Heterosis in early maize ear inflorescence development: A genome-wide transcription analysis for two maize inbred lines and their hybrid

International Journal of Molecular Sciences

Volumn 15, Issue 8, 2014, Pages 13892-13915

  Ding, Haiping ^a   Qin, Cheng ^a,b   Luo, Xirong ^b   Li, Lujiang ^a   Chen, Zhe ^a   Liu, Hongjun ^a   Gao, Jian ^a   Lin, Haijian ^a   Shen, Yaou ^a   Zhao, Maojun ^a   Lübberstedt, Thomas ^c   Zhang, Zhiming ^a   Pan, Guangtang ^a  

^a SICHUAN AGRICULTURAL UNIVERSITY   (China)

^b Zunyi Academy of Agricultural Sciences ^*  (China)

^c IOWA STATE UNIVERSITY   (United States)

Author keywords

DGE (digital gene expression); Differentially expressed genes; Heterosis; Maize (Zea mays L.); Multiple molecular mechanisms

Indexed keywords

ADENOSYLMETHIONINE DECARBOXYLASE; ALDEHYDE DEHYDROGENASE; ARGININE; ARGININOSUCCINATE SYNTHASE; AUXIN; BRASSINOSTEROID; ETHYLENE; GLYOXYLATEREDUCTASE; GLYOXYLIC ACID DERIVATIVE; GUANOSINE PHOSPHATE REDUCTASE; INOSINATE DEHYDROGENASE; MESSENGER RNA; ORNITHINE CARBAMOYLTRANSFERASE; OXIDOREDUCTASE; PHOSPHOENOLPYRUVATE CARBOXYLASE; PROLINE; PYRUVATE PHOSPHATE DIKINASE; PYRUVIC ACID; TERPENE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; TRANSCRIPTOME; VEGETABLE PROTEIN;

ARABIDOPSIS; ARTICLE; CELL COMPONENT; CONTROLLED STUDY; EARLY MAIZE EAR; GENE ACTIVITY; GENE EXPRESSION; GENE MAPPING; GENE ONTOLOGY; GENE SEQUENCE; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; HETEROSIS; HYBRID; INBRED STRAIN; INFLORESCENCE; MERISTEM; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; OVERLAPPING GENE; PLANT EAR; PURINE METABOLISM; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPLICEOSOME; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENE LIBRARY; GENETICS; HIGH THROUGHPUT SEQUENCING; INBREEDING; MAIZE; METABOLISM; PLANT GENOME;

GENE EXPRESSION REGULATION, PLANT; GENE LIBRARY; GENETIC VARIATION; GENOME, PLANT; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HYBRID VIGOR; INBREEDING; INFLORESCENCE; PLANT PROTEINS; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION FACTORS; TRANSCRIPTOME; ZEA MAYS;

EID: 84925876569     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms150813892     Document Type: Article

References (72)

1. Shull, G.H. The composition of a field of maize. J. Hered. 1908, 4, 296-301.
2. Bruce, A.B. The Mendelian theory of heredity and the augmentation of vigor. Science 1910, 32, 627.
3. Jones, D.F. Dominance of linked factors as a means of accounting for heterosis. Genetics 1917, 6, 466-479.
4. Davenport, C.B. Degeneration, albinism and inbreeding. Science 1908, 28, 454.
5. East, E.M. Heterosis. Genetics 1936, 21, 375-397.
6. Birchler, J.A.; Auger, D.L.; Riddle, N.C. In search of the molecular basis of heterosis. Plant Cell 2003, 15, 2236-2239.
7. Yu, S.B.; Li, J.X.; Xu, C.G.; Tan, Y.F.; Gao, Y.J.; Li, X.H.; Zhang, Q.F.; Saghai Maroof, M.A. Importance of epistasis as the genetic basis of heterosis in an elite rice hybrid. Proc. Natl. Acad. Sci. USA 1997, 99, 9226-9231.
8. Li, Z.K.; Luo, L.J.; Mei, H.W.; Wang, D.L.; Shu, Q.Y.; Tabien, R.; Zhong, D.B.; Ying, C.S.; Stansel, J.W.; Khush, G.S.; 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, 1737-1753.
9. Xiao, J.; Li, J.; Yuan, L.; Tanksley, S.D. Dominance is the major genetic basis of heterosis in rice as revealed by QTL analysis using molecular markers. Genetics 1995, 140, 745-754.
10. Stuber, C.W.; Lincoln, S.E.; Wolff, D.W.; Helentjaris, T.; Lander, E.S. Identification of genetic factors contributing to heterosis in a hybrid from two elite maize inbred lines using molecular markers. Genetics 1992, 132, 823-839.
11. Auger, D.L.; Gray, A.D.; Ream, T.S.; Kato, A.; Coe, E.H., Jr.; Birchler, J.A. Nonadditive gene expression in diploid and triploid hybrids of maize. Genetics 2005, 169, 389-397.
12. Hoecker, N.; Keller, B.; Muthreich, N.; Chollet, D.; Descombes, P.; Piepho, H.P.; Hochholdinger, F. Comparison of maize (Zea mays L.) F1-hybrid and parental inbred line primary root transcriptomes suggests organ-specific patterns of nonadditive gene expression and conserved expression trends. Genetics 2008, 179, 1275-1283.
13. Song, R.; Messing, J. Gene expression of a gene family in maize based on noncollinear haplotypes. Proc. Natl. Acad. Sci. USA 2003, 100, 9055-9060.
14. Stupar, R.M.; Springer, N.M. cis-Transcriptional variation in maize inbred lines B73 and Mo17 leads to additive expression patterns in the F1 hybrid. Genetics 2006, 173, 2199-2210.
15. Vuylsteke, M.; van Eeuwijk, F.; van Hummelen, P.; Kuiper, M.; Zabeau, M. Genetic analysis of variation in gene expression in Arabidopsis thaliana. Genetics 2005, 171, 1267-1275.
16. Zhang, H.Y.; He, H.; Chen, L.B.; Li, L.; Liang, M.Z.; Wang, X.F.; Liu, X.G.; He, G.M.; Chen, R.S.; Ma, L.G.; et al. A genome-wide transcription analysis reveals a close correlation of promoter INDEL polymorphism and heterotic gene expression in rice hybrids. Mol. Plant 2008, 1, 720-731.
17. Guo, M.; Yang, S.; Rupe, M.; Hu, B.; Bickel, D.; Arthur, L.; Smith, O. Genome-wide allele-specific expression analysis using Massively Parallel Signature Sequencing (MPSSTM) Reveals cis-and trans-effects on gene expression in maize hybrid meristem tissue. Plant Mol. Biol. 2008, 66, 551-563.
18. Chen, X.; Li, M.; Shi, J.; Fu, D.; Qian, W.; Zou, J.; Zhang, C.; Meng, J. Gene expression profiles associated with intersubgenomic heterosis in Brassica napus. Theor. Appl. Genet. 2008, 117, 1031-1040.
19. Zhuang, Y.; Adams, K.L. Extensive allelic variation in gene expression in populus F1 hybrids. Genetics 2007, 177, 1987-1996.
20. Jahnke, S.; Sarholz, B.; Thiemann, A.; Kühr, V.; Gutiérrez-Marcos, J.; Geiger, H.; Piepho, H.-P.; Scholten, S. Heterosis in early seed development: A comparative study of F1 embryo and endosperm tissues 6 days after fertilization. Theor. Appl. Genet. 2010, 120, 389-400.
21. Pea, G.; Ferron, S.; Gianfranceschi, L.; Krajewski, P.; Enrico Pe, M. Gene expression non-additivity in immature ears of a heterotic F1 maize hybrid. Plant Sci. 2008, 174, 17-24.
22. Riddle, N.; Jiang, H.; An, L.; Doerge, R.; Birchler, J. Gene expression analysis at the intersection of ploidy and hybridity in maize. Theor. Appl. Genet. 2010, 120, 341-353.
23. Guo, M.; Rupe, M.A.; Yang, X.; Crasta, O.; Zinselmeier, C.; Smith, O.S.; Bowen, B. Genome-wide transcript analysis of maize hybrids: Allelic additive gene expression and yield heterosis. Theor. Appl. Genet. 2006, 113, 831-845.
24. Paschold, A.; Marcon, C.; Hoecker, N.; Hochholdinger, F. Molecular dissection of heterosis manifestation during early maize root development. Theor. Appl. Genet. 2010, 120, 383-388.
25. Meyer, S.; Pospisil, H.; Scholten, S. Heterosis associated gene expression in maize embryos 6 days after fertilization exhibits additive, dominant and overdominant pattern. Plant Mol. Biol. 2007, 63, 381-391.
26. Stupar, R.M.; Gardiner, J.M.; Oldre, A.G.; Haun, W.J.; Chandler, V.L.; Springer, N.M. Gene expression analyses in maize inbreds and hybrids with varying levels of heterosis. BMC Plant Biol. 2008, 8, 33.
27. Uzarowska, A.; Keller, B.; Piepho, H.P.; Schwarz, G.; Ingvardsen, C.; Wenzel, G.; Lubberstedt, T. Comparative expression profiling in meristems of inbred-hybrid triplets of maize based on morphological investigations of heterosis for plant height. Plant Mol. Biol. 2007, 63, 21-34.
28. Sun, Q.; Wu, L.; Ni, Z.; Meng, F.; Wang, Z.; Lin, Z. Differential gene expression patterns in leaves between hybrids and their parental inbreds are correlated with heterosis in a wheat diallel cross. Plant Sci. 2004, 166, 651-657.
29. Swanson-Wagner, R.A.; DeCook, R.; Jia, Y.; Bancroft, T.; Ji, T.; Zhao, X.; Nettleton, D.; Schnable, P.S. Paternal dominance of trans-eQTL influences gene expression patterns in maize hybrids. Science 2009, 326, 1118-1120.
30. 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. USA 2009, 106, 7695-7701.
31. Swanson-Wagner, R.A.; Jia, Y.; DeCook, R.; Borsuk, L.A.; Nettleton, D.; Schnable, P.S. All possible modes of gene action are observed in a global comparison of gene expression in a maize F1 hybrid and its inbred parents. Proc. Natl. Acad. Sci. USA 2006, 103, 6805-6810.
32. Song, G.S.; Zhai, H.L.; Peng, Y.G.; Zhang, L.; Wei, G.; Chen, X.Y.; Xiao, Y.G.; Wang, L.; Chen, Y.J.; Wu, B.; et al. Comparative transcriptional profiling and preliminary study on heterosis mechanism of super-hybrid rice. Mol. Plant 2010, 3, 1012-1025.
33. Chen, Z.J. Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annu. Rev. Plant Biol. 2007, 58, 377-406.
34. Ha, M.; Lu, J.; Tian, L.; Ramachandran, V.; Kasschau, K.D.; Chapman, E.J.; Carrington, J.C.; Chen, X.; Wang, X.J.; Chen, Z.J. Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids. Proc. Natl. Acad. Sci. USA 2009, 106, 17835-17840.
35. He, G.; Zhu, X.; Elling, A.A.; 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, 17-33.
36. Liu, H.; Qin, C.; Chen, Z.; Zuo, T.; Yang, X.; Zhou, H.; Xu, M.; Cao, S.; Shen, Y.; Lin, H.; et al. Identification of miRNAs and their target genes in developing maize ears by combined small RNA and degradome sequencing. BMC Genomics 2014, 15, 25.
37. Hollick, J.B.; Chandler, V.L. Epigenetic allelic states of a maize transcriptional regulatory locus exhibit overdominant gene action. Genetics 1998, 150, 891-897.
38. Zhao, X.; Chai, Y.; Liu, B. Epigenetic inheritance and variation of DNA methylation level and pattern in maize intra-specific hybrids. Plant Sci. 2007, 172, 930-938.
39. Ni, Z.; Kim, E.D.; Ha, M.; Lackey, E.; Liu, J.; Zhang, Y.; Sun, Q.; Chen, Z.J. Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature 2009, 457, 327-331.
40. Wang, X.; Cao, H.; Zhang, D.; Li, B.; He, Y.; Li, J.; Wang, S. Relationship between differential gene expression and heterosis during ear development in maize (zea mays L.). J. Genet. Genomics 2007, 34, 160-170.
41. Li, R.; Yu, C.; Li, Y.; Lam, T.W.; Yiu, S.M.; Kristiansen, K.; Wang, J. SOAP2: An improved ultrafast tool for short read alignment. Bioinformatics 2009, 25, 1966-1967.
42. Li, P.; Ponnala, L.; Gandotra, N.; Wang, L.; Si, Y.; Tausta, S.L.; Kebrom, T.H.; Provart, N.; Patel, R.; Myers, C.R.; et al. The developmental dynamics of the maize leaf transcriptome. Nat. Genet. 2010, 42, 1060-1067.
43. Schnable, P.S.; Ware, D.; Fulton, R.S.; Stein, J.C.; Wei, F.; Pasternak, S.; Liang, C.; Zhang, J.; Fulton, L.; Graves, T.A.; et al. The B73 maize genome: Complexity, diversity, and dynamics. Science 2009, 326, 1112-1115.
44. Ashburner, M.; Ball, C.A.; Blake, J.A.; Botstein, D.; Butler, H.; Cherry, J.M.; Davis, A.P.; Dolinski, K.; Dwight, S.S.; Eppig, J.T.; et al. Gene ontology: Tool for the unification of biology-The gene ontology consortium. Nat. Genet. 2000, 25, 25-29.
45. Carbon, S.; Ireland, A.; Mungall, C.J.; Shu, S.; Marshall, B.; Lewis, S. AmiGO: Online access to ontology and annotation data. Bioinformatics 2009, 25, 288-289.
46. Xie, C.; Mao, X.; Huang, J.; Ding, Y.; Wu, J.; Dong, S.; Kong, L.; Gao, G.; Li, C.-Y.; Wei, L. KOBAS 2.0: A web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res. 2011, 39, W316-W322.
47. Storey, J.D.; Tibshirani, R. Statistical significance for genomewide studies. Proc. Natl. Acad. Sci. USA 2003, 100, 9440-9445.
48. Mao, X.; Cai, T.; Olyarchuk, J.G.; Wei, L. Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 2005, 21, 3787-3793.
49. Wu, J.; Mao, X.; Cai, T.; Luo, J.; Wei, L. KOBAS server: A web-based platform for automated annotation and pathway identification. Nucleic Acids Res. 2006, 34, W720-W724.
50. Vilella, A.J.; Severin, J.; Ureta-Vidal, A.; Heng, L.; Durbin, R.; Birney, E. EnsemblCompara GeneTrees: Complete, duplication-aware phylogenetic trees in vertebrates. Genome Res. 2009, 19, 327-335.
51. Liang, C.; Jaiswal, P.; Hebbard, C.; Avraham, S.; Buckler, E.S.; Casstevens, T.; Hurwitz, B.; McCouch, S.; Ni, J.; Pujar, A.; et al. Gramene: A growing plant comparative genomics resource. Nucleic Acids Res. 2008, 36, D947-D953.
52. Eveland, A.L.; Satoh-Nagasawa, N.; Goldshmidt, A.; Meyer, S.; Beatty, M.; Sakai, H.; Ware, D.; Jackson, D. Digital gene expression signatures for maize development. Plant Physiol. 2010, 154, 1024-1039.
53. Fu, H.; Dooner, H.K. Intraspecific violation of genetic colinearity and its implications in maize. Proc. Natl. Acad. Sci. USA 2002, 99, 9573-9578.
54. Lai, J.; Li, R.; Xu, X.; Jin, W.; Xu, M.; Zhao, H.; Xiang, Z.; Song, W.; Ying, K.; Zhang, M.; et al. Genome-wide patterns of genetic variation among elite maize inbred lines. Nat. Genet. 2010, 42, 1027-1030.
55. Shen, Y.; Zhang, Y.; Chen, J.; Lin, H.; Zhao, M.; Peng, H.; Liu, L.; Yuan, G.; Zhang, S.; Zhang, Z.; et al. Genome expression profile analysis reveals important transcripts in maize roots responding to the stress of heavy metal Pb. Physiol. Plant. 2012, 147, 270-282.
56. Xiao, S.; Jia, J.; Mo, D.; Wang, Q.; Qin, L.; He, Z.; Zhao, X.; Huang, Y.; Li, A.; Yu, J.; et al. Understanding PRRSV infection in porcine lung based on genome-wide transcriptome response identified by deep sequencing. PLoS One 2010, 5, e11377.
57. Gibson, G.; Riley-Berger, R.; Harshman, L.; Kopp, A.; Vacha, S.; Nuzhdin, S.; Wayne, M. Extensive sex-specific nonadditivity of gene expression in Drosophila melanogaster. Genetics 2004, 167, 1791-1799.
58. Charlesworth, D.; Willis, J.H. The genetics of inbreeding depression. Nat. Rev. Genet. 2009, 10, 783-796.
59. Guo, M.; Rupe, M.A.; Zinselmeier, C.; Habben, J.; Bowen, B.A.; Smith, O.S. Allelic variation of gene expression in maize hybrids. Plant Cell 2004, 16, 1707-1716.
60. Birchler, J.A.; Riddle, N.C.; Auger, D.L.; Veitia, R.A. Dosage balance in gene regulation: Biological implications. Trends Genet. 2005, 21, 219-226.
61. Springer, N.M.; Stupar, R.M. Allelic variation and heterosis in maize: How do two halves make more than a whole? Genome Res. 2007, 17, 264-275.
62. Zhu, Y.; Fu, J.; Zhang, J.; Liu, T.; Jia, Z.; Wang, J.; Jin, Y.; Lian, Y.; Wang, M.; Zheng, J.; et al. Genome-wide analysis of gene expression profiles during ear development of maize. Plant Mol. Biol. 2009, 70, 63-77.
63. Qin, Y.F.; Fang, H.M.; Tian, Q.N.; Bao, Z.X.; Lu, P.; Zhao, J.M.; Mai, J.; Zhu, Z.Y.; Shu, L.L.; Zhao, L.; et al. Transcriptome profiling and digital gene expression by deep-sequencing in normal/regenerative tissues of planarian Dugesia japonica. Genomics 2011, 97, 364-371.
64. Mardis, E.R. The impact of next-generation sequencing technology on genetics. Trends Genet. 2008, 24, 133-141.
65. Livak, K.J.; Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method. Methods 2001, 25, 402-408.
66. C't Hoen, P.A.; Ariyurek, Y.; Thygesen, H.H.; Vreugdenhil, E.; Vossen, R.H.; de Menezes, R.X.; Boer, J.M.; van Ommen, G.J.B.; den Dunnen, J.T. Deep sequencing-based expression analysis shows major advances in robustness, resolution and inter-lab portability over five microarray platforms. Nucleic Acids Res. 2008, 36, e141.
67. Morrissy, A.S.; Morin, R.D.; Delaney, A.; Zeng, T.; McDonald, H.; Jones, S.; Zhao, Y.; Hirst, M.; Marra, M.A. Next-generation tag sequencing for cancer gene expression profiling. Genome Res. 2009, 19, 1825-1835.
68. Tatusov, R.L.; Fedorova, N.D.; Jackson, J.D.; Jacobs, A.R.; Kiryutin, B.; Koonin, E.V.; Krylov, D.M.; Mazumder, R.; Mekhedov, S.L.; Nikolskaya, A.N.; et al. The COG database: An updated version includes eukaryotes. BMC Bioinform. 2003, 4, 41.
69. Consortium, T.G.O. The gene ontology project in 2008. Nucleic Acids Res. 2008, 36, D440-D444.
70. Kanehisa, M. The KEGG Database. In "In Silico" Simulation of Biological Processes; John Wiley & Sons: Manhattan, NY, USA, 2008; pp. 91-103.
71. Marioni, J.C.; Mason, C.E.; Mane, S.M.; Stephens, M.; Gilad, Y. RNA-seq: An assessment of technical reproducibility and comparison with gene expression arrays. Genome Res. 2008, 18, 1509-1517.
72. Benjamini, Y.; Hochberg, Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc. B 1995, 57, 289-300.