Comparative transcriptional profiling of three super-hybrid rice combinations

International Journal of Molecular Sciences

Volumn 15, Issue 3, 2014, Pages 3799-3815

  Peng, Yonggang ^a   Wei, Gang ^a,b   Zhang, Lei ^a   Liu, Guozhen ^c   Wei, Xiaoli ^a   Zhu, Zhen ^a  

^a INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^b FUDAN UNIVERSITY   (China)

^c Chinese Academy of Sciences   (China)

Author keywords

Circadian clock; Heterosis; Photosynthesis; Rice; Transcriptional profiling

Indexed keywords

BETA FRUCTOFURANOSIDASE; BETA GLUCOSIDASE; CYTOCHROME P450; OLIGONUCLEOTIDE; PHOSPHORIBULOKINASE; PYRUVATE PHOSPHATE DIKINASE; CARBON DIOXIDE; VEGETABLE PROTEIN;

ARTICLE; CIRCADIAN RHYTHM; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE MAPPING; GENETIC DATABASE; GENOME IMPRINTING; GLYCOLYSIS; HETEROSIS; MICROARRAY ANALYSIS; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PHOTOSYNTHESIS; PLANT YIELD; QUANTITATIVE TRAIT LOCUS; RICE; RNA EXTRACTION; SUCROSE METABOLISM; CLUSTER ANALYSIS; COMPARATIVE STUDY; DNA MICROARRAY; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; GROWTH, DEVELOPMENT AND AGING; HYBRIDIZATION; METABOLISM; PLANT GENE; PROCEDURES; SIGNAL TRANSDUCTION;

CARBON DIOXIDE; CLUSTER ANALYSIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GENE REGULATORY NETWORKS; GENES, PLANT; HYBRID VIGOR; HYBRIDIZATION, GENETIC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ORYZA SATIVA; PLANT PROTEINS; QUANTITATIVE TRAIT LOCI; SIGNAL TRANSDUCTION;

EID: 84895495010     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms15033799     Document Type: Article

References (67)

1. Melchinger, A.E.; Gumber, R.K. Overview of Heterosis and Heterotic Groups in Agronomic Crops. In Concepts and Breeding of Heterosis in Crop Plants; Lamkey, K.R., Staub, J.E., Eds.; Crop Science Society of America: Madison, WI, USA, 1998; pp. 29-44.
2. Cheng, S.H.; Zhuang, J.Y.; Fan, Y.Y.; Du, J.H.; Cao, L.Y. Progress in research and development on hybrid rice: A super-domesticate in China. Ann. Bot. 2007, 100, 959-966.
3. Zhang, L.; Peng, Y.; Dong, Y.; Li, H.; Wang, W.; Zhu, Z. Progress of Genomics and Heterosis Studies in Hybrid Rice. In Polyploid and Hybrid Genomics; Chen, Z.J., Birchler, J.A., Eds.; John Wiley & Sons, Inc.: Oxford, UK, 2013; pp. 117-135.
4. Birchler, J.A.; Auger, D.L.; Riddle, N.C. In search of the molecular basis of heterosis. Plant Cell 2003, 15, 2236-2239.
5. Semel, Y.; Nissenbaum, J.; Menda, N.; Zinder, M.; Krieger, U.; Issman, N.; Pleban, T.; Lippman, Z.; Gur, A.; Zamir, D. Overdominant quantitative trait loci for yield and fitness in tomato. Proc. Natl. Acad. Sci. USA 2006, 103, 12981-12986.
6. Birchler, J.A. Reflections on studies of gene expression in aneuploids. Biochem. J. 2010, 426, 119-123.
7. Bruce, A.B. The Mendelian theory of heredity and the augmentation of vigor. Science 1910, 32, 627-628.
8. Jones, D.F. Dominance of linked factors as a means of accounting for heterosis. Genetics 1917, 2, 466-479.
9. Shull, G.H. The composition of a field of maize. Am. Breed. Assoc. Rep. 1908, 4, 296-301.
10. East, E.M. Heterosis. Genetics 1936, 21, 375-397.
11. Yu, S.B.; Li, J.X.; Xu, C.G.; Tan, Y.F.; Gao, Y.J.; Li, X.H.; Zhang, Q.; Saghai Maroof, M.A. Importance of epistasis as the genetic basis of heterosis in an elite rice hybrid. Proc. Natl. Acad. Sci. USA 1997, 94, 9226-9231.
12. Hochholdinger, F.; Hoecker, N. Towards the molecular basis of heterosis. Trends Plant Sci. 2007, 12, 427-432.
13. Schnable, P.S.; Springer, N.M. Progress toward understanding heterosis in crop plants. Annu. Rev. Plant Biol. 2013, 64, 71-88.
14. Krieger, U.; Lippman, Z.B.; Zamir, D. The flowering gene SINGLE FLOWER TRUSS drives heterosis for yield in tomato. Nat. Genet. 2010, 42, 459-463.
15. Bao, J.; Lee, S.; Chen, C.; Zhang, X.; Zhang, Y.; Liu, S.; Clark, T.; Wang, J.; Cao, M.; Yang, H.; et al. Serial analysis of gene expression study of a hybrid rice strain (LYP9) and its parental cultivars. Plant Physiol. 2005, 138, 1216-1231.
16. 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.
17. Song, S.; Qu, H.; Chen, C.; Hu, S.; Yu, J. Differential gene expression in an elite hybrid rice cultivar (Oryza sativa, L.) and its parental lines based on SAGE data. BMC Plant Biol. 2007, 7, 49.
18. 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.
19. 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.
20. 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.
21. 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.
22. 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.
23. Ni, Z.; Sun, Q.; Liu, Z.; Wu, L.; Wang, X. Identification of a hybrid-specific expressed gene encoding novel RNA-binding protein in wheat seedling leaves using differential display of mRNA. Mol. Gen. Genet. 2000, 263, 934-938.
24. Wu, L.M.; Ni, Z.F.; Meng, F.R.; Lin, Z.; Sun, Q.X. Cloning and characterization of leaf cDNAs that are differentially expressed between wheat hybrids and their parents. Mol. Genet. Genomics 2003, 270, 281-286.
25. Yao, Y.; Ni, Z.; Zhang, Y.; Chen, Y.; Ding, Y.; Han, Z.; Liu, Z.; Sun, Q. Identification of differentially expressed genes in leaf and root between wheat hybrid and its parental inbreds using PCR-based cDNA subtraction. Plant Mol. Biol. 2005, 58, 367-384.
26. 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.
27. 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.
28. Ge, X.; Chen, W.; Song, S.; Wang, W.; Hu, S.; Yu, J. Transcriptomic profiling of mature embryo from an elite super-hybrid rice LYP9 and its parental lines. BMC Plant Biol. 2008, 8, 114.
29. Flint-Garcia, S.A.; Buckler, E.S.; Tiffin, P.; Ersoz, E.; Springer, N.M. Heterosis is prevalent for multiple traits in diverse maize germplasm. PLoS One 2009, 4, e7433.
30. 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.
31. China Rice Data Center. Available online: http://www.ricedata.cn (accessed on 24 January 2014).
32. 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.
33. Law, P.J.; Claudel-Renard, C.; Joubert, F.; Louw, A.I.; Berger, D.K. MADIBA: A web server toolkit for biological interpretation of Plasmodium and plant gene clusters. BMC Genomics 2008, 9, 105.
34. Bar-Even, A.; Noor, E.; Lewis, N.E.; Milo, R. Design and analysis of synthetic carbon fixation pathways. Proc. Natl. Acad. Sci. USA 2010, 107, 8889-8894.
35. Fujimoto, R.; Taylor, J.M.; Shirasawa, S.; Peacock, W.J.; Dennis, E.S. Heterosis of Arabidopsis hybrids between C24 and Col is associated with increased photosynthesis capacity. Proc. Natl. Acad. Sci. USA 2012, 109, 7109-7114.
36. Li, J.; Ou-Lee, T.M.; Raba, R.; Amundson, R.G.; Last, R.L. Arabidopsis flavonoid mutants are hypersensitive to UV-B irradiation. Plant cell 1993, 5, 171-179.
37. Bieza, K.; Lois, R. An Arabidopsis mutant tolerant to lethal ultraviolet-B levels shows constitutively elevated accumulation of flavonoids and other phenolics. Plant Physiol. 2001, 126, 1105-1115.
38. Peer, W.A.; Murphy, A.S. Flavonoids and auxin transport: Modulators or regulators? Trends Plant Sci. 2007, 12, 556-563.
39. Korn, M.; Peterek, S.; Mock, H.P.; Heyer, A.G.; Hincha, D.K. Heterosis in the freezing tolerance, and sugar and flavonoid contents of crosses between Arabidopsis thaliana accessions of widely varying freezing tolerance. Plant Cell Environ. 2008, 31, 813-827.
40. Shen, H.; He, H.; Li, J.; Chen, W.; Wang, X.; Guo, L.; Peng, Z.; He, G.; Zhong, S.; Qi, Y.; et al. Genome-wide analysis of DNA methylation and gene expression changes in two Arabidopsis ecotypes and their reciprocal hybrids. Plant Cell 2012, 24, 875-892.
41. Barabasi, A.L.; Oltvai, Z.N. Network biology: Understanding the cell's functional organization. Nat. Rev. Genet. 2004, 5, 101-113.
42. Nikitin, A.; Egorov, S.; Daraselia, N.; Mazo, I. Pathway studio-The analysis and navigation of molecular networks. Bioinformatics 2003, 19, 2155-2157.
43. Farre, E.M.; Harmer, S.L.; Harmon, F.G.; Yanovsky, M.J.; Kay, S.A. Overlapping and distinct roles of PRR7 and PRR9 in the Arabidopsis circadian clock. Curr. Biol. 2005, 15, 47-54.
44. Nakamichi, N.; Kiba, T.; Henriques, R.; Mizuno, T.; Chua, N.H.; Sakakibara, H. Pseudo-response regulators 9, 7, and 5 are transcriptional repressors in the Arabidopsis circadian clock. Plant Cell 2010, 22, 594-605.
45. Dalchau, N.; Baek, S.J.; Briggs, H.M.; Robertson, F.C.; Dodd, A.N.; Gardner, M.J.; Stancombe, M.A.; Haydon, M.J.; Stan, G.B.; Goncalves, J.M.; et al. The circadian oscillator gene GIGANTEA mediates a long-term response of the Arabidopsis thaliana circadian clock to sucrose. Proc. Natl. Acad. Sci. USA 2011, 108, 5104-5109.
46. Mizoguchi, T.; Wheatley, K.; Hanzawa, Y.; Wright, L.; Mizoguchi, M.; Song, H.R.; Carre, I.A.; Coupland, G. LHY and CCA1 are partially redundant genes required to maintain circadian rhythms in Arabidopsis. Dev. Cell 2002, 2, 629-641.
47. Murakami, M.; Tago, Y.; Yamashino, T.; Mizuno, T. Comparative overviews of clock-associated genes of Arabidopsis thaliana and Oryza sativa. Plant Cell Physiol. 2007, 48, 110-121.
48. Yu, J.W.; Rubio, V.; Lee, N.Y.; Bai, S.; Lee, S.Y.; Kim, S.S.; Liu, L.; Zhang, Y.; Irigoyen, M.L.; Sullivan, J.A.; et al. COP1 and ELF3 control circadian function and photoperiodic flowering by regulating GI stability. Mol. Cell 2008, 32, 617-630.
49. Fornara, F.; Panigrahi, K.C.; Gissot, L.; Sauerbrunn, N.; Ruhl, M.; Jarillo, J.A.; Coupland, G. Arabidopsis DOF transcription factors act redundantly to reduce CONSTANS expression and are essential for a photoperiodic flowering response. Dev. Cell 2009, 17, 75-86.
50. Kim, W.Y.; Fujiwara, S.; Suh, S.S.; Kim, J.; Kim, Y.; Han, L.; David, K.; Putterill, J.; Nam, H.G.; Somers, D.E. ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light. Nature 2007, 449, 356-360.
51. Harmer, S.L. The circadian system in higher plants. Ann. Rev. Plant Biol. 2009, 60, 357-377.
52. Yakir, E.; Hilman, D.; Harir, Y.; Green, R.M. Regulation of output from the plant circadian clock. FEBS J. 2007, 274, 335-345.
53. Graf, A.; Schlereth, A.; Stitt, M.; Smith, A.M. Circadian control of carbohydrate availability for growth in Arabidopsis plants at night. Proc. Natl. Acad. Sci. USA 2010, 107, 9458-9463.
54. 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.
55. Youens-Clark, K.; Buckler, E.; Casstevens, T.; Chen, C.; DeClerck, G.; Derwent, P.; Dharmawardhana, P.; Jaiswal, P.; Kersey, P.; Karthikeyan, A.S. Gramene database in 2010: Updates and extensions. Nucleic Acids Res. 2011, 39, D1085-D1094.
56. Wang, E.; Wang, J.; Zhu, X.; Hao, W.; Wang, L.; Li, Q.; Zhang, L.; He, W.; Lu, B.; Lin, H.; et al. Control of rice grain-filling and yield by a gene with a potential signature of domestication. Nat. Genet. 2008, 40, 1370-1374.
57. Xing, Y.; Zhang, Q. Genetic and molecular bases of rice yield. Ann. Rev. Plant Biol. 2010, 61, 421-442.
58. Yu, J.; Hu, S.; Wang, J.; Wong, G.K.; Li, S.; Liu, B.; Deng, Y.; Dai, L.; Zhou, Y.; Zhang, X.; et al. A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 2002, 296, 79-92.
59. Yu, J.; Wang, J.; Lin, W.; Li, S.; Li, H.; Zhou, J.; Ni, P.; Dong, W.; Hu, S.; Zeng, C.; et al. The genomes of Oryza sativa: A history of duplications. PLoS Biol. 2005, 3, e38.
60. Ma, L.; Chen, C.; Liu, X.; Jiao, Y.; Su, N.; Li, L.; Wang, X.; Cao, M.; Sun, N.; Zhang, X.; et al. A microarray analysis of the rice transcriptome and its comparison to Arabidopsis. Genome Res. 2005, 15, 1274-1283.
61. Eisen, M.B.; Brown, P.O. DNA arrays for analysis of gene expression. Methods Enzymol. 1999, 303, 179-205.
62. Bachem, C.W.B.; Oomen, R.J.F.J.; Visser, R.G.F. Transcript imaging with cDNA-AFLP: A step-by-step protocol. Plant Mol. Biol. Rep. 1998, 16, 157-157.
63. Ma, L.; Gao, Y.; Qu, L.; Chen, Z.; Li, J.; Zhao, H.; Deng, X.W. Genomic evidence for COP1 as a repressor of light-regulated gene expression and development in Arabidopsis. Plant Cell 2002, 14, 2383-2398.
64. Ma, L.; Li, J.; Qu, L.; Hager, J.; Chen, Z.; Zhao, H.; Deng, X.W. Light control of Arabidopsis development entails coordinated regulation of genome expression and cellular pathways. Plant Cell 2001, 13, 2589-2607.
65. Altschul, S.F.; Gish, W.; Miller, W.; Myers, E.W.; Lipman, D.J. Basic local alignment search tool. J. Mol. Biol. 1990, 215, 403-410.
66. Altschul, S.F.; Madden, T.L.; Schaffer, A.A.; Zhang, J.; Zhang, Z.; Miller, W.; Lipman, D.J. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 1997, 25, 3389-3402.
67. Maglott, D.; Ostell, J.; Pruitt, K.D.; Tatusova, T. Entrez gene: Gene-centered information at NCBI. Nucleic Acids. Res. 2011, 39, D52-D57.