis. / Theor Appl Genet 2010,120(2):227-37. CrossRef
    8. Li L, Lu K, Chen Z, Mu T, Hu Z, Li X: Dominance, overdominance and epistasis condition the heterosis in two heterotic rice hybrids. / Genetics 2008,180(3):1725-742. CrossRef
    9. Hua J, Xing Y, Wu W, Xu C, Sun X, Yu S, Zhang Q: Single-locus heterotic effects and dominance by dominance interactions can adequately explain the genetic basis of heterosis in an elite rice hybrid. / Proc Natl Acad Sci U S A 2003,100(5):2574-579. CrossRef
    10. Luo LJ, Li ZK, Mei HW, Shu QY, Tabien R, Zhong DB, Ying CS, Stansel JW, Khush GS, Paterson AH: Overdominant epistatic loci are the primary genetic basis of inbreeding depression and heterosis in rice. II. Grain yield components. / Genetics 2001,158(4):1755-771.
    11. Li ZK, Luo LJ, Mei HW, Wang DL, Shu QY, Tabien R, Zhong DB, Ying CS, Stansel JW, Khush GS, / et al.: Overdominant epistatic loci are the primary genetic basis of inbreeding depression and heterosis in rice. I. Biomass and grain yield. / Genetics 2001,158(4):1737-753.
    12. Stupar RM, Springer NM: Cis-transcriptional variation in maize inbred lines B73 and Mo17 leads to additive expression patterns in the F1 hybrid. / Genetics 2006,173(4):2199-210. CrossRef
    13. Zhang X, Borevitz JO: Global analysis of allele-specific expression in Arabidopsis thaliana. / Genetics 2009,182(4):943-54. CrossRef
    14. Wei G, Tao Y, Liu G, Chen C, Luo R, Xia H, Gan Q, Zeng H, Lu Z, Han Y, / et al.: A transcriptomic analysis of superhybrid rice LYP9 and its parents. / Proc Natl Acad Sci U S A 2009,106(19):7695-701. CrossRef
    15. He G, Zhu X, Elling AA, Chen L, Wang X, Guo L, Liang M, He H, Zhang H, Chen F, / et al.: Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids. / Plant Cell 2010,22(1):17-3. CrossRef
    16. Paschold A, Jia Y, Marcon C, Lund S, Larson NB, Yeh CT, Ossowski S, Lanz C, Nettleton D, Schnable PS, / et al.: Complementation contributes to transcriptome complexity in maize (Zea mays L.) hybrids relative to their inbred parents. / Genome Res 2012,22(12):2445-454. CrossRef
    17. Bix M, Locksley RM: Independent and epigenetic regulation of the interleukin-4 alleles in CD4+ T cells. / Science 1998,281(5381):1352-354. CrossRef
    18. Chess A, Simon I, Cedar H, Axel R: Allelic inactivation regulates olfactory receptor gene expression. / Cell 1994,78(5):823-34. CrossRef
    19. Lyon MF: X chromosomes and dosage compensation. / Nature 1986,320(6060):313. CrossRef
    20. Pernis B, Chiappino G, Kelus AS, Gell PG: Cellular localization of immunoglobulins with different allotypic specificities in rabbit lymphoid tissues. / J Exp Med 1965,122(5):853-76. CrossRef
    21. Zhang K, Li JB, Gao Y, Egli D, Xie B, Deng J, Li Z, Lee JH, Aach J, Leproust EM, / et al.: Digital RNA allelotyping reveals tissue-specific and allele-specific gene expression in human. / Nat Methods 2009,6(8):613-18. CrossRef
    22. Gimelbrant A, Hutchinson JN, Thompson BR, Chess A: Widespread monoallelic expression on human autosomes. / Science 2007,318(5853):1136-140. CrossRef
    23. Yan H, Yuan W, Velculescu VE, Vogelstein B, Kinzler KW: Allelic variation in human gene expression. / Science 2002,297(5584):1143. CrossRef
    24. Springer NM, Stupar RM: Allele-specific expression patterns reveal biases and embryo-specific parent-of-origin effects in hybrid maize. / Plant Cell 2007,19(8):2391-402. CrossRef
    25. Guo M, Rupe MA, Zinselmeier C, Habben J, Bowen BA, Smith OS: Allelic variation of gene expression in maize hybrids. / Plant Cell 2004,16(7):1707-716. CrossRef
    26. Lam HY, Pan C, Clark MJ, Lacroute P, Chen R, Haraksingh R, O’Huallachain M, Gerstein MB, Kidd JM, Bustamante CD, / et al.: Detecting and annotating genetic variations using the HugeSeq pipeline. / Nat Biotechnol 2012,30(3):226-29. CrossRef
    27. Nodine MD, Bartel DP: Maternal and paternal genomes contribute equally to the transcriptome of early plant embryos. / Nature 2012,482(7383):94-7. CrossRef
    28. Stupar RM, Gardiner JM, Oldre AG, Haun WJ, Chandler VL, Springer NM: Gene expression analyses in maize inbreds and hybrids with varying levels of heterosis. / BMC Plant Biol 2008, 8:33. CrossRef
    29. Springer NM, Stupar RM: Allelic variation and heterosis in maize: how do two halves make more than a whole? / Genome Res 2007,17(3):264-75. CrossRef
    30. Birchler JA, Veitia RA: The gene balance hypothesis: implications for gene regulation, quantitative traits and evolution. / New Phytol 2010,186(1):54-2. CrossRef
    31. Birchler JA, Yao H, Chudalayandi S, Vaiman D, Veitia RA: Heterosis. / Plant Cell 2010,22(7):2105-112. CrossRef
    32. Fujimoto R, Taylor JM, Shirasawa S, Peacock WJ, Dennis ES: Heterosis of Arabidopsis hybrids between C24 and Col is associated with increased photosynthesis capacity. / Proc Natl Acad Sci U S A 2012,109(18):7109-114. CrossRef
    33. Hochholdinger F, Hoecker N: Towards the molecular basis of heterosis. / Trends Plant Sci 2007,12(9):427-32. CrossRef
    34. Fischer RA, Kohn GD: The relationship of grain yield to vegetative growth and post-flowering leaf area in the wheat crop under conditions of limited soil moisture. / Aust J Agric Res 1966, 17:281-95. CrossRef
    35. Mai M, Yokomizo A, Qian C, Yang P, Tindall DJ, Smith DI, Liu W: Activation of p73 silent allele in lung cancer. / Cancer Res 1998,58(11):2347-349.
    36. Hollander GA, Zuklys S, Morel C, Mizoguchi E, Mobisson K, Simpson S, Terhorst C, Wishart W, Golan DE, Bhan AK, / et al.: Monoallelic expression of the interleukin-2 locus. / Science 1998,279(5359):2118-121. CrossRef
    37. Rhoades KL, Singh N, Simon I, Glidden B, Cedar H, Chess A: Allele-specific expression patterns of interleukin-2 and Pax-5 revealed by a sensitive single-cell RT-PCR analysis. / Curr Biol 2000,10(13):789-92. CrossRef
    38. Wittkopp PJ, Haerum BK, Clark AG: Evolutionary changes in cis and trans gene regulation. / Nature 2004,430(6995):85-8. CrossRef
    39. Cowles CR, Hirschhorn JN, Altshuler D, Lander ES: Detection of regulatory variation in mouse genes. / Nat Genet 2002,32(3):432-37. CrossRef
    40. Guo M, Yang S, Rupe M, Hu B, Bickel DR, Arthur L, Smith O: Genome-wide allele-specific expression analysis using Massively Parallel Signature Sequencing (MPSS) reveals cis- and trans-effects on gene expression in maize hybrid meristem tissue. / Plant Mol Biol 2008,66(5):551-63. CrossRef
    41. Zhang M, Zhao H, Xie S, Chen J, Xu Y, Wang K, Guan H, Hu X, Jiao Y, Song W, / et al.: Extensive, clustered parental imprinting of protein-coding and noncoding RNAs in developing maize endosperm. / Proc Natl Acad Sci U S A 2011,108(50):20042-0047. CrossRef
    42. Wolff P, Weinhofer I, Seguin J, Roszak P, Beisel C, Donoghue MT, Spillane C, Nordborg M, Rehmsmeier M, Kohler C: High-resolution analysis of parent-of-origin allelic expression in the Arabidopsis Endosperm. / PLoS Genet 2011,7(6):e1002126. CrossRef
    43. 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(12):4221-233. CrossRef
    44. Luo M, Taylor JM, Spriggs A, Zhang H, Wu X, Russell S, Singh M, Koltunow A: A genome-wide survey of imprinted genes in rice seeds reveals imprinting primarily occurs in the endosperm. / PLoS Genet 2011,7(6):e1002125. CrossRef
    45. Shoemaker R, Deng J, Wang W, Zhang K: Allele-specific methylation is prevalent and is contributed by CpG-SNPs in the human genome. / Genome Res 2010,20(7):883-89. CrossRef
    46. Song R, Messing J: Gene expression of a gene family in maize based on noncollinear haplotypes. / Proc Natl Acad Sci U S A 2003,100(15):9055-060. CrossRef
    47. Meyer RC, Witucka-Wall H, Becher M, Blacha A, Boudichevskaia A, Dormann P, Fiehn O, Friedel S, von Korff M, Lisec J, / et al.: Heterosis manifestation during early Arabidopsis seedling development is characterized by intermediate gene expression and enhanced metabolic activity in the hybrids. / Plant J 2012,71(4):669-83. CrossRef
    48. Krieger U, Lippman ZB, Zamir D: The flowering gene SINGLE FLOWER TRUSS drives heterosis for yield in tomato. / Nat Genet 2010,42(5):459-63. CrossRef
    49. Ma Q, Hedden P, Zhang Q: Heterosis in rice seedlings: its relationship to gibberellin content and expression of gibberellin metabolism and signaling genes. / Plant Physiol 2011,156(4):1905-920. CrossRef
    50. Li R, Yu C, Li Y, Lam TW, Yiu SM, Kristiansen K, Wang J: SOAP2: an improved ultrafast tool for short read alignment. / Bioinformatics 2009,25(15):1966-967. CrossRef
    51. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B: Mapping and quantifying mammalian transcriptomes by RNA-Seq. / Nat Methods 2008,5(7):621-28. CrossRef
    52. Audic S, Claverie JM: The significance of digital gene expression profiles. / Genome Res 1997,7(10):986-95.
    53. Wang W, Liu Z, Guo Z, Song G, Cheng Q, Jiang D, Zhu Y, Yang D: Comparative transcriptomes profiling of photoperiod-sensitive male sterile rice Nongken 58S during the male sterility transition between short-day and long-day. / BMC Genomics 2011, 12:462. CrossRef
  • 作者单位:Gaoyuan Song (21)
    Zhibin Guo (21)
    Zhenwei Liu (21)
    Qin Cheng (21)
    Xuefeng Qu (21)
    Rong Chen (21)
    Daiming Jiang (21)
    Chuan Liu (21)
    Wei Wang (21)
    Yunfang Sun (21)
    Liping Zhang (21)
    Yingguo Zhu (21)
    Daichang Yang (21)

    21. State Key Laboratory of Hybrid Rice and College of Life Sciences, Wuhan University, Luojia Hill, Wuhan, Hubei Province, 430072, China
  • ISSN:1471-2229
文摘
Background Extensive studies on heterosis in plants using transcriptome analysis have identified differentially expressed genes (DEGs) in F1 hybrids. However, it is not clear why yield in heterozygotes is superior to that of the homozygous parents or how DEGs are produced. Global allele-specific expression analysis in hybrid rice has the potential to answer these questions. Results We report a genome-wide allele-specific expression analysis using RNA-sequencing technology of 3,637-,824 genes from three rice F1 hybrids. Of the expressed genes, 3.7% exhibited an unexpected type of monoallelic expression and 23.8% showed preferential allelic expression that was genotype-dependent in reciprocal crosses. Those genes exhibiting allele-specific expression comprised 42.4% of the genes differentially expressed between F1 hybrids and their parents. Allele-specific expression accounted for 79.8% of the genes displaying more than a 10-fold expression level difference between an F1 and its parents, and almost all (97.3%) of the genes expressed in F1, but non-expressed in one parent. Significant allelic complementary effects were detected in the F1 hybrids of rice. Conclusions Analysis of the allelic expression profiles of genes at the critical stage for highest biomass production from the leaves of three different rice F1 hybrids identified genotype-dependent allele-specific expression genes. A cis-regulatory mechanism was identified that contributes to allele-specific expression, leading to differential gene expression and allelic complementary effects in F1 hybrids.

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